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PREFACE
Oneofthemajorbasicproblemsofpsychologyandbiologyistheeffectofheredityuponbehavior;yetinthe1930'sandearly1940'sresearchinthisareahadalmostcompletelygoneoutofstyle.Atthattimeitwaspossibletocountonthefingersofonehandthepersonswhohaddonesignificantresearchinthefield.Tryonhaddoneanextensiveexperimentonheredityandmazerunninginrats,followedupbyimportantstudiesfromhisstudents,HallandSearle.Dawsonhadbeguntoworkwithbehaviorindogs,buthisprojectwasterminatedbytheoutbreakofwar.
Inthehumanarea,interestintheThirtieswaslargelyconfinedtoasomewhatsterilecontroversyovertheextenttowhichIQscorescouldbemodifiedbyspecialtraining,althoughThurstoneandStrandskovhadbecomeinterestedinapplyingthetechniqueoffactorialanalysistoproblemsofbehaviorgenetics.AmongmostscientiststherehadbeenarevulsionagainsttheexaggeratedclaimsoftheearlyeugenicistsandtheracistdoctrinesofNaziGermany,anditwasnotinfrequentlystatedthatheredityhadnoeffectuponhumanbehavior.
ItwasagainstthisgeneralbackgroundthatDr.AlanGregg,thenDirectorfortheMedicalSciencesattheRockefellerFoundation,wenttolunchwithDr.C.C.Little,thedirectorandfounderoftheJacksonLaboratory,andexpressedtheopinionthatpsychiatristsandsociologistswerepayingtoolittleattentiontothefactorofheredityasitaffectedbehavior.Dr.Little'simaginationcaughtfire,andtheoutcomewasatentativearrangementforalong-rangeproject,laterknownas"GeneticsandtheSocialBehaviorofMammals."
Theresultsofthatprojectarenowsummarizedinthisbook,whichisprimarilyanaccountofanexperimentlastingsomethirteenyearsandinvolvingintensiveandextensivemeasurementsonthebehaviorofhundredsofpurebredandhybriddogs,studiedfrombirthtooneyear.Astheexperimentprogressed,weweremoreandmoreimpressedwiththedevelopmentalapproachtotheproblemofthegeneticsofbehavior,andmuchofourworkispresentedfromthatviewpoint.Inaddition,wehaveanalyzedthegeneticresultsbymostoftheconventionalstatisticalmethodsandhavedevelopedcertainnewonesaswell.Finally,wehaveshownhowtheseresultsrelatetothegeneralproblemsofhumanandanimalbehavior.
Aswellaspresentingourownwork,wehavecollectedagreatdealof
Aswellaspresentingourownwork,wehavecollectedagreatdealofbackgroundinformationontheoriginandnatureofgeneticdiversityindogs.Thebookasawholeisthereforeasourceofgeneralinformationonbehaviorofdogsandshouldbeofinteresttodogownersandbreedersaswellastheoreticalscientists.
Thisis,naturally,notthelastwordonthesubject.Ourworkhasraisedasmanynewquestionsasithasansweredoldones,andwepresentourfindingstodateinthehopethattheymayprovideabackgroundformuchneededfuturework.Onethingwhichhasimpressedusisthatthedog,forallitseightthousandyearsorsoofassociationwithhumanbeings,isstillinmanyrespectsascientificallyunknownanimal.Despitethehundredsofpapersthathavebeenpublishedaboutthisanimal,therearevastareasofinformationwhicharestillunexplored.Withthemoregeneroussupportnowavailableforresearch,itshouldeventuallybepossibletoknowinsteadofmerelyspeculateaboutthenatureofman'sbestfriend.
Whilethisexperimenthasbeengoingon,muchprogresshasbeenmadeelsewhereandinmanyscientificdisciplines.Manyworkershavecontributedtotherevivalofinterestintheproblemofgeneticsandbehavior,inparticulartheethologistsundertheleadershipofTinbergenandLorenz,whosestudiesofinstincthavereformulatedthequestionofgeneticdifferencesbetweenspecies.Inotherfields,symposiaonbehaviorgeneticshavebeenheldatthetwo1963InternationalCongressesofgeneticsandpsychology.ArecentpresidentialaddressoftheAmericanPsvchologicalAssociationwasdevotedtothesubjectofgeneticsandschizophrenia.AcommitteeonbehaviorgeneticshasbeensetupbytheSocialScienceResearchCouncil.AtasymposiumoftheAmericanPsychiatricSociety(publishedafterwardasavolumeentitledRootsofBehavior)one-fourthotthepapersweredirectlyconcernedwithbehaviorgenetics,
PREFACEvH
andeightofthethirty-oneauthorshadsomedirectassociationwiththeJacksonLaboratory.
IfAlanGreggwerealivetoday,wethinkthathewouldbepleasedwiththeresults.
J.P.Scott
J.L.Fuller
J.L.Fuller
ACKNOWLEDGMENTS
Thepronoun"we"isuseddeliberatelyinthisbook,notonlybecauseithastwoauthors,butinrecognitionofthecontributionsmadebyournumerousco-laborersontheproject.
Weparticularlywishtorecognizetheeffortsofourresearchassistants,onwhomtheaccuracyandintegrityofthedatasolargelydepended.Manyofthemhavesincegoneontoadvancedtrainingandhavebecomeindependentinvestigators.WeareespeciallyindebtedtoMargaretCharlesHigginsandEdnaDuBuisfortheirlongperiodsofservice,andtoC.L.Brace,OrvilleElliot,AlbertPawlowski,andJosephRoycefortheircontributionstodataanalysis.Otherswhomadecontributionsoverthe13-yearspanoftheprojectwereDuaneBlume,MarianBurns,JohnCraig,Jr.,DonaldDickerson,ClariceEasier,AlanE.Fisher,PriscillaHinch-cliffe,DavidKing,NancyM.King,MonaMeltzer,RobertPettie,MaxineSchnitzer,JoyceSprague,MaryE.Smith,andElizabethWilliams.
Wewerefortunateinhavingoverthewholeperiodmuchthesamegroupofgeneralassistants,onwhomauniformsystemofcarefortheanimalsdepended.WeespeciallythankFrankClark,GordonGilbert,SheldonIngalls,PearlMcFarland,andDanReynolds.
Manyscientificinvestigatorsmadenotablecontributions.C.C.Little,thentheDirectoroftheJacksonLaboratory,acquiredthefoundationstocksandworkedoutthecolorgeneticsofthebreeds;C.S.HallandW.T.Jamesgaveadviceandhelpedorganizetheproject;B.E.GinsburgandShermanRosscontributedmuchaslongtimeVisitingInvestigators.Othercolleaguesandassociatestoonumeroustomentionherehelpedwithencouragementandcounsel.
xACKNOWLEDGMENTS
MajorfinancialsupportwasgivenbytheRockefellerFoundationovera13-yearperiodduringwhichthebasicdataweregathered.ContinuingsupportenablingtheprocessingofthedataandwritingthisbookwasprovidedbytheFordFoundationandbytheNationalInstitutesofHealth(GrantsMH01775andMH04481).
Certainfiguresandtableshavebeenpreviouslypublishedinthefollowingbooksandjournals:TheConceptofDevelopment(UniversityofMinnesotaPress,
andjournals:TheConceptofDevelopment(UniversityofMinnesotaPress,1957),JournalofComparativeandPhysiologicalPsychology,AnimalBehaviour,JournalofHeredity,AmericanZoologist,MonographsoftheSocietyforResearchinChildDevelopment,Science,JournalofGeneticPsychology,PsychosomaticMedicine,andAnnalsoftheNewYorkAcademyofSciences.Permissiontoreproducethismaterialisherebyacknowledged.
CONTENTS
PartIVGENERALIMPLICATIONS
15.IMPLICATIONSFORTHEARTOFDOGBREEDING/383
16.THEEVOLUTIONOFDOGSANDMEN/397
17.TOWARDASCIENCEOFSOCIALGENETICS/413
BIBLIOGRAPHY/435AUTHORINDEX/449SUBJECTINDEX/452
PLATESfollowingpage176
Thefivepurebreeds
Outsiderunsandnurseryroominterior
TheBehaviorLaboratoryandstaff
Breedingstock(cockerspaniels)andFjhybrids
Breedingstock(basenjis)andFxhybrids
Litterfrombackcrosstocockerspaniel
Litterfrombackcrosstobasenji
BCSF2litter
CSBF2litter
AboriginaldogsofAfrica,Iraq,andAustralia
EarlyEnglishlandspanielsandhounds
Forcedtraining
Rewardtraining
Problem-solving:detourandmanipulationtests
Problem-solving:detourandmanipulationtests
MazetestandT-mazeanddelayed-responsetest
Trailingandspatial-orientationtests
FIGURES
1.1BasicMendeliancross/9
1.2Floorplanofnurseryroom/25
1.3Floorplanofall-weatherdogkennel/27
2.1GeographicaldistributionofwildmembersofgenusCanis/32
2.2Centersofdomesticationandadaptiveradiation/36
2.3Skullwidthacrosscheekbonesasrelatedtoskulllength/40
2.4Greatestwidthofupperjawrelativetoskulllength/41
2.5Sizeofmolarteethrelativetoskulllength/41
2.6Relativebreadthofupperjawinfivemodernbreeds/44
4.1Rateofdistressvocalizationduringfirst4weeks/92
4.2Developmentofwalkingandplayfulfighting/95
4.3Developmentofmotorabilityduringtransitionperiod/96
4.4Developmentoflearningcapacitiesduringneonatalandtransitionperiods/98
4.5Changeinresponsetoconditioningbetweentransitionandsocializationperiods/99
4.6Developmentofdistressvocalizationofbeaglepuppiesunder2conditionsofisolation/103
5.1Developmentoftheheartrate/121
5.2Effectofsocializationatdifferentagesuponavoidanceofanactivehandler/125
5.3Timingmechanismslimitingtheprocessofsocialization/126
5.4Performanceintheleash-controltest/127
tivLISTOFILLUSTRATIONS
5.5Eatingduringtheleash-controltest/128
5.6Avoidanceandvocalizationinresponsetohandling/134
5.7Avoidanceandfearfulbehaviorinresponsetohandling/135
5.8Agonisticbehavior(playfulfighting)inresponsetohandling/136
5.9Attractionandfollowinginresponsetohandling/138
5.10Et-epimeleticbehaviorandsocialinvestigationinresponsetohandling/138
6.1Percentageofoccurrenceofcompletedominanceinpurebredlitters/157
6.2Occurrenceoffightsorone-sidedattacksduringdominancetests/158
6.3Occurrenceofcompletedominanceinmale-femalepairs/160-62
6.4Declineofnursingbehaviorbymothersduringtheneonatalperiod/170
6.5Averagetimespentwithhandlerduringthefollowingtest/175
7.1Distributionofrunningtimes/188
7.2Distributionofmotivation-speedscores/189
8.1Totalreactivityratingsforthefivepurebreeds/198
9.1Proportionofanimalsratedasquietduringweighing/206
9.2Typesofdemeritsgivenduringleash-controltest/209
9.3Leveloftrainingonsuccessivedaysofobediencetest/213
9.4Meantimescoresongoal-orientationtest/217
9.5Proportionofanimalssucceedingoneachtrialofthemotor-skilltest/220
10.1Problemsinthebarriertest/227
10.2Resultsofthemanipulationtestonsuccessivedays/231
10.3Floorplanofthemazetest,left-handpattern/233
10.4Learningcurves:errorsinmazetest/235
10.5Learningcurves:timesofsolutionofmazetest/235
10.6Relativeperformanceofdifferentbreedsinthemaze/238
10.7T-mazeusedforcue-response,discrimination,anddelayed-responsetests/239
10.8Speedscoresincue-responsetest/240
10.9Apparatususedintheopatial-orientationtest/248
10.10Breedscoresonthespatial-orientationtest/252
10.11Individualerrorscoresonthespatial-orientationtest/252
10.12Inter-trialandintraclasscorrelationsinthespatial-orientationtest/255
11.1Distributionofscoresforplayfulfightingat13-15weeks/270
11.2Theoccurrenceofplayfulfightingtransformedtoascaleofthreshholdofstimulation/272
11.3Occurrenceofbarkingduringdominancetestsatdifferentages275
11.4Distributionofbarkingtoexcessinpurebreedsandhybridsat11weeks/277
I1.5Monthinwhichbreedingbeganinrelatedcockerspaniels/280
I1.5Monthinwhichbreedingbeganinrelatedcockerspaniels/280
1l.nIntervalsbetweenfirsttwoestrusperiods/281
11.7Proportionolcockersandbasenjisratedascompletelvquietduring
weighing2881isDevelopmentanddifferentiationofposturalresponses/289-9012.1Meanscoresofhybridsohsixmeasuresofleashtraining/300L2.2Meanmotivationspeedscoresofhybrids/307
Vttainmenlbyhybridsofcriterioninthecue-responsetest/308
12.4Attainmentbyhvbridsofcriterioninthedelayed-responsetest/310
12.5Meanscoresofhybridsontheobediencetest/311
12.6Meantotalreactivityscoresofhybridsat17,34,and51weeks/312
12.7Meanscoresofhybridsontworeactivitytestmeasures/314
12.8Proportionofeachhybridgroupratedas"high"intailwaggingat17,34,and51weeks/315
12.9Meancorrectchoicesscoresofhvbridsonthespatial-orientationtest/318
12.10Meanpersistencescoresofhybridsonthespatial-orientationtest/319
12.11Meanadjustedspeedscoresofhvbridsonthespatial-orientationtest/320
13.1Absoluteweightgainperweekinmalepuppiesofthelargestandsmallestbreeds/327
13.2Combinedgrowthcurveforbasenjimales/328
13.3Maleandfemalegrowthcurvesinbasenjisandcockerspaniels/330
13.4Growthcurvesofthefivepurebreeds/331
13.5Inheritanceofhairlength/335
13.6Distributionofdifferencesinstaninesbetweenlongandshort-coatedanimalsinrelationto34behavioralvariables/337
13.7Relativephvsicalproportionsofcockerspanielsandbasenjis/340
17.1Functionaldifferentiationofformduringgrowth/421
17.2Functionaldifferentiationofbehaviorinrelationtothephysicalenvironment/421
17.3Functionaldifferentiationofasocialrelationship/422
1.1Masterlistofexperimentalanimals/10
1.2Scheduleoffeeding,cleaning,anddiseaseprevention/14
1.3Scheduleofobservations,training,andtesting/24
2.1Averageskullmeasurementsofdifferentbreedsofdogs/43
2.2Ratiosofskullmeasurementstolengthofskull/44
2.3Coefficientsofinbreedingoffoundationstock/49
2.4HybridsreportedbetweenspeciesofthegenusCanis/53
3.1BehavioralsvstemsandknownbehavioralpatternsinthefamilyCanidae/63-65
4.1Timeofcompleteopeningoftheeye/90
4.2Timeoffirstfunctionoftheear/94
4.3Timeoferuptionofuppercanineteeth/96
4.4Timeofdevelopmentofallelomimeticbehavior/106
4.5Occurrenceofsexualbehaviorin160purebredpuppies(0-16weeksofage)/107
4.6Naturalperiodsofdevelopmentindogandman/114
5.1Estimatedvariationindevelopmentaleventsassociatedwiththebeginningoftheperiodsoftransitionandsocialization/120
5.2Relativeadjustmentofpuppiesat1yearofage/123
5.3Rankorderofpuppiesontestsgivenafter14weeksofage/128
5.4Developmentoftailwagging/139
6.1Socialrelationshipsofdogandman/153
6.2Effectofsizeondominance-subordinationrelationships/164
6.3Percentageofcompletedominanceinbasenjis,cockers,andtheirhvbridsat15weeks/166
6.4Occurrenceofmothersnursingpuppiesunder2weeksofage171
6.5Occurrenceofretrieving1-week-oldpuppiesbvpurebredandhvbridmothers/172
7.1Conversiontable—originalscoretostanine/189
7.2Simplifiedinterpretationofanalysisofvarianceinbreedcomparisonexperiment/192
8.1Specificresponseratings/197
8.2"Resting"heartrate/199
8.3Changeinheartrateduringquieting/199
8.4Meanstaninescoresoffivepurebreedsontenbehavioralandfourheartratemeasuresatthreeages/200
8.5Percentageofsubjectsexceedingarbitrarythresholdsoneightmeasuresinreactivitytest/202
9.1Meannumberofdemeritsinleashtraining/208
[ntercorrelarjonsoftypesofdemeritsduringleashtraining/2109.3Typesofdemeritsinearly,middle,andlatephasesofleash-controltest
211()1Meanstaninescoresonobedienceforpurebreeds/214
9.5Rankfivepurebreedsunderforcedtraining/215
9.6Correlationsbetweentestsofforcedtraining/216
9.7Percentageofanimalssuccessfullytrainedinretrievingtest/219
9.8Over-allperformanceonmotor-skilltest/221
10.1Performanceofthedifferentbreedsonthedetourtest—firsttrialsonly
229
10.2Percentageoftotalvarianceofmazescoresrelatedtobreed,mating,litter,andbackgroundvariables/236
10.3Attainmentofcriterionincue-responsetest/241
10.4Delaved-responseperformanceoffivepurebreeds/243
10.5Animalsshowingperfectperformanceonthefinaltrialofthetrailingtest/246
10.6Relativeranksofbreedsonperformanceonmostdifficulttrialoftrailingtest/246
10.7Distributionoffearreactionsintrailingtest/247
10.8Comparisonsbetweenpurebreedsonspatial-orientationscores/251
10.9Analysisofvarianceofspatial-orientationmeasures/253
10.10Ranksofthedifferentbreedsinvariousproblem-solvingtests/258
11.1ModificationsoftheCastle-Wrightformulafortheanalysisofquantitativeinheritance/264
11.2Theoreticalratiosforthedifferencesbetweenbackcrosses,F/s,andF2'scomparedtothedifferencebetweenparentalstrains/266
11.3Scoresforavoidanceandfearfulvocalizationat5weeksofageinresponsetoahumanhandler/267
11.4Tendencytobiteandjerktheleash/269
11.5Percentofanimalsbarkingperopportunity,comparedwithexpectedpercentage/276
11.6Percentofanimalsbarking19orfewertimesat11weeks/276
11.7Testsinvolvingpersistentdifferencesbetweenmaternallines/285
11.8Distributionofadultweightmeasurementsinbasenjis,cockers,andtheirhybrids/286
11.9Distributionofaverageheartrates,11-16weeks/287
12.1Leash-trainingdemeritsofhybrids/299
12.2Within-littervarianceofthefightingscoreofleashtraining/301
12.3Analysisofvariance—leash-fightingscoresofhybridsbymatingsandlitters/302
12.4Leash-controlfightingscore—offspringofF:siresbydifferentdams/302
12.5Leash-controlfightingscore—offspringofpurebreddamsbydifferentsires/303
12.6Analysisofvariance—fightingscoreinleashtraining/304
12.7Leash-controlvocalizationscore—offspringofsiresbydifferentdams/306
12.8Leash-controlvocalizationscore—offspringofdamsbydifferentsires/306
12.9Discriminationorcueresponse—analysisofvarianceofhybridperformance/309
12.10Analysisofvariance—totalreactivityscoresofhybrids/316
12.11Totalreactivityratings:meansofmatingsofpurebreddamsbypurebredsiresandFjsires/317
12.12MatingsofF^siresbypurebredandF^dams/317
xviiiLISTOFTABLES
13.1Percentageofadultweightreachedat16weeksofage/329
13.2Breedrankinbodymeasurementsrelativetoweight/342
13.3Significantcorrelationsbetweenphysicalmeasurementsandbehavioralvariablesinpurebreedsandhybrids/345
13.4FactorloadingsofphysicalvariablesinthecombinedF2population/346
13.5Factorloadingsoffactor1(generalsize)incombinedpurebreeds/348
13.6Factorloadingsoffactor1(generalsize)inShetlandsheepdogsandfoxterriers/349
14.1Compositionofcombinedpopulations/357
14.2Numberofvariablesinwhichthecombinedvarianceofsegregatingpopulationsexceedsthatofnon-segregatingpopulations/358
14.3Proportionofvarianceattributabletopopulationdifferences/360-61
14.4VariancecomponentsofeachselectedbackcrossandF2population/365
14.5MeanvariancecomponentsinvariablesshowingdifferencesbetweenthebackcrosseswithaP<.01/366
14.6Factor2(activity-success)inthecombinedF2generation/372
14.7Factor3(heart-rate)inthecombinedF2generation/372
14.8Factor2(reactivity)inthecombinedF1hybrids/374
14.9Correlationsofpoorperformanceonthetrailingtestwithperformanceinothertestsintwohybridpopulations/374
14.10CommonvarianceintrailingtestasindicatedbycorrelationwithperformanceinT-maze/377
16.1Mortalityrateper100birthsinpurebreedsandhybrids/40617.1Subdivisionsofgenetics/413
Subdivisionsofgenetics/413
THEDEVELOPMENT
OFBASIC
BEHAVIOR
PATTERNS
ASCHOOLFORDOGS
Formanyyearswehavehadpsychologistsandzoologistsworkingsidebysideinourbehaviorlaboratories.Whenwefirstbroughtthemtogether,weoftengotstereotypedreactionstoanynewdiscoveryinthefieldofbehavior.Azoologistwouldsay,"Whatawonderfulexampleofinstinct,"andapsychologistwouldcounter,"My,whataremarkableexampleoflearning!"Thishappenedoverandoveragainintheearlystagesofourwork,anditillustratestheconfusionwhichonceexisted,andmaystillpersist,regardingtheroleofheredityinrelationtobehavior.
Inthemoreremotepast,scientistssuchasJohnB.Watsontooktheviewthatheredityhadlittleimportanceandthatthebehaviorofahumaninfantcouldbemoldedinanydirectionbylearning.Others,followingSigmundFreud,heldthathumanbehaviorwasdeeplyrootedininstinctswhosesuppressioncouldresultinseriousmentaldisorders.Thevastmajorityofpsychologists,psychiatrists,andotherpracticalworkersinthefieldofhumanbehaviorhadnodefiniteinformationabouteithertherapidlydevelopingscienceofgeneticsorthewaysinwhichgeneticvariationcouldaffectbehaviordirectly.Norwastheclinicalobservationofhumanbehaviormuchhelp.True,manychildrenrearedinpoorfamilybackgroundslaterdevelopedinadequateandmaladjustedbehavior,butsomeofthemwereapparentlyunaffected,andstillothersworkedharderthanmostpeopletocompensatefortheirearlyexperience.Wastheirabilitytoriseaboveenvironmentduetoheredityortosomeunknowndifferenceinearly
aboveenvironmentduetoheredityortosomeunknowndifferenceinearlyexperience?
Thequestion"Whatdoeshereditydotobehavior?"isthereforeabasicone,boththeoreticallyandpractically.Therearemanydif-
BEHAVIORPATTERNS
ferentwaysoftryingtoanswerit.Onecaneithermakecomparisonsbetweenasmanyaspossibleofthemillionorsospeciesofanimalsintheworldorconcentrateonone,aswedid.Scientistsworkingwithbirdshavediscoveredmanystereotypedbehaviorpatternswhicharelargelyorganizedandgovernedbyheredity.Weourselveschoseamammal,partlybecausemammalsaremorecloselyrelatedtohumanbeingsthanarebirds,andpartlybecausethejobhadnotyetbeendone.Amongmammals,wechosethedogbecauseitshowsoneofthebasichereditarycharacteristicsofhumanbehavior:ahighdegreeofindividualvariability.Wereasonedthatiftherewereanyanimalmostlikelytoshowimportanteffectsofheredityonbehavior,itwasthedog,andthattheseeffectscouldbeassumedtobeatleastsomewhatsimilartothosewhichappearinhumanbeings.
Toputthisinmoreenthusiasticterms,thedogisaveritablegeneticgoldmine.Besidestheenormousdifferencesbetweenbreeds,allsortsofindividualdifferencesappearatthestrokeofthegeneticist'spickaxe,inthiscasethetechniqueofmatingtwocloselyrelatedanimals.Anyonewhowishestounderstandahumanbehaviortraitorhereditarydiseasecanusuallyfindthecorrespondingconditionindogswithverylittleeffort.Dogsaretimidorconfident,peacefuloraggressive,andmaybebornwithundershotjaws,clubfeet,orhemophilia(Dawson,1937;Burns,1952;Fuller,1960).
Althoughitistruethatadogisalarge,long-lived,andrelativelyexpensiveanimaltokeep,itisagooddealsmaller,shorter-lived,andlessexpensivethansomeothermammals.Dogsbreedmorerapidlythanprimatesoreventhecommonherdanimals,exceptforpigs.Dogscanpassthroughonecompletegenerationwithinayear.Amaturefemalecontinuestoreproduceforfivetosevenyears,bearingheryoungabouttwiceayearinlittersaveragingfourorfiveanimals.Nevertheless,itrequiresverycarefulplanningtogetthemaximumamountofinformationfromanexperimentwithdogs,andoneinitialmistakecanruinyearsofeffort.
Therefore,beforeourworkhadgonebeyondtheearlyplanningstage,weasked
Therefore,beforeourworkhadgonebeyondtheearlyplanningstage,weaskedanumberofleadinggeneticistsandpsychologistsintheUnitedStatestoattendaresearchplanningconferenceatBarHarbor.Manyofthesemenandwomenweredoingrelatedresearch,eitheronanimalsoronpeople.ThechairmanwasDr.RobertM.Yerkes,oneofthepioneerworkersonheredityandbehavior,thefounderoftheYerkesLaboratoryofPrimateBiology,andatthattimetherecognizeddeanofanimalbehavioristsintheUnitedStates.Equallydistinguishedworkersmadeuptherestof
SCHOOLFORDOGS5
thegroup.Dr.FrankBeachservedassecretary,organizingtheproceedingsintoacoherentwhole.ForthreedayswemetwiththemonMountDesertIslandanddiscussedthedirectionwhichtheresearchshouldtake.Muchofourfinalplanresultedfromthisconference(ScottandBeach,1947).
Atthestartwehadcertainguidingprinciplesandsignpostsderivedfromwhathadbeendiscoveredaboutotheraspectsofheredity.Weknewthatbehavioritselfisnotinherited.Infact,theonlythingswhicharebiologicallyinheritedfromtheparentsaretheeggandsperm.Wealsoknewthatthebasicfactorsofheredityaregenes,whicharenothingmorethanlargeorganicmoleculesarrangedinlargerbodiescalledchromosomes.Eventheseareonlypartsofthenucleusofalivingcell.Thegenesthemselvescanactonlybycontrollingthesynthesisofproteins,someofwhich,theenzymes,modifyotherchemicalorphysiologicalreactions,usuallyinthecellsthemselves.Allthisisalongwayfromtheactivityofawholeorganism,orbehavior,andtheconcretefactofwhetheradogbitesyouorwagsitstail.
Oneoftheprimaryquestionswehadtoanswerwaswhetherhereditycouldproduceanimportanteffectuponbehaviorinahigheranimalorwhetheritsimplysetthestageforbehavioralactivitywhichwasthenguidedandmoldedbyothercauses.Thequestionmakesagreatdealofsenseinrelationtotheconceptoflevelsoforganization(seeTable17.1).Hereditystandsatthemostbasiclevel,andthereforewecanassumeittobeveryimportant.Butassumptionsareonlythebeginningofscientificinquiry,andthequestionstillremains,Whatexactlycanafactoroperatingonalowleveloforganizationdotoaphenomenonoperatingonahigherlevel?Forbehaviorisprimarilyaphenomenonexistingontheor-ganismicorpsychologicallevel(Wright,1953).
Atthesametimewerealizedthatwecouldnotneglectfactorsoperatingonstill
Atthesametimewerealizedthatwecouldnotneglectfactorsoperatingonstillotherlevels.Amajortrendinanimalbehaviorresearchinthelastthirtyyearshasbeentodemonstratetheimportanceoftheeffectsofsocialorganizationuponbehavior.Theactivityofanindividualisunderstandableonlyintermsofhisrelationshipstothemembersofalargergroup.Ourworkwasthereforedesignedinrelationtolevelsoforganizationandcanbesodescribed.
Inaddition,wehadthesuccessesandmistakesofourpredecessorstoguideus.ProfessorTryon(1930-41,1963)ofthePsychologyDepartmentoftheUniversityofCaliforniahadpreviouslydoneextensiveandmeticulousresearchonheredityandbehaviorinrats.
BEHAVIORPATTERNS
Hedevisedamechanicalmazeoperatinginsuchawaythattheexperimentercouldnotinfluencetheresultsconsciouslyorunconsciouslyandselecteddifferentstrainsofratsfromthosewhichlearnedthemazemostquicklyorslowly.Thesedifferencespersistedforgenerationaftergeneration,indicatingthathereditycouldproduceanimportanteffectuponbehavior.Itappearedthatselectionhadaffectedintelligencealone,butwhenastudentofhis,Searle(1949),testedtheseratsondifferentsortsofmazes,hecametotheconclusionthatoneoftheprincipalreasonswhythetwostrainsofratsdifferedinperformancewasthattheslowrunningor"dull"ratswereafraidofthemechanicalmaze.Insteadofselectingpurelyforintellectualability,Tryonhadalsoselectedforadifferenceinemotionalreaction.
C.S.Hall(1941)hadshownbyhisselectionexperimentsonthedefecationratesofratstakenfromtheircagesandplacedinanopenspacethathereditycouldalteranotherkindofemotionality.Hiswork,andthatofSearle,suggestedthatemotionalcapacitieswerehighlyvariableandcouldproduceimportanteffectsuponperformance.Fromthesepreviousexperimentsweknewthathereditaryemotionaldifferencesmighthaveimportanteffectsonbehaviorwhichatfirstglancedidnotappeartobeemotional.Wealsorealizedthatwithsuchalong-livedandexpensiveanimalasthedog,wewouldseldombeabletoduplicateourexperiments.Inotherwords,therewouldbeverylittlegoingbacktotakeasecondlook.Wewouldhavetomeasureasmanyimportantcharacteristicsaswecouldwhiletheexperimentwasinprogress.
Besidestheworkonotheranimals,therehadbeenanearliermajorattempttoworkwithheredityindogs.ThelateProfessorC.R.StockardoftheCornellUniversityMedicalSchoolhadbegunwiththeidea(apromisingoneatthetime)
UniversityMedicalSchoolhadbegunwiththeidea(apromisingoneatthetime)thatmanyofthedifferencesbetweenbreedsofdogswerecausedbyhereditarydisordersintheductlessglands(1941).Hedid,indeed,findbreeddifferencesintheendocrineglands,butanatomicalpeculiaritiesinthesamebreeds,suchasdwarfismandshortleggedness,turnedoutnottobecausedbyglandsbutbyhereditaryfactorsworkinginotherways.ProfessorStockarddiedbeforehecouldchangetheprojecttoallowforthis.SincehisoriginalexperimentwasnotdesignedtotestaMendelianhypothesis,theresultswereinconclusive,andwedecidedtosetupourexperimentinthebroadestpossibleway,realizingthatwecouldnotpredicttheimportantresultsinadvanceandthatitwechosetoonarrowanapproachwemightendwithnoth-
SCHOOLFORDOGS7
ing.Bothfromthisviewpointandthesimplestatisticsoflifeinsurancetables,weknewitwasimperativethatthisprojectbeacooperativeventure,notaone-manshow,andinthisbookweshalltrytorecognizetheinnumerablecontributionsmadebyco-operatorsandco-workersintheyearscoveredbytheexperiment.
Ourover-allexperimentaldesignwastosystematicallyvarythegeneticconstitutionofthedogswhilekeepingallotherfactorsasconstantaspossible.Thedependentvariablewasbehavior,butsincebehavioroccursonlyinreactiontostimulation,wehadnotonlytheproblemofdesigningauniformsystemoftestsituationswhichwouldmeasurethedog'sreactionstospecifiedchangesinhissocialandphysicalenvironment,butalsothatofkeepingallotherenvironmentalfactorsasconstantaspossible.Equallyimportantwasthetaskofkeepingthedog'sinternalenvironmentconstantbyseeingthateachanimalwasadequatelynourishedandfreeofdisease.
GENETICMETHODS
Choiceofbreeds.—Geneticvariationwastheprimaryvariableinourexperiment:thesupposedcausewhichmightormightnotaffectbehavior.Wethereforedividedtheexperimentintotwophases.Inthefirstwemadeasurveyofthedifferentdogbreedsinordertoselectthosewhichshowedthebiggestbehavioraldifferences.ThankstotheenergyofDr.C.C.Little,wehadawidevarietyfromwhichtochoose,rangingfromtheGreatPyrenees,awhitedogroughlyresemblingaSaintBernard,tothetinyChihuahuas.Wesooneliminatedtheabnormalsizesatbothendsofthescale,realizingthatthelargebreedsweretooexpensiveforlongexperimentsandthatthetoyordwarfbreedswere
tooexpensiveforlongexperimentsandthatthetoyordwarfbreedswereunsuitablebecauseoftheirlowfertility.Furthermore,ifwechosedogsofapproximatelythesamesize,wecouldusethesameapparatusforall.
Certainbreedswerediscardedearly.BothdachshundsandScottishterriershaveareputationforbeingstubbornandself-willed,butthosewestudiedsnowednotraceofthisaspuppies,beinguniformlyfriendlyanddemonstrativeanimals,notunlikebeaglesandcockersinthisrespect.Wewouldobviouslyhavetowaittoolongforthebehavioralpeculiaritiesofthesebreedstodevelop.
Wefurtherdecidedtoconcentrateonbreedswithnormalphysique.Althoughitistruethattheshortleggednessofthedachshund,forexample,hasaneffectuponitsbehavior,thisdoesnotrequire
8BEHAVIORPATTERNS
anelaboratescientificexperimentforproof.Wepreferredtoworkwiththemoresubtleandperhapsmoreimportantwaysinwhichheredityaffectsbehavior.
Wefinallyselectedfivebreedsforintensivestudy:basenjis,beagles,Americancockerspaniels,Shetlandsheepdogs(shelties),andwire-hairedfoxterriers.Asitturnedout,thesewererepresentativesofthemajorgroupsofdogsasrecognizedbydogbreedersandomittedonlythetoyandnon-sportingbreeds.
Inthefirstphaseintheexperiment,wedevelopedourtestsandraisedallfivebreedsinthesameenvironment,measuringtheirsimilaritiesanddifferences.Wealsostudiedthedevelopmentoftheirbehaviorbymakingdailyobservationsfrombirthupto16weeksofage.Whereverpossible,wecross-fosteredpuppiesbetweenthebreedsinanefforttoseewhetherthematernalenvironmentaswellasbiologicalhereditywasaffectingbehavior.Wealsoexperimentedwithanevenmoredrasticshiftinthesocialenvironmentbytakingcertainpuppiesoutofthekennelsandrearingtheminhomes.Thisnotonlygaveusachancetostudytheeffectofmaternalenvironment,buttoseewhetherornotourkennel-reareddogswerereasonablynormalcomparedtodogsrearedoutside.Unfortunately,wewereabletodothisonlyonaveryfewanimals,partlybecauseofthelimitednumberoffriendsandfellowworkersonwhomwecouldimpose,andpartlybecauseofthedangerofdiseasetransmission.Anticipatingalittle,wecansaythatGyp,thebasenji;George,thebeagle;andSilver,theShetlandsheepdog,didnotdostrikinglybetterorworseonmostofthetests,althoughtheydevelopedverydifferentrelationshipswithdogsandpeople.
AMendeliancross.—ThesecondphaseoftheexperimentwastomakeaMendeliancrossbetweentwoofthebreeds(Fig.1.1).PreliminaryresultsindicatedthattheAmericancockerspanielandtheAfricanbasenjishowedagreatmanydifferencesinbehavior.Ontheonehandwehadagentleandpamperedhousepetdescendedfrombirddogs,andontheotherabreedwhichhadrecentlycomefromtherough-and-tumbleconditionsofAfricanvillagelife.Furthermore,therewasgoodevidencethatthebasenjis,havingbeenfirstbroughtoverfromAfricain1937,hadneverbeencrossedwiththeEuropeanbreeds,whereasthecocker(aswellastheotherthree)hadoriginallycomefromtheBritishIsles,wheretherehadbeenabundantopportunityforcrossinginthepastandconsiderablehistoricalevidencethatthishadactuallytakenplace.Thesetwobreedshadbeenmadegeneticallydifferentbyisolationaswellasbyselection.
SCHOOLFORDOGS9
Wedidnotattempttoaccentuatethedifferencesbetweenthebreedsbyfurtherselection,asthiswouldhavebeenaten-yearprograminitself.Instead,wedecidedtorelyontheselectionwhichthepracticaldogbreedershadalreadydoneoveraperiodofcenturies.Thisselection,however,hasnotproducedcompleteuniformity.Inmostcasesthebreedstandardspermitconsiderablevariation,eveninsuchobviouscharacteristicsascolor,andwehadalreadyfoundthattherewasagreatdealofvariationbetweenbothindividualsandstrainswithinthepurebreeds.Inordertolimitthiskindofvariation,wedecidedtomakeallourcrossesfromtheoffspringofasinglepairofanimalsineachbreed.Thiswouldlimitthegeneticvariabilityintheparentstothatwhichhadexistedinasinglebrother-sisterpairratherthanthatwhichwascharacteristic
CS?,CockerSpanielXBA<?,BasenjiCSa*,CockerSpaniel,XBA$,Basenji
L
-X—BCSF,<?XBCSR?CSB?XCSB<?~X'
11II
BCSXCSBCSF2CSBF2CSBXBA
BACKCROSSTOCOCKERBACKCROSSTOBASENJI
BCSCROSSCSBCROSS
Fig.1.1.—DiagramofMendeliancrosswithsymbolsusedfordifferentgeneticpopulations.Thebasicplanwastorepeateachofthetwocrosseswithfourmatingsandobtaintwolittersfromeachmating.Becauseofdeathsamongthecockerspanielfemales,replicationwascompletedonlythreetimesintheBCScross(seeTable1.1).
oftheentirebreed.Wewereabletocarryoutthisplansuccessfullywiththebasenjis,butinthecaseofthecockerswewerenotabletoobtainenoughmalesfromasinglematingattherighttimeandhadtomodifyourplanslightlybyusingasourfoundationstockanimalsfromtwocloselyrelatedmatingsinwhichthesamemalewasmatedtohissisterandmother.
Inordertocontrolforthepossibleeffectsofthematernalenvironmentandalsotodemonstratesex-linkedinheritanceifitshouldexist,wemadereciprocalcrosses.Theidealplanwastomatefourbasenjimaleswithfourcockerfemalesandviceversa.ThiswouldgiveustwoFipopulations,onefromcockermothersandonefrombasenjimothers.Thenwetookafirstgenerationmalefromeachmatingandcrossedhimbacktohismother.Inthiswaywecouldcomparetwosetsofoffspringofthesamemother.Inthebackcross
BEHAVIORPATTERNS
groupweexpectedthatthegeneswouldbeassortingandrecombin-ingindifferentcombinationsaccordingtothelawsofMendelianinheritance,whereasintheFigenerationallanimalswouldreceivethesameinheritanceandbemuchlessvariable.ThenwetookthesameFimalesandmatedthemtotheirsistersinordertoproduceanF2generationinwhichthemaximumgeneticvariabilitywould
occur.
Weanticipatedthatwewouldbeabletostudytheeffectsofhereditychieflyfromthevariabilityofbehavior,andwethereforeplannedtoraiseatleasttwenty-fivetothirtyanimalsineachpopulation,thisbeingthesmallestnumberinwhichareasonablyaccuratesampleofapopulationdistributedinanormal
inwhichareasonablyaccuratesampleofapopulationdistributedinanormalcurvecanbeobtained.Thesearenotlargenumbersforgeneticdata;ifwehadbeenworkingwithfruitflies,forexample,wewouldhavepreferredtoobtainatleastahundredineachgroup.Therefore,wemadeanefforttogetanunusuallylargenumberofF2*s,themostcrucialpopulationforalltypesofgeneticanalysis.Furthermore,weplannedtoobtainatleasttwolittersofpuppiesfromeachmating,sothatwecouldcomparevariationinsiblingswhichwerelittermatesandsiblingswhichwerenot.
table1.1MasterListofExperimentalAnimals*andKeytoBreeds
BreedorHybrid,andSymbol
Basenji(BAorB)
Beagle(BEA)
Cockerspaniel(CS)
ShetlandsheepdogorSheltie(SH)
Wire-hairedfoxterrier(\VH)
F,BAd"XCS9(BCS)
F.CSd"XBA9(CSB)
BackcrosstoCS(BCSXCS)
BackcrosstoBA(CSBXB)
F2fromBCS(BCSXBCS)
F2fromCSB(CSBXCSB)
All
•Includesallanimalsuponwhichsomeexperimentalworkwasdoneandwhichlivedatleastto16weeks.
Thedatacouldbeanalyzedinanumberofways.Analysisofvariancewouldmeasurethechangesinvariationproducedbygeneticsegregation,by
measurethechangesinvariationproducedbygeneticsegregation,bydifferencesintheenvironmentproducedbydifferentmothers,andbytheaccidentofbeingbornatdifferenttimestothesamemother.Correlationalanalysiswouldrevealthe
extenttowhichcloserelativesresembledeachother,aswellastheresemblancebetweendifferentkindsofbehavioraltests.Inaddition,wecouldanalyzetheeffectofphysicaltraitsonbehaviorbycalculatingthecorrelationsbetweenbodymeasurementsandpsychologicalmeasurements.Wecouldalsodeterminewhetherornottheexternalcolorfactorswereassociatedwithbehavioraldifferences.Forexample,theownersofcockershaveoftenallegedthattheredsandblackshavedifferenttemperaments.
Lookingbackontheexperiment,wenowseehowwemighthaveorganizeditinabetterfashion.Weshouldhaveallowedforalargernumberofsparematings,asaccidentsanddeathswilloccureveninthebestregulatedlaboratories.Inaddition,wehadplannedtheexperimentwiththeanticipationthatmostofthetraitswouldshowmultiple-factorinheritance.Surprisingly,wefoundthatmanyofthebreeddifferencescouldbeexplainedintermsofsimpleone-andtwo-factorinheritance.Ifwehadtheexperimenttodoagain,wewouldemphasizethebackcrosses,makingasecondbackcrosstothepurebreedsineachcase,thisbeingacriticaltestforsingle-factorinheritance.WealsofoundthatourFifemalesbecamemuchsuperiormotherscomparedtothepurebredanimals,producinglargequantitiesofmilkandgivingexcellentcaretotheiroffspring,sothattheF2'shadabetterstartinlife.ThesegeneticandenvironmentaladvantagesoftheFi'sandF2'sarereflectedindecreasedmortality(Table16.1).Itwouldhavebeeninterestingtohavemadeback-crossestothepurebreedsfromtheFifemalesaswellasfromthemalesinordertodeterminetheeffectofsuperiorearlyenvironmentonthesamegenetictypes.
Stillanotherunanticipatedresultwasthelargeamountofvariationbetweenlitters.Littermatestendtobealike,and,inananimalwhichrearsitsyounginlitters,thebestunitofthepopulationisnottheindividualbutthelitter.Itwouldhavebeendesirabletohavehadmorelittersthanwedid.However,allthiswouldprobablyhavetakentwenty-fiveorthirtyyearstocompleteinsteadofthirteen.
THEINTERNALENVIRONMENT:CONTROLOFNUTRITIONANDDISEASE
Feeding.—Sincegeneticswasourchiefexperimentalvariable,weattemptedto
Feeding.—Sincegeneticswasourchiefexperimentalvariable,weattemptedtokeepphysiologicalfactorsasconstantaspossible.Oneoftheseisthestateofnutrition,and,aswehaveseen,thisispartlydependentuponthemotherandhenceuponherheredity.Therewasnowayinwhichwecouldforcethemotherstoproduceaconstant
12BEHAVIORPATTERNS
amountofmilk,butinallotherwayswecouldprovideauniformdiet.
Whenwebegantheexperimentin1945,meatsofanykindweredecidedlyvariableinsupply.However,onepreparedanimalfoodwithaguaranteedconstantformulawasreadilyavailable.ThisfoodwasPurinaLaboratoryChow,andwedecidedtomakeitthebasiciteminthediet,keepingitconstantlyavailableinametalfeeder.Itwasnotaperfectfoodfordogs,asithadbeendevelopedasanall-purposelaboratoryfoodforrats,mice,guineapigs,andmonkeysaswellasdogs.Itcontainedmoreroughageandlessfatthanwasideallysuitablefordogs.Itproved,however,tobeanintrinsicallysounddiet,asourexperimentalanimalsdevelopedintohealthyandvigorousadultswitheveryindicationthattheirgrowthwasequaltonormalbreedstandardsorbetter(seeChap.13).
Theyoungpuppiesandnursingmothershadtohavesupplementaryfood,andthiswaskeptassimpleaspossible.Onenaturalfoodwhichisextraordinarilyconstantincompositionismilk,andthiswastheprincipalsupplement.Weusedcannedmilkatfirst,butlaterswitchedtopowderedwholemilkbecauseofitslowercost.Tothisweaddedavitaminsupplement,Abbott'sHaliverMalt,inordertoprovideasourceofvitaminsAandD,whicharethosemostlikelytobelostfromtheagingofdrypreparedfoods.WealsohadavailableatalltimesforthepuppiesandmothersdryPurinaKibbledMeal,mostofwhichwasafinepowderwhichtheyoungpuppiesbegantoeatassoonastheywereable.ThisfooddidnothavethestandardizedformulaoftheLaboratoryChowbutwasdesignedprimarilyasadogfoodandwassuperiortoitinthatrespect.
Thedogsconsequentlyhadbeforethemaconstantsupplyofdryfoodwhichtheycouldeatatanytime.Thisreducedthelaborofcaringfortheanimalsbutalsohadanotherpurpose.Wewishedtoraisethepuppiesinnaturalsocialgroupsandkeptthemtogetherintheirlittersratherthanrearingthemasisolatedindividuals.Ifallowedtocompeteforfood,asfrequentlyhappenswithdishesofmeatorwetmash,unequalnutritionwouldsoonresult.Asitturnedout,puppiesinalitterdidnotcompeteforthemilk,asdogsneverappeartofightforaliquid,
inalitterdidnotcompeteforthemilk,asdogsneverappeartofightforaliquid,andtheyrarelyshowedanydispositiontoquarreloverthedryfood.Inanycase,nodogcouldkeepguardoverthedryfoodeveryminuteofthedayinalargepen.
Inmanypsychologicalexperimentsweusedafoodreward,asmallspoonfulofcannedherringhavingastrongfishyflavorsimilartosardines.Thedogsseemedtorelishthesetidbits,andtheamountstakenwerenotlargeenoughtodisturbtheirnutrition.
Sanitation.—Oursecondconcernwastokeeptheanimalshealthyandfreefromdiseaseatalltimes.Thefirstproblemwassanitation.Manykennelsmaintaintheirdogsonbarefloorsandwashthesedaily.However,thismeansthatthefloorsareconstantlywet,dogsandattendantsfrequentlystepinfeces,andthereisaconstantstrongodor.Sinceourexperimentalcrewhadtoworkwiththedogsinthepens,wehadtoconsiderthecomfortofboth.Wedecidedtocoverthefloorsofthepenswithwoodshavingswhichabsorbmoisturefromurineandfeces.Thisproducedsweet-smellingroomsinwhichbothdogsandattendantscouldeasilykeepthemselvesclean.Feceswerepickeduponceadayaftertheanimalswerefed,leavingtheroomrelativelycleanfortherestoftheday.This,ofcourse,didnotsubstituteforthoroughcleaning,whichnecessitatedmovingthedogsfromthepens,removingtheshavings,andsteam-cleaningthefloorsandwalls.Wewishedtoavoiddisturbingpuppiesatcriticaltimesofdevelopmentandatthesametimetogivethemalluniformtreatment.Thepenswerethereforethoroughlycleanedonceeveryfourweeksafterthepuppieswereborn.Thissystemwasacompromisebetweencompletesanitationandpsychologicaldisturbance,butworkedreasonablywell.
Diseasecontrol.—Themostcommondangerousdiseaseforyoungpuppiesiscausedbyintestinalroundwormswhichcanmakeayoungpuppyseriouslyillorevenkillhim.Itisalmostimpossibletoabolishtheseparasitescompletely,astheycanbepassedalongtothepuppiesbythemotherevenbeforebirth.Wethereforesetuparoutinesystemofworming(seeTable1.2)forallpuppies,whetherornottheywereinfected,sothateverypuppywouldhavethesametypeofexperienceandthesamechancesforgoodhealth.Wormingwascorrelatedwiththecleaningschedule,sothatpuppieswerewormedat4and8weeks,beforebeingputbackintoacleanpen,andagainat16weeks,whentheyweretransferredtoanewpen.
Cleaningandhealthactivitieswerethusorganizedarounda4-weekunit,and
Cleaningandhealthactivitieswerethusorganizedarounda4-weekunit,andthisscheduleresultedinthedevelopmentofa4-weekmoduleforplanningthesocialexperienceofthepuppies.Thiswaslateramplifiedandextendedinthepsychologicaltestingprocedure.
Thesecondmajorthreattohealthwascaninedistemper.Thisisahighlyinfectious,airbornediseasewhichattackstherespiratoryandnervoussystemandproduces50-or60-percentfatalities,whileexposingeventhesurvivorstoalingeringillnessandprolongedconvalescence.Itspreventionissoimportantthatinthisonerespectwedeliberatelydepartedfromouridealofuniformconditions
14BEHAVIORPATTERNS
TABLE1.2ScheduleofFeeding,Cleaning,andDiseasePreventionforPuppies
Age(weeks)
Food
Cleaning
DiseasePrevention*
45678
91011121314151617-52
Mother'sMilkonlyuntil3weeks
Cow'sMilk&HaliverMalt,KibbledMeal,LaboratoryChowadded
Motherremoved
LaboratoryChowonly
Dailycleaning(continuedthrough52weeks)
Steamcleaning
Steamcleaning
Steamcleaning
SteamcleaningDailycleaningonly(movedtooutsiderun)
Worming,Spratt'sCapsules
Worming,N-butylchlorideAnti-distemperserum
Anti-distemperserum
Killeddistempervirus
Livedistempervirus
Worming,N-butylchloride
Latermodified.Seetext.
throughouttheentirecourseoftheexperiment.Atthetimewestarted,thebestsystemofpreventionconsistedofaseriesofthreeinjections,twoweeksapart.Thefirsttwoinjectionsconsistedofakilledviruswhichproducedapartialimmunity.Inthefinalone,thelivevirusproducedapermanentimmunity.Althoughnodogsdiedafterthistreatment,manyofthembecameillfromtheinjectionofthelivevirus,andthisinterferedwiththeirbehavioraltests.Wethereforeabandonedtheuseofthelivevirus.InthemeantimetheLederleCompanyhaddevelopedanavianizedlivevirus,oneinjectionofwhichcouldproducepermanentimmunitywithoutanysignsofillness,andweswitchedtothissystem.Bothmethodswereputtoanactualtestbytheaccidentalintroductionofadogwithlatentdistemperintothecolony.Everyanimalwhichwasnotcompletelyprotectedcamedownwiththedisease,includingmostofthosedogswhichhadreceivedonlytheinjectionsofthekilledvirusandaFewotchosewhichhadbeenprotectedbysingleinjectionsofavianized\irus.Allresearchcametoastandstillforsixmonthswhilethediseasewasbroughtundercontrol.Asaresultofthisexperience,anewsystemwassetup.Beginningat8weeksofage,thetimewhen
mostpuppiesbegintolosetheimmunityacquiredbvnursingfromimmunemothers(Bakeretal,1959),thepuppiesweregiventemporaryimmunitythroughseruminjectionsandatthesametimegiventheavianizedvaccine.Twoweekslaterthevaccinewasreinjected,incasethefirstdidnottake.Thewholecolonyofadultswasreinjectedeven'twoyearsoroftenerinordertomaintainimmunity,withcompletelyeffectiveresultsthroughouttherestoftheexperiment.Thissupersafesystemcouldnothavebeencarriedoutwithoutthe
experiment.Thissupersafesystemcouldnothavebeencarriedoutwithouttheco-operationoftheLederleCompany,whichgenerouslycontributedthenecessaryveterinarysupplies.
Anotherhighlyfataldiseaseindogsisinfectioushepatitis.Itisspreadthroughurineratherthanairandhencedoesnotdiffuseasrapidlyasdistemper.However,itprovidesarealthreattoadogcolonybecauseanindividualwhichrecoversmaybeacarrierandkeepspreadingthediseaseforyearsafterward.Injectionsofthekilledvirusresponsibleforthisdiseasewerelateraddedtothedistemperinjections,providingimmunityforapproximatelysixmonths.Thishadtobemaintainedbyrepeatedinjections.Atthepresenttimeapermanenttypeofvaccinecombinedwiththedistempervaccineisavailableandisusedinourcolonv.
Tomakesurethatreasonablyuniformphysiologicalconditionswerebeingmaintainedforthepuppies,weweighedthemonceaweek,beginningatbirthandcontinuingthrough16weeks.Inayounganimal,continuedgrowthisthebestindicationofgoodhealth,andfailuretogainisoftenthefirstindicationthatallisnotwell.Inaddition,wecountedtheheartrateswithastethoscope.Thismeasureturnedouttobeanimportantindicationofprobablesurvivalinnewbornpuppies.Thosewithaslowheartrateusuallydidnotsurvivemorethanadayorso.Theheartratealsobecameanimportantindirectmeasureofbehavioraldevelopment,beingstronglycorrelatedwithmajorchangesinbehavior.Theweeklyweighings,besidesfunctioningasacheckonhealth,gaveusanopportunitytomakevariousbehavioralobservationsupondevelopmentandtomakesurethatthepuppiesweretrulynormalintheirsensoryandmotorcapacities.
THEOBSERVATIONOFDEVELOPMENT
Fromtheveryfirstitwasobviousthatourpuppieswerechangingfromdaytodayandweektoweek,andthatwhiletheheredityofasinglepuppyremainedconstant,itwasactinguponaverydifferentanimalatbirththanafewweekslater.Wethereforebeganregular
16BEHAVIORPATTERNS
dailyobservationsofourpuppies,startingatbirthandcontinuingupto16weeksofage,hopingtoobservetheveryearliestmanifestationsofhereditarydifferences.Wealsohopedthatwemightinthiswayseetheactionofhereditypureandundefiled,beforeitbecamecontaminatedwiththeeffectsof
pureandundefiled,beforeitbecamecontaminatedwiththeeffectsofexperience.
Themethodwassimple.Eachdayatrainedobserverwatchedthepuppiesfor10minutesthroughthewindowsofthenurseryroomsandwrotedowneverythingtheydid.Onthebasisofourfirstobservations,wecompiledachecklistonwhichtheearliestappearanceofvariousbehaviorpatternscouldberecorded.Duringthefirsttwoweeksafterthebirthofalitter,theobserverwentintothepenandsatquietlybythenestboxinordertoseethepuppiesmoreclosely.Afterthistime,whentheeyeswereopenandthepuppieswerelikelytorespondtotheobserver,theobservationsweremadefromoutsidetheroom.Observationswerealwaysmadeinthemorning,closetothetimewhenthemotherswerebeingfedandthepenscleaned,asthiswasthetimewhenthepuppieswerelikelytobemostactive.Atothertimesoftheday,theentirelittermightbeasleepduringthewhole10-minuteperiod.Afterthepuppieshadbecome10weeksoldandweremuchmoreactiveandshowedfewerchangesfromdaytoday,theobservationperiodwasreducedto5minutes,duringwhichtimeasmuchormoreactivitycouldberecordedasbefore.
Theresultswerequiteunexpectedbutscientificallyexciting.Duringtheveryearlystagesofdevelopmenttherewassolittlebehaviorobservedthattherewaslittleopportunityforgeneticdifferencestobeexpressed.Whenthecomplexpatternsofbehaviordidappear,theydidnotshowpureanduncontaminatedeffectsofheredity.Instead,theywereextraordinarilyvariablewithinanindividualandsurprisinglysimilarbetweenindividuals.Inshort,theevidencesupportedtheconclusionthatgeneticdifferencesinbehaviordonotappearallatonceearlyindevelopment,tobemodifiedbylaterexperience,butarethemselvesdevelopedundertheinfluenceofenvironmentalfactorsandmayappearinfullfloweronlyrelativelylateinlife.
Morethanthis,wesoonrealizedthatweweredealingwitharemarkableseriesofdevelopmentalchanges;thatthepuppycomesintotheworldnotasasimplifiedversionofanadultbutasananimalhighlyadaptedtoaninfantileexistence,andthathelaterundergoesatransformationinbehaviorwhichisalmostasspectacularasthemetamorphosisofthetadpoleintoafrog.
Thustheconceptofdevelopmentbecameaveryimportantonein
interpretingourresults,bothinrelationtothedevelopmentofsocialrelationshipsandinrespecttotheincreaseincapacityforpsychologicalperformance.Theconceptofdevelopmentalchangetowardincreasing
performance.Theconceptofdevelopmentalchangetowardincreasingcomplexityoforganizationtiestogethertheactionofthemanyfactorswhichaffectbehavioronalllevelsoforganization.Forexample,geneticsdoesnotactinstantaneouslybutmustworkthroughphysiologyoverlongperiodsoftimeinordertoaffectbehavior.Likewise,apuppyisbornwithoutexperienceoftheoutsideworld,andhisbehaviorisorganizedandreorganizedinrelationtothesocialandphysicalenvironmentsthroughouthislifetime.Allthesefactorscontinuallyacttogetheranduponeachothertoproducethecapacitytoreacteffectivelytoeachnewenvironmentalsituationthroughoutlife.
THESOCIALENVIRONMENT:TESTSOFSOCIALBEHAVIOR
Controllingthesocialenvironment.—Ourobservationsofdevelopmenthadshownusthatthe4-weekmoduledidnotcoincidewithimportantchangesinsocialdevelopment.Amajorchangeinbehaviortakesplaceatabout3weeksofage,whenthesenseorgansfirstbecomecompletelyfunctionalandthepuppybeginstoformitsprimarysocialrelationshipsandtoeatsolidfood.Anotherbasicsocialchangeisweaning,whichmayoccurnaturallyasearlyas7weeks.Wedecidedtokeepthemotherswiththepuppiesuntil10weekssothattheseparationwouldnotcoincidewiththecleaningandfeedingschedule.
Wealsohadtodecidewhentomovethepuppiestothelargeoutdoorpens.Wechose16weeks,primarilybecausethiswasatimewhenallthepuppiesweresufficientlydevelopedphysicallytobeabletostandthechangetooutdoorconditionsatanytimeofyear.Fromsomeotherviewpoints,thiswasnotanidealtime.Manyofthedogswerejustgettingtheirsecondteethandmayhavehadsomedifficultyinhandlingsolidfood.Laterobservationsonpuppiesraisedinlargeone-acrepensindicatedthattheystayedveryclosetothekennelor"den"untilabout12weeksofage,afterwhichtheybegantowandermorewidely.TheexperienceofC.J.Pfaffenberger(1963)withguidedogsindicatedthatpuppieskeptinkennelsbeyond14weeksalreadybegintoshowtheusualdeleteriouseffectsofprolongedkennelrearing:timidityandlackofconfidence.Theidealtimetomovethepuppiesoutdoorswouldprobablyhavebeenbetween12and14weeks.However,sinceallanimalsweretreated
18BEHAVIORPATTERNS
alikeinthisrespect,thelaterdatedidnotaffectthebehavioralcomparisons.
Afewexceptionsweremadetothisplan.Whenfemalescameintoestrusbefore
Afewexceptionsweremadetothisplan.Whenfemalescameintoestrusbeforeayearofage,theyweretemporarilyremovedfromtheirlittersandhousedtogetherinaseparatepen.Inthefoxterrierlitters,groupattacksoncertainindividualsmadeitnecessarytoremovethevictims.Sometimesthelitterwasdivided,andinothercasesasingleanimalwastransferredtoagroupofmorepeacefulanimalsofthesameagebutadifferentbreed.
Testsofsocialrelationships.—Duringthefirstfewweeksthepuppiesstayedwiththeirmotherandlittermatesintheirnurseryrooms.Onceadaythecaretakercameintofeedandwaterthemotherandtocleantheroom.Onceaweekapairofexperimenterscameinfortheweeklyweighing.Otherwisethepuppieshadnocontactwithhumanbeings.Whentheyreached5weeksofage,wefirstbegantodevelopandmeasuretheirsocialrelationships.Thefirstprocedurewasahandlingtest,inwhichwedidallthesortsofthingswhichpeopleusuallydotoyoungpuppiesandnotedtheirreactionsonachecklist.Thistestwasgiveneverytwoweeksfrom5through15weeks,andonceagainatayear.
Asinglepairofexperimentersworkedwiththepuppiesupto16weeksofage.Thesewerealwaysamanandagirl,sothatthepuppieswouldhaveexperiencewithbothsexesandanopportunitytoshowdifferentialreactionstothem.Asecondpairofexperimenterswasaddedafter16weeks,butmanytestswerestillgivenbythefirstpair,sothateachlitterhadcontactwiththesameindividualsthroughouttheirtests.
Whenthepuppiesreached5weeks,webegantestingforthedevelopmentofsocialrelationshipsbetweenthepuppiesthemselves.Herewechoseonlyoneaspectofsuchrelationships,thatofdominanceandsubordination.Webeganpreparingforitat2weeksofagebyplacingabonebeforeallthepuppiesinthepen.Thiswasdoneonceaweekthereafter.At5weeksofage,thepuppieswerepairedineverypossiblecombinationwithinthelitterandallowedtocompetefortheboneoveraperiodof10minutes.Thiswasrepeatedat11and15weeks,andagainatoneyear.Apuppywasnotallowedtocompetemorethantwiceonthesameday.Thismeantthatthetesttookthegreaterpartofaweek,involvingagreatdealofhandlingandcontactwiththehumanexperimentersintheprocess.Italsomeantthatthelargerlittersobtainedmorecontactthanthoseinasmalllitter.Tims,ineachdominancetest,apuppy
inalitterof6wouldbehandled5times,whereasoneinalitterof4wouldbehandledonly3times.
THEPSYCHOLOGICALLEVEL:MEASURINGBEHAVIOR
Onthephysiologicalandsociallevels,ourchiefconcernwastokeepconditionsconstantsothatanydifferencesmightbecausedprincipallybygenetics.Whenwecametopsychologicalprocessessuchastheeffectoflearningandexperienceuponbehavior,wecarriedoutthesameprincipleforthefirstfewweeksoflife,interferingwiththepuppiesaslittleaspossibleandconfiningourdatatotheresultsofdailyandweeklyobservations.
However,insuchastandardizedandsimplifiedenvironment,therewasverylittleopportunityforlearningofanysort,exceptlearningtodonothing.Thisposedaproblem,asmanyofthemajordifferencesbetweenthedogbreedsshowupascapacitiestolearnvariousspecializedtasks.Wethereforedeliberatelybegantosubjectthedogstocertainkindsofproblemsandtraining.Indoingthiswesetupasecondareseriesofexperiments.Thesedidnotinterferewiththemajorgeneticexperimentbecauseeverydogwastreatedalike.Inthesecondaryexperiments,eachdogwasitsowncontrol,andtheresultsconsistedofchangesinbehaviorinreactiontothenewexperience.Differencesbetweenindividualscould,ofcourse,beinterpretedastheresultofheredity.
Thesocialtestsweredeliberatelyspacedatlongintervalssothattheeffectsoflearningresultingfromthetestitselfwouldbeminimized.Incontrast,eachpsychologicaltestwasdoneinashortandcondensedperiodoftimeinordertogetthemaximumeffectoflearningandexperience.Whiletheeffectsoflearningarelonglasting,theirgreatesteffectisimmediate.
Atfirstwethoughtofthesetestsasintelligencetests,butastimewentonandwehadmoreexperience,webegantocallthemperformancetests,sincetheanimalsseemedtosolvetheirproblemsinmanywaysotherthanthroughpurethoughtorintellect.
Firstbarrierordetourtest.—Wegavethefirstperformancetestat6weeksofage.Itillustratesmanyofthegeneralprincipleswhichwefoundusefulindesigningagoodanimaltest.Inthefirstplace,thetesthadtofitthecapacitiesofthespecies.Therewasnosenseinrequiringdogstodothingswhichdemandedtheuseofhands.Sincedogsareprimarilyhuntinganimals,wedesignedthetestaroundaproblemoffindinganobjectcontainingfood.Secondly,
20BEHAVIORPATTERNS
youngpuppiescouldnotberequiredtogobeyondtheirstrengthandgeneral
youngpuppiescouldnotberequiredtogobeyondtheirstrengthandgeneraldevelopment.Until3weeksofagetheyaresoimmaturethatlittlecanbedonewiththem,and,indeed,theyappeartobehighlyprotectedfrompsychologicalexperience.Wethereforedecidedtodothefirstperformancetestat6weeksofage.Beforethistimetheyoungpuppieshadalwayslivedinsidetheirpensandhadalmostnoexperiencewithbarriersofanykindexceptthewalls,whichtheycouldneithersurmountnorgoaround.Wethereforeattemptedtodiscoverwhetherornottherewasanygeneticallyproducedabilitytodealwithbarrierswithoutexperience.Wetookthepuppiesoutoftheirpensandplacedtheminastrangeroom.Forthefirsttwodaysagirlexperimentersimplytookapuppyintotheroom,putitonthefloor,andletitfindadishoffoodplacedbetweenherfeet.Thepuppywasgiventwominutestoeatandexplorethearea.Thiswasdoneonceonthefirstdayandthreetimesonthesecond,bywhichtimethepuppiesusuallywentrapidlytothefoodandateit.Onthethirdday,therewasabarrierintheroom.Experimenterandfoodwereononeside,thepuppywasplacedontheother,anditstaskwastofinditswayaroundtheobstacle.Sincethepuppycouldseethefoodthroughthebarrier,thedifficultylayinthefactthatithadtogoawayfromthefoodinordertoreachit.Onceithadsucceeded,thetestwasrepeatedtwicemore,inordertoreinforcememoryoftheevent.Onthenextdayamoredifficultbarrierwasintroduced,andonthethirddaythemostdifficultofall(Fig.10.1).
Thefirsttwodayswerethusdevotedtolearningthelocationofthegoalandtointensifyingmotivationbyrepeatedreinforcement.Withsuchyounganimalstheperformancecouldnotberepeatedmorethantwoorthreetimesinclosesuccessionwithoutthepuppylosinginterestorbecomingfatigued.Indeed,formanyofthemthreetimesappearedtobetoomany.
Motivation.—Intheseearlyexperimentsacombinationofrewards—food,theproximityoftheexperimenter,andbeingreturnedtothelittermates—wereallusedaspartofthemotivation.Becausetheexperimentermightaccidentallygivecuestothepuppies,shewasinstructedtositquietlyanddonothingbuttakenotes.Inexperi-mentswitholderanimals,theexperimenterwasifpossiblekeptcompletelyoutsidetheroomsothatthepuppyhadtoactindependently.
Thefoodrewardwasthusmadethebasicsourceofmotivation,sinceitcouldbestandardizedagooddealbetterthananyreward
ofapprovalorsocialcontact.Weusedateaspoonofcannedfishfortherewardandfounditworkedverysuccessfully.Therewasnoneedtostarvethepuppies
andfounditworkedverysuccessfully.Therewasnoneedtostarvethepuppiesbecausetheyeagerlyatethisadditiontotheirregulardietanddidnotbecomesatiatedonthesmallamountsfedthem.Makingthepuppieshungrywouldhavebeenundesirableinanycasebecauseofpossiblebadeffectsongrowth.Thesamecannedfishwasusedinallsubsequentexperimentsinvolvingafoodreward.
Relationshipbetweenperformancetests.—Asageneralprinciple,eachperformancetestwasdesignedtoprovidepretrainingforthosetocome.At8weekstherewasagoal-orientationtestinwhichthepuppieslearnedtoruntoaparticularspotintheroomforfood,andlatertoadifferentplace.Thistestinturnwasfoundationtrainingforamanipulationtestinwhichfoodwasplacedinthesamelocationbuthadtobeobtainedeitherbypullingthefooddishoutfromunderacoverorbypullingoffthecover.
At13weeksofagethepuppiesgotasecondbarriertest,thistimeinamorecomplexform.Thustheperiodupto16weekswaslargelydevotedtoobservationofdevelopmentandtestsofsocialbehavior,withafewelementarypsychologicalteststhrownin.Theperiodfrom16weeksto35weeks,ontheotherhand,wasdevotedlargelytoperformancetests,sincetheanimalswerenowphysiologicallycapableofalargenumberofco-ordinatedmovements.Thepuppieswerealsolargeenoughbythistimesothattheirphysiologicalreactionscouldbeeasilymeasured.
At16weekseachlitterwasplacedinalargeoutdoorrunwhereitremainedasaunituntilthepuppiesreachedtheageofoneyear.Theywereatfirstsomewhatdisturbedintheirnewsurroundings,andwefoundthattheymadethetransitionmuchmorepeacefullyifweputthemoutforafewhoursononeday,broughtthembackintotheirformerpenovernight,andthenextdaypermanentlymovedthemoutside.
Thereaftertestsweredoneinoneofthreeplaces.Onewasthehomepenitself,inwhichthepuppiessoonbecamehighlyconfidentandrelaxed.TheothertwoareaswereinsidetheBehaviorLaboratoryinplacesunfamiliartothepuppies,sothatwehadtheproblemofpreparingthemforworkinginanunfamiliarenvironment.
Emotionalreactivitytests.—Wefirstdevisedatestofemotionalreactionstoatotallynewsituation(Fuller,1948).Thepuppieswerecarriedintoacontrolled-environmentlaboratoryandsubjectedtoavarietyofmildlyfrighteningsituations(loudnoises,
situations(loudnoises,
22BEHAVIORPATTERNS
isolation,weakelectricshock,etc.)whiletheirexternalandinternalemotionalreactionswerebeingrecorded.Thistestwasdoneat17,30,and51weeksofage.
Trainingtests.—Thefirstofthisgroupwasleashtraining(Fuller,1955).Thepuppywastaughttofollowanexperimenterintothebuilding,givenafoodreward,andafterwardstakenonaleashoverthesameroute.Thereafterhewasledalloverthebuildingwithoutfurtherrewards,inordertofamiliarizehimwiththenewtestsituations.Themethodwasessentiallythatofforcedtraining,combinedintheearlyphaseswithfoodrewards.Anotherexperienceofforcedtrainingwasgivenintheobediencetest,scheduledat30weeksofage,inwhichpuppieswereplacedonaboxandtaughtto"stay"untilacommandwasgiven.
Testsforspecialabilities.—Stillanothergroupoftestsattemptedtomeasurecertainspecialabilitiespeculiartotheindividualbreeds.Thefirstofthesewasanartificialtrackingtest.FishjuicewassmearedonmetalplatesattachedtothinstripsofboardwhichcouldthenbelaidoutinvariouspatternsleadingtoaSyracusedishholdingasmallbitoffish.Similaruntreatedplateswerelaidoutasfalsetrails.Wewishedtoseewhetherbeagles,whicharegenerallyusedfortrackingbyscent,wouldgiveasuperiorperformanceinthissituation.
Asecondtestofthiskindattemptedtomeasurethespecialclimbingabilityofbasenjis,whichwehadalreadyobservedintheirsuccessfulattemptstoclimbupontheirhousesandtoescapefromtheirruns.Inthistestthedogshadtoclimbsteeperandsteeperrampstoreachthetopofapileofboxesonwhichfoodwasplaced.Thefinaltestrequiredtheanimalstowalkacrossanarrowplankstretchedbetweendieboxesandthetopofthedoghouseintheirhomepen.Asitturnedout,theoutcomeofthetestwasstronglyaffectedbymotivationalfactorsaswellasmotorskill.
Athirdtestofthissortwastheretrievingtest,inwhichweattemptedtomeasurethewell-knownabilityofcockerspanielstolearntoretrieveobjectsmorerapidlythansomeotherbreeds.Ouroriginalattemptstomeasureretrievingweredonewithyoungcockerpupsbetween8and10weeksofage,andtheseanimalsdidverywellwhentestedagainat32weeks.However,whenwesubsequentlyabandonedtheearlytraining,performanceatthelateragewasverypoorforallbreeds,andthetestthereforegaveinconclusiveresults.Thereisanindication
breeds,andthetestthereforegaveinconclusiveresults.Thereisanindicationhereofacriticalperiodforlearningthisparticularsortofskill.
Problem-soilingtests.—Finally,therewasagroupoftestswhich
SCHOOLFORDOGS23
attemptedtomeasuremoreabstractkindsofintelligence.FromWeeks22to26,allthepuppiesweregivenaseriesoftestsinasimpleT-maze.Afterlearningtorunthroughthemazetoreceivefood,thedogsweretrainedtoruntowardthearmoftheTinwhichapanelwasmovedrhythmically.Amovingobjectwaschosenasthecuebecausethedogsappearedtonoticemovingobjectsmorereadilythanstationaryones.Someanimalsshowedextremelyrapidlearninginreactiontothiscue,butotherswereafraidofitand,indeed,ofthewholeT-maze,andtheirlearningwasconsequentlyretarded.Inthis,asinallotherperformancetests,emotionalandmotivationalfactorswerealwaysimportant.Thistrainingwasusedasthebasisforadelayedresponse,orvisualmemorytest.
Anothertestofintellectualcapacitywasdevelopedfromthemotor-skilltestandwascalledspatialorientation.Theanimalshadtoclimbrampsandcrossbridgessimilartothoseusedintheearliertest.Theapparatusremainedinthepenscontinuouslythroughoutthetest,sothatthesubjectscouldbecomecompletelyfamiliarwithit,anditoftenbecameafavoriteplaceforthedogstostandorsit.Duringthetesttheapparatuswasarrangedwithacentralfoodboxtowhichtherewasonlyoneopenpathway.Ahumanbeingcouldhavevisuallyinspectedthebarriersandimmediatelygonetothecorrectramp.Wehopedbythistesttomeasureobjectivelytheextenttowhichthevariousbreedsareorientedbyvisionandcapableofsolvingproblemsthroughtheuseofthissense.Ourhopeswerenotcompletelyrealized.Strikingindividualandbreeddifferenceswereobtained,buttheresultsdidnotsupportthehypothesisofasimpledifferenceinsensorydominance.Manyoftheanimalsappearedtosolvetheproblembyroutinelytryingeachpossiblesolutioninturnwithoutvisualinspection.
Aftertheterminationofthespatial-orientationtest,atabout8monthsofage,thedogsweregivenavacationuntiltheywereapproximatelyayearold.Duringthistimetheywereobservedregularlybutgivennoformaltests.Beginningat51weeks,alltheanimalsweregivenafinalbatteryoftests,mostofwhichrepeatedearlierones,withtheideaoffindingouthowstablethepreviouslyobserveddifferenceshadbecome.Thereactivityandhandlingtestswererepeated,social-dominancerankswereagainmeasuredwithineachlitter,physicalmeasurementsweretakenforathirdtime,andanewtestoffrustrationtolerancewasgiven,in
weretakenforathirdtime,andanewtestoffrustrationtolerancewasgiven,inwhichdogswereconfinedtosmallcagesandsubjectedtovarioussortsofstimulation.
BEHAVIORPATTERNS
historyofeachanimalintheexperimentissummarizedinTable1.3.Asthereweresome30majortestingsituations,eachofwhichincludedmultiplemeasurementsresultinginfrom5to40scores,thedataoneachanimalranintothehundreds.Testinghundredsofanimals,weeventuallyaccumulatedthousandsofmeasurements.
TABLE1.3
ScheduleofObservations,Training,andTesting
Test
Dailyobservation
Weeklyobservation,weighing
Maternalbehavior
Responsetohandling
Dominance
Group
Paired
Firstbarrier(detour)
Responsetoveterinarycare..Goalorientationorhabit
formation
Manipulation
Secondbarrier(maze)
(Transferredtooutsideruns).Bi-weeklyinspection,
catchingtime
Somatotype,weighing
Reactivity
Following
Leashcontrolandstair
climbing
Motivation,T-maze
Discrimination,T-maze
Delayedresponse,T-maze...
Trailing
Motorskill
Obedience
Retrieving
Spatialorientation
Physiologicalassessment
Responsetoconfinement
Social
Emotional
ForcedTraining
RewardTraining
ProblemSolving
PhysicalorPhysiological
Age(weeks)
0-160-16
1.7
5,7,9,11,13,15,52
2,3,4,6,7,8,9,10
5,11,15,52
6
8,10,12,14
9
10
14-1517
11:2
17,34,5117,34,5118
19-20
22
23
24-26
27
29
30
32
33-36
51
51
Inthefollowingchapterswehaveselectedforexhaustivetreatmentonlythosemeasureswhichseemedmostmeaningfulinviewofourgeneralobjective:todiscovertheinfluenceofhereditarydifferencesuponbehavior.Moredetaileddescriptionsofsomeofthetestsandmeasuresaregivenlaterintheappropriatechapters.
Byandlarge,thissystemoftestingwasverysatisfactory.Thepuppieseasilytransferredtheirbasicmotivationaltrainingfromonetesttoanother,andtherewasnoindicationthattheyweresolvingtheirproblemsbywatchingtheexperimenterinsteadofusingtheirbrains.Ontheotherhand,thepuppieswerecontinuallybeingexposedtonewsituationsandnewproblems,andtheyneverhadachancetogobackandpracticefamiliartasks.Iftheprogramhadbeensetupsothatthepuppiescouldhavegonebackandrepeatedsomeofthethingswhichtheyhadalreadylearned,theymighthave
SCHOOLFORDOGS
25
shownmoreconfidencewhentheycameupagainstnewproblems.Oursubjectiveimpressionwasthatourpuppieswerenothighlyconfidentinpsychologicaltests,contrastingwiththeirbehaviorinsocialrelationshipswitheachotherandwiththeexperimenters,inwhichlongfamiliaritymadethemhighlyconfident.
THEECOLOGICALLEVEL:SPACEANDCOMPLEXITY
Ourchiefconcernherewastokeepthephysicalenvironmentasuniformaspossibleforallanimalsandatthesametimemaintainsurroundingsreasonablynormalfordogs.Oneofourchieflimitationswasspace.Wecouldnotgiveeachdogthesquaremileorsoofterritorywhichhemighthavehadifraisedona
dogthesquaremileorsoofterritorywhichhemighthavehadifraisedonafarm.Duringpuppyhoodwekepteachlitterinalargeroommeasuring10by18feet,whichisnotfarfromthesizeofthespaceinwhichveryyoungpuppiesconfinetheirwanderings.At16weeksofagetheywereputintolargeoutsideruns,20feetwideby75feetlong.Inthese,a
i
m
NestBox
SideCover
Bench
IE"——
Motorr*'—'—'—
Rodi
Romp
•Door
Step
FoodPlatform
NURSERYROOM18*x13'
Fence
Waterw
Alley8Gutter
ObservationWindow
Door
FLOORPLAN
Fig.1.2.—Floorplanofnurseryroom.Theentirelivingspaceforthemotherandpuppiesis10X18feetandsoarrangedthatallpupsarevisiblefromtheobservationwindows.Onesideofthenestboxcanberemovedandlaiddownonthefloorsothatitsinteriorisalsovisible.
26BEHAVIORPATTERNS
litterofsixdogscouldliveinclosecontactbutnotseriouslyinterferewitheachother'sfreedomofmovement.Subsequentexperiencewithsmallerpens,20by40feet,indicatesthatinsuchpensinterferencedoestakeplacewithingroupsofthissize.
Astoobjectswithinthepensweprovidedonlyaminimumnumber,sothatitwouldbeeasiertokeepconditionsuniform.Inthenurserypenstherewasthenestbox,thewaterpail,fooddishes,andasmallbenchwhichwasfrequentlyusedbythepuppiesasahidingplace.Apieceofautomobiletirecasingwasleftinthepensforthepuppiestochewon,andasimilarpiecehungfromtheceilingwheretheycouldleapupandgrabit.Assoonasthepuppieswereoldenough,theirfoodwasplacedonaplatformwhichcouldbemountedeitherbystepsoralongarampconsistingofacleatedboardabout6incheswide.Thisgavethepuppiesexperiencewithverticalaswellashorizontalspace.
Intheoutsidepenstherewereveryfewobjectsexceptthenestboxes,waterdishes,andafewstonesmixedinwiththegravelfloorofthepen.Thenestboxesthemselveswereconstructedwithinsulatedwallsandroofforprotectionagainsttheweatherandwerereachedbyanindirectpassage(seeFig.1.3)sothatthedogslivedinwhatwasessentiallyanartificialdenkeptwarmbytheirbodiesandprovidedwithampleventilationwithoutdrafts.
Thereweremanyphysicalfactorswhichcouldnotbecompletelycontrolled.Thesewereenteredintherecordssothattheirpossibleeffectscouldbelateranalyzed.Onesuchvariablewastheseasoninwhichthepuppieswereborn,thisdeterminingtheseasoninwhichtheywerelatertestedandthusproducinganartificialcorrelationbetweentestresultsandtemperatureandotherweatherconditions.Wealwaysnotedthetemperatureatwhichanytestwasgivenandmaintainedapermanentrecordoftheoutsidetemperatureonarecordingthermometer.Whentestsweregivenoutdoors,werecordedtheweatherconditions,suchasrain,snow,etc.Testswerenevergivenduringactualstorms.
Theenvironmentintheoutsiderunswas,ofcourse,muchmorevariablethanthatinthenurseryrooms.Thiscircumstancewasnotentirelybad,becauseitmadetheolderdogssomewhatinsensitivetorandomenvironmentalstimulationfromnoisesoutsidetheirpens,whereasananimalkeptcontinuouslyinamorelimitedenvironmentwouldbelikelytoover-reactattheslightestnewstimulation.
Hebb(1947)liasshownintheMcGillUniversityPsychologicalLaboratoriesthatratsraisedaspetsinahomearesuperiorintheir
SCHOOLFORDOGS
27
performanceinpsychologicalteststoratswhichareraisedinordinarylaboratorycages.Heinterpretsthisastheresultofenrichingtheirenvironment.Judgedbythisstandard,thephysicalenvironmentofourdogswasrelativelybarren.Weattemptedtoenrichitintwoways:bybringingobjectsintotherearingpensduringtheexperiments,andbytakingthedogsoutandintroduc-
3"6'
FoodIHopperQ
-ifiT—.
Sun
porch
FLOORPLAN
FLOORPLAN
HOUSE3'6"x3'6"
Cleanoutdoor
(I'6"x2')
mmmt^§
I2H
Insulatedwall
3'6"IV
Insulatedroof(removable)
SIDEVIEW
Skid
INSULATEDDOGHOUSE
Fig.1.3.—Floorplanofall-weatherdogkennel.Theindirectentranceisdraft-freebutprovidesventilation.Insulatedwallsandroofkeeptemperaturesatcomfortablelevelsinbothcoldandwarmweather.
ingthemtootherenvironments.Ouranimalscertainlydidnothaveasrichanexperienceasadogrunningfreeonafarm,althoughtheirenvironmentmightcomparequitefavorablywithadogrearedinacityapartmentandnevertakenoutexceptonaleash.Underourconditionsthedogsprobablyneverdevelopedalloftheircapacitiestoamaximumdegree.Oneofourmajorconcernswastoprotectthemfromenvironmentalaccidentswhichmight
eithercrippleorgiveanundueadvantagetooneindividual.Fromanecologicalviewpoint,wehadtodevelopasortofmicro-climateandmicro-environmentwhichpartiallyexcludedtheoutsideworld.Forexample,ourdogsintheoutsiderunsweresurroundedbyfences4feethighwhichpreventedtheirobservingthingsatadistanceandalsopreventedceaselessrunningandbarkingatdogsintheneighboringpens.Theycouldtellwhendogsorpeoplecameclose,butthesecontactshadlittleseriouseffectontheirlives.Theimportanteventstookplacewithintheirpensorinthetestingrooms.
SUMMARY
Whenwestoodbackandlookedatthecompleteddesignofourexperiment,wediscoveredthatwehadevolvedavirtual"schoolfordogs."Ittookusnearly5yearstogeteverythingrunningsmoothlv,andtheschoolwastooperateatitspeakefficiencyforalmost8yearsthereafter,whilewetestedsomefivehundredpurebredandhybridpuppies.
Inthesameamountoftime,anelementaryschoolteacherwithaclassofthirtypupilsayearcouldhavemetandinfluencedthesamenumberofindividuals.We,asteachersinthisuniqueestablishment,learnedagreatdealwhichhasapplicationtothescienceofeducation,aswillappearinlaterpages.However,wewereprimarilyexaminersratherthanteachers,andourchiefconcernwastomakesurethatourpupilsgaveusanswerstothebasicscientificquestionswhichwehadaskedthem.
Oneofthefirstquestionswas,Whatkindofananimalisadog?Inevaluatingtheanswerswewouldfindthatadogisnotafour-leggedandchildishhumanbeingdressedupinafurcoat.Ourdogscouldthereforegiveusanswerstootherquestionsonlyasdogs,closelyrelatedtohumanbeingsthroughsocialcontactsbutbasicallycarnivoresintheirheredity.
DOGS,WOLVES,ANDMEN
Dogsareextraordinarilyvariableanimalsinallvisiblerespects.Therangeinsizeisalmostincredible;aChihuahuamayweigh4poundsandafull-grownSaintBernard160,orfortytimesasmuch.Legsvaryfromthesquatextremitiesofdachshundstothelong,gracefullimbsofgreyhoundsandsalukis.Atoppositeextremesweseetheundershotjawsandforeshortenedheadsofbulldogsandpugs,andthelong,narrowheadsoftheborzois.Tailsvaryfromatightcurltoasickleshape.Manifoldvariationsinthecolor,length,andtextureofhairexist
sickleshape.Manifoldvariationsinthecolor,length,andtextureofhairexistandthereisevenapermanentlybaldbreed,theMexicanhairless,contrastingwiththepoodlewithitscontinuouslygrowinghair.
Linnaeus,thegreatSwedishnaturalistwhooriginatedoursystemofclassificationofanimalsandplants,placedthedoginonespeciesandcalleditCanisfamiliaris,thefamiliardogascontrastedwithCanislupus,thewolfdog.Laternaturalistswonderedwhethersuchahighlyvariablespeciescouldreallyhavehadonecommonorigin(Darwin,1859;Packard,1885;Hilzheimer,1908).
Thisraisedthequestions,Whatisadog?andWherediditcomefrom?aswellastherelatedproblemsofwhenandhowthisoccurred.Sincethesearequestionsofprehistory,therecanneverbeanycompleteandfinalanswerstothem,andthebestwecandoistoassembletheavailableevidenceanddrawthemostprobableconclusions.Asweshallsee,mostoftheevidencesupportstheideathatdogshaveaunifiedcommonancestry,beingdomesticatedfromwolvessomeeighttotenthousandyearsago.
29
30BEHAVIORPATTERNS
EVIDENCEFROMTAXONOMY
ANDGEOGRAPHICALDISTRIBUTION
Taxonomyisthescienceofclassification.BeginningwithLinnaeus,biologistsbegantoclassifyanimalsaccordingtogenusandspeciesonthebasisoffundamentalsimilarities.Theideaofwhatconstitutesaspecieshasgraduallydevelopeduntiltodaywedefineaspeciesasapopulationofanimalswhichbreedtogetheror,togiveageneticdefinition,apopulationhavingaccesstoacommonstoreofgenes.Thismeansthatgroupsoflandanimals(likemostmammals)mustshowgeographicalcontinuityintheirdistributioninordertobeconsideredspecies.Suchpopulationscansometimesbedividedintolocalraces,butthesearestillpartofthesamespeciesifthereiscontinuousinterbreedingbetweenthem.Alocalraceiscalledasubspeciesifitshowsdistinctdifferencesfromothersuchpopulations.
Thedefinitionofaspeciesasapopulationhasproducedagradualbutdramaticrevolutioninthescienceofclassification.Theearlytaxonomistsworkedbyfirstminutelydescribingaparticularindividualspecimen,or"tyPe>"andthenincludinginaspeciesallindividualswhichcloselyresembledit.Sincethereisa
includinginaspeciesallindividualswhichcloselyresembledit.Sincethereisagreatdealofvariationwithinapopulation,itwaseasyfortwodifferentnaturaliststopickupdifferentspecimensfromthesamepopulationanddescribethemasseparatespecies.Consequently,theolderscientificliteratureonthesubjectisveryconfusing,andeventodaytheclassificationschemehasnotbeencompletelyrevised.Thefollowingdescriptionisbasedonthelatestavailableclassificationofdogsandtheirrelatives.
Tobeginwiththelargertaxonomicdivisions,dogsbelongtotheorderCarnivora,whichisdividedintotwolargegroups,thewater-livingformslikethesealsandotters,andtheland-livingones,whichincludesevendifferentfamilies:thebears,raccoons,weasels,civets,hyenas,cats,anddogs.
Membersofthedogfamilytypicallyrunontheirtoes,incontrasttothebearsandraccoonswhichwalkontheirheels.Theyarebestadaptedforswiftrunninginopencountry,andthelargeronesusuallycapturetheirpreybyrunningitdown.ThefamilyCanidaeincludestheFoxesandtheso-called"wilddogs"—theAfricanhuntingdog,theSouthAmericanbushdog,andthedholeofIndia—aswellasthetruedogsandwolves.
Thetaxonomistsoriginallyplacedseveralcommonanimalsinthe
genusCanis:C.familiaris,thedomesticdog;C.dingo,theAustralianwilddog,ordingo;C.lupus,thegraywolf;C.latrans,thecoyote;andC.aureus,thejackal.AllofthesearestillincludedinthegenusCanis,exceptthejackal,whichsomeexpertsplaceinaseparategenus,Thos.Eachofthesespeciesoccupiesasomewhatdifferentecologicalniche.WolvesarehuntersofthelargeungulatesintheNorthernHemisphere,pursuingcaribouinarcticregionsanddeerormooseinmoresouthernclimates.Theyliveontundras,inforests,oronplains,wherevertheirpreyisfound(AllenandMech,1963;YoungandGoldman,1944).Theircloserelatives,thecoyotes,aresmalleranimalsoftheplainsanddeserts,chieflyhuntingrabbitsandsmallrodentswhichtheyfindthere,aswellasbeingscavengersandcarrioneaters(YoungandJackson,1951).IntheOldWorld,jackalsarethecounterpartsofcoyotes,beingscavengersofthesouthernandequatorialdeserts.Domesticdogs,ofcourse,arefoundallovertheworldincloseassociationwithman,livinginavarietyofclimatesandeatingavarietyoffood.ThedingoisahunterofmarsupialsentheAustralianplainsanddeserts,andmorerecentlyhastakentopreyingondomesticsheep.
ThefossilevidenceshowsthatthefamilyCanidaeoriginallycamefromthe
ThefossilevidenceshowsthatthefamilyCanidaeoriginallycamefromtheNorthernHemisphere,andthedistributionofitsdescendantsisconsistentwiththis.WolvesarefoundonlyinNorthAmericaandEurasia.YoungandGoldman(1944)recognizedtwospeciesofwolvesinNorthAmerica,C.lupus,thegraywolf,andC.niger,theredwolfformerlyfoundintheMississippiValleyandsoutherncoastalpartsoftheUnitedStates.Eachcanbedividedintovarioussubspecies.Thegraywolf,C.lupus,isalsofoundinnorthernEuropeandAsia,withasubspecies,pallipes,inIndia.Thisisasomewhatsmalleranimal,andsomescientistsconsideritaseparatespecies.TherearenonativewolvesinAfrica,SouthAmerica,Australia,orAntarctica.
Thecoyote,C.latrans,isfoundonlyinNorthAmerica,andoriginallyrangedfromAlaskanearlytoPanama(YoungandJackson,1951).Thejackalshavesometimesbeendividedintomanyspecies,butatpresentthereareonlythreedefinitelyrecognizedspecies(Hildebrand,1954).TwooftheseliveonlyinAfrica.Thecommonyellowjackal,C.aureus,rangesfromnorthernAfricathroughAsiaMinortosoutheasternEurope,andinaneasterlydirectiontoIndiaandbeyond.Thejackalsarethusamoresoutherngroupthananyothermembersofthegenus.
Thedomesticdoghasthewidestdistributionofany,beingnowfoundonallinhabitedcontinentsandalwaysincloseassociation
BEHAVIORPATTERNS
withman.Beforemoderntimes,dogswerefoundonallcontinentsexceptAustraliaandAntarctica.TherewereseveralkindsofnativedogsinAfricaandSouthAmerica.EveninAustraliatherewasthedingo,whichissosimilartothedomesticdogthatitissupposedtohavebeenintroducedbytheaboriginesandlatergonewild.Thisismademoreprobablebythefactthatthedingoisoneofthefew
W=Southernboundaryofdistributionofwolf(Cornslupus)J»Northernboundaryofdistributionofjockal(Conisaureus)C=Distributionofcoyote(Conistotrons)*-#Proboblecenteroforiginofdog
AmericanMapCo.,NewYork.
Fig.2.1.—GeographicaldistributionofwildmembersofthegenusCards.WolvesarenorthernanimalsofEurasiaandNorthAmerica,whereasjackalsbelonginAfricaandsouthernAsiaandcoyotesareconfinedtoNorthAmerica.Theearliestknownremainsofdogs(inDenmark)fallwithintherangeofthewolf.(ModifiedfromWerth,1944)
placentalmammalsoriginallyfoundinAustralia.Theothersincludeman,severalkindsofratsandmice,andavarietyofbats.
AssumingthatthedogmusthavebeendomesticatedfromsomeexistingspeciesbelongingtothegenusCanis,andthatthisspeciesmusthavebeendomesticatedataplacewithinitsnaturalrange,thegeographicalevidenceeliminatesSouthAmericaasapossibledomesticationcenter,sincenowildspeciesofthegenusCanishaseverlivedthere.WecanalsoeliminateAustralia,asthedingoisFarmorelikelytobeadomesticdoggonewildthanitistobeanancestralform(Werth,1944).WecannoteliminateAfrica,butif
DOGS,WOLVES,ANDMEN33
dogswerefirstdevelopedonthatcontinent,theycanonlyhavebeendomesticatedfromjackals,sincejackalspeciesaretheonlyonesfoundinthatarea.InEurasia,dogscouldhavebeendomesticatedfromeitherwolvesorjackals,whereasinNorthAmericatheonlypossiblecandidatesarewolvesand
jackals,whereasinNorthAmericatheonlypossiblecandidatesarewolvesandcoyotes.
Theevidencefromgeographicaldistributionoflivinganimalsthusnarrowsdownthepossibleancestorsofthedog.Thereremainsthepossibilitythatthedogcouldhavebeendomesticatedfromawildspeciesnowextinctorfromsomeoftheso-called"wilddogs"nowliving.
EVIDENCEFROMFOSSILS
The"wilddogs"caneasilybeeliminated.ThesedistantrelativesofthedogincludeLycaon,theAfricanhuntingdog;Icticyon,theSouthAmericanbushdog;andCuon,thedholeofIndia(the"reddog"ofKiplingstories).AccordingtoMatthew(1930),thefoxesandwolveshaveacommonancestorintheMiocene,somesevenandahalfmillionyearsago,buttheirrelationshipwiththewilddogsismuchmoreremote,tracingbacktoacommonancestorintheOligocene,sometwentymillionyearsago.Thisprettywellexcludesthe"wilddogs"asancestorsofthedomesticones.TheyareactuallymoredistantlyrelatedtothegenusCanisthanarefoxesandarequiterightlyplacedindifferentgenerafromthedog.
Atvarioustimesscientistshavespeculatedthatthemoderndogisdescendedfromasmallwilddogwhichisnowextinct(Allen,1920).Todate,nosuchhypotheticalancestorhasbeendiscovered.Matthewfindsthatwolves,coyotes,jackals,andfoxeswerepresentinessentiallytheirmodernformsinPleistocenetimes,overhalfamillionyearsagoaccordingtorecentestimates(Kulp,1961).Thesefourkindsofanimalshaveremaineddistinctfromeachothereversince,andtherearenoskeletalremainsuntilrecenttimeswhichcanbeidentifiedasdomesticdogs.Thesedogremainsarenotfossilsbuttruebones,discoveredbyarcheologistsinassociationwithhumanskeletons,ruins,andartifacts.
EVIDENCEFROMPREHISTORY
Beingadomesticanimal,thedogisalwaysfoundincloseassociationwithman,andthebestevidencefortheexistenceofprehistoricdogscomesfrombonesfoundwithprehistorichumanremains.Thescienceofarcheologyisnowinastateofferment,partly
34BEHAVIORPATTERNS
becauseofnewtechniquessuchasradiocarbondating,whichmakesitpossible
becauseofnewtechniquessuchasradiocarbondating,whichmakesitpossibletoestimatetheageofbonesandotherorganicremainsonanobjectivescale,andpartlybecauseofanewinterestinthedomesticationofanimalsandplants.
BraidwoodandReed(1957)describetheprehistoric"agriculturalrevolution"whichproducedasprofoundchangesinthelivesofearlymenasdidtheindustrialrevolutionintheexistenceofmodernman.Earlymenlivedbygatheringwildplantsandotherfood,andoccasionallyhuntinginpacks.Withthedomesticationofplantsandanimals,theyhadaccesstoagreatlyincreasedfoodsupply,couldliveinmuchgreaternumbers,andbegantosettleinvillagesandtowns.Thedogisdifferentfrommostdomesticanimalsinthatitwouldhavebeenusefulbothtohuntersandtoprehistoricfarmersandherdsmen.
Theagriculturalrevolutiontookplaceinmanypartsoftheworld,butitfirstbeganinthe"fertilecrescent,"thefoothillsofthemountainssurroundingMesopotamiaandPalestine,andthisistheareawhichBraidwoodandReedhavestudiedmostintensively.Reed(1959,1960)statesthattheearliestauthenticremainsofadoghavebeenfoundinJerichoanddatesthematapproximately6500B.C.oreighty-fivehundredyearsago.InthecontemporaryagriculturalvillageofJarmothereareseveralclayfigurineswhichareidentifiableasdogsbecauseoftheircurlytails.Itispossiblethatevenearlierremainsofdogswillbefoundinthefuture,butthisisamatterofconjecture.Incontrast,thefirstevidenceofdogsinEgyptisdatedatonly3500B.C.,somethreethousandyearslater.Theevidenceisabowlwitharecognizablepictureofsomegreyhounds,orsalukis.Long-limbedskeletonsofthesamedatehavebeenfoundinMesopotamia,wheresalukiswereprobablyfirstdeveloped.ItlooksasiftheuseofthedogspreadslowlyfromPalestineintoEgypt.
ThedogsinIraqtodayincludethesaluki,atallgreyhound-likeanimalusedforhuntinggazelles,andalargeheavilybuiltguardandherddogusedbytheKurdishshepherds(Hatt,1959).Itisdifficultorimpossibletodiscriminatethebonesoftheselatterdogsfromthoseofthelocalwolves,andthisregionisdefinitelyapossiblecenterforthefirstdomesticationofthedog(Reed,1959,1960).
TheonlyotherareaoftheworldwhichhasbeenstudiedasintensivelyisWesternEurope.TheoldestauthenticdogremainscomefromDenmark,discoveredtherebyDegerb0l(1927).ThebonesandhumanartifactsfoundwiththembelongtoaculturalperiodknownastheMaglemosian,thelatterpartoftheMesolithicperiod
DOGS,WOLVES,ANDMEN35
duringthetransitiontotheNeolithic.Theseremainshavenotbeencarbondated,butotherestimatesplacethemfrom8,000to10,000b.c.Reed(1959)thinksthattheymaybeeitherolderorsomewhatmorerecentthanthebonesfoundinJericho.Astheevidencenowstands,theearliestremainsofdomesticdogscomefromDenmark,withthosefromtheMiddleEastfallinginsecondplace;butthisconclusionmayhavetoberevisedinthelightoffuturediscoveries.
MorerecentStoneAgedogshavebeenfoundinEuropeassociatedwiththeSwisslakedwellers,andothershavebeendugupfromthebottomofLakeLadogainRussia.Usingthetypemethod,theolderarcheologistsdescribedeachoftheseremainsasseparatesubspeciesofdogs,givingthemsuchnamesas"Cantsfamiliarismatrisoptimae,"andStuder(1901)triedtotracemodernbreedsbacktothem.Dahr(1937)foundthattheseStoneAgedogs,farfrombeingspecializedbreeds,wereallverymuchalikeascomparedtothewidelyvaryingmodernbreeds,andmostauthorsnowagreethattheirremainsaresimilartotheskeletonsofmodernEskimodogs.Degerb0lstatedthathisearlierspecimensweredistinctlydifferentfromwolvesinhavingsmallerteethandjaws.Thiswouldargueagainstthedogbeingdomesticatedinthatarea,butagainwemustconcludethattheevidenceisstillquiteincomplete.
TheoriginaldoginhabitantsofNorthAmericawereextensivelystudiedbyAllen(1920),whofoundthatallofthemshowedresemblancestowolvesratherthantocoyotes.Haag(1948)laterestimatedthattheearliestdogremainsintheWesternHemispherecanbedatedabout1500b.c,butthisdatemaybetoorecent.Atanyrate,itismuchlaterthaneventheEgyptiandogs,anditislogicaltosupposethatdogswereintroducedintoNorthAmericabytradingorbymigratingpeoplescomingacrosstheBeringStraitintoAlaska.Otherareasoftheworld,includingSoutheastAsia,areallrelativelyunknownfromthearcheologicalpointofview.Perhapsnewdiscoverieswillchangethepicture,butatpresenttheonlystrongcontendersforthecenterofdomesticationofthedogareDenmarkandMesopotamia.
Therearetwopossibletheoriesregardingtheoriginofthedog.Oneisthatthedogwasdomesticatedonceandspreadrapidlyallovertheworldfromthiscenter.Analternatetheoryisthatthedogwasdomesticatedatseveraldifferenttimesandplaces.IfthefirsttheoryiscorrectandDenmarkwasthecenteroforigin,thedogcouldonlyhavebeendomesticatedfromthewolf,asthatistheonlywildmemberofthegenusCaniswhichexistedinthatregion.If
onlywildmemberofthegenusCaniswhichexistedinthatregion.IfMesopotamiawasthecenter,dogscouldhavebeendomesticated
BEHAVIORPATTERNS
AmericanMapCo.,NewYork.
Fig.2.2.—Centersofdomesticationandhypotheticaladaptiveradiationofdogsfromthesecenters.Solidlinesrepresentthenortherndogs,andbrokenlinesthesoutherndogs,includingthebasenjianddingo.
fromeitherthewolforthejackal.However,ifdogsweredomesticatedatvarioustimesandplaces,thefieldofpossibleancestorsisstillwideopen.
EVIDENCEFROMCOMPARATIVEANATOMYANDPHYSIOLOGY
OneofthedifficultiesofstudyingprehistoricdogsisthattheirbonesaresometimesindistinguishablefromthoseofwolvesorothermembersofthefamilyCanidae.Biologistsfrequentlyhavethesamedifficultyinidentifyingrecentlykilledspecimens.IsthelargedoglikeanimalwhichwasshotwhilekillingdeerasmalltimberwolforalargeGermanshepherd?Inmanycasestheexpertcanonlygiveanopinionratherthanadefiniteidentification.
Anyonewholooksatwolvesinzoologicalparksisimmediatelyimpressedwiththeirdoglikeappearance.Thereareonlyafewnoticeabledifferences.Theyhaveheaviercoatsthanmostdogsandlong,bushytailswhichareonlyslighdycurved.Thegeneralshapeoftheirheadsisdoglike,andtheirearsareerect.Theyarelargerthanmostdogsandmayweighanywherefrom60to175pounds(YoungandGoldman,1944).Theirlarge,heavyheadsandlong,heavilyboned
(YoungandGoldman,1944).Theirlarge,heavyheadsandlong,heavilybonedlegscontrastwiththoseofmostdogs.Inshort,they
DOGS,WOLVES,ANDMEN37
arepowerful,ruggedanimals,nothighlyspecializedforanyoneactivity.Theylooklikebigdogs,butwithoutanyoftheheadortaildeformitieswhicharecharacteristicofsomedogbreeds.
Coyotes,ontheotherhand,aremuchsmalleranimals.Theaveragecoyoteweighsabout25pounds,withtherangeextendingbetween18and30,exceptforsomeexceptionallylargeanimalswhichmayweighasmuchas74pounds(YoungandJackson,1951).Theirgeneralbodyproportionsarethesameaswolves(Hildebrand,1954),buttheyhaveproportionatelylongernecksandnarrowermuzzles,givingthemthegeneralappearanceofalargefox.Theyarespecializedforfastrunningandforhuntingsmallanimalslikerabbitsandgroundsquirrelsontheopenplains.
ThethirdgroupofwildrelativesofthedogsarethejackalsoftheAfricanandAsiandeserts.Theyareverysimilartothecoyotesbothinappearanceandwayoflivingbutareevensmallerinsize,theaverageadultweighingonlyabout20pounds.
Wecanconcludethattheprincipalanatomicaldifferencebetweenthesethreewildspeciesisamatterofsizebutthatthisisnotanabsolutedifference,sincecoyotesoverlapbothwolvesandjackals.Dogs,ofcourse,overlapalltheseanimalsinsize,thedwarfbreedsbeingsmallerthanthesmallestjackals,andthelargestdogsbeingaslargeasthelargestwolf.Thereisthereforenodistinct"dogtype"whichcanbeimmediatelydistinguishedfromthewildspecies.Ofcourse,therearecertainindividualdogsandbreedswhicharedistinctlydifferent.NoonewouldconfuseaChihuahuawithajackal,andabulldogisimmediatelyrecognizableforwhatitis.Suchextrememutanttypesamongdogsareeasilyidentified,butthevastmajorityofthebreedsarereasonablynormalinbasicanatomy,andifwearetodiscoveranythingregardingtheirrelationshipswithoneanother,wemustdoitonapopulationbasis.
Apopulationcanbedescribedintermsoftheaverageandtheamountofvariationfromtheaverage,usuallyexpressedinstatisticaltermsasthemeanandstandarddeviation.Whenwedescribeaspecies,wemustmakemanysuchmeasurementsonmanyindividualsinordertogiveanaccuratestatisticalpictureofthepopulation.Fewsuchstudieshavebeendoneondogsbecauseofthe
ofthepopulation.Fewsuchstudieshavebeendoneondogsbecauseoftheimmenseamountofworkinvolved,particularlyifonehastoworkwithhandcalculatorsratherthancomputers.Mostattentionhasbeenconcentratedontheskull,partlybecausethisistheportionoftheskeletonwhichismostlikelytobepreserved,andpartlybecauseitshowsthemostvariation.
Dahr(1937)measuredtheskullsofStoneAgedogsofnorthern
38BEHAVIORPATTERNS
Europeandcomparedtheirdimensionswiththoseofmodernbreeds.Oneofthehighlyvariablecharacteristicsofcurrentdogbreedsistheshapeoftheupperjaw.(Figs.2.3,2.4,2.6).Bulldogshaveshort,broadjaws,andthoseofgreyhoundsarelongandnarrowcomparedwiththoseofotherbreeds.WhenDahrcomputedtheratioofsnoutlengthtobreadthoftheupperjawatthenarrowestpointandgraphedthisratioagainstskulllength,hefoundthattheStoneAgedogsallfellinaclosegroupinthemiddleofthemoderndogbreeds.Whenhemeasuredtheheightofthelowerjawfromtoptobottominrelationtothelengthoftherowofmolarteeth,heagainfoundthattheStoneAgedogsformedacompactgroupinthemiddleofthemoderndogbreeds.HeconcludedthattheseearlyEuropeandogsallbelongedinthesamepopulationandthatthemodernbreedpopulationshavedivergedinalldirectionsfromthem.
Anothervariablecharacteristicindogskullsistheshapeofthelowerjaw.ThewolvesstudiedbyDahrhadlongerandheavierlowerjawsthanmostmodernbreeds,althoughtheiraveragejawthicknesswasexceededbytheverylargebreedsliketheSaintBernard.Thelengthofthemolartoothrowisagoodindicatorofjawlength.NoteventheSaintBernardshaveaslongarowofmolarteethasdothewolves,sothatthewolvesstandatthetopendofthescalewithregardtojawsize.Itisobviousthatifwolveswereancestorsofmoderndogs,theremusthavebeenaveryearlyselectionforanimalswithsmallerjawsandteeth.Dahrwasinclinedtothinkthattheoriginaldogswereamiddle-sizedraceofwolveswhicharenowextinct.Judgingfromthetendencyforwolvestobesmallerinmoresouthernregions,thisisareasonablehypothesis,and,asmentionedearlierinthischapter,therearestillsuchwolveslivinginMesopotamia,indistinguishablefromcertainlocaldogsintheirskeletalcharacteristics.Werth(1944)arguesthattheprobableancestoristheIndianwolf(C.lupuspallipes)whichlivesinthatregion,andLawrence(1956)hasindependentlyreachedthesameconclusion.
DahrbasedmanyofhisconclusionsonmeasurementsmadebyWagner(1930).
DahrbasedmanyofhisconclusionsonmeasurementsmadebyWagner(1930).ThelattertraveledaroundthemuseumsinOslo,Copenhagen,andBerlin,measuringthedogs'skullsfoundthere.Someoftheseskullsdatebackasearlyas1863andmaynotreflectthemodernbreedsaccurately.HewasabletocollecttenormoreskullsFromtwelvedifferentdogbreeds,withsmallernumbersfromalargenumberofothers.Becauseofthepreferenceformalesamongdogowners,mostofthesemusthavebeenofonesex.Healsomeas-
DOGS,WOLVES,ANDMEN39
uredseventeenwolfskullswhichhadbeencollectedinScandinavia,Greenland,andSiberiaandthereforemusthavecomefromthelargenorthernracesofwolves.
Wagnermadesomefortydifferentmeasurementsoneachskull.Ofthese,thebestmeasureofover-allsizeisthebasallength,thedistancebetweentheopeningintherearoftheskullfortheentranceofthespinalcordtothemostanteriorpointontheupperjawatthebaseoftheupperincisorteeth.Othermeasurementscanbegraphedagainstthis,asshowninFigures2.3-2.6.
Oneofthefirstthingswenoticeaboutlivingwolvesisthattheyseemtohavebroadheadsandheavyjaws.Ifwegraphthegreatestwidthacrossthecheekbones,whichincludesthejawmuscle,wefindthatwolves'skullsarewiderthanmostdogbreedsexceptfortheSaintBernards(Fig.2.3).Thebulldogbreedsalsohavemuchthesameproportions.Suchwidecheekbonesreflecttheskeletaleffectofhavingheavyjawmuscles.
Whenwegraphthegreatestbreadthoftheupperjaw(takenoppositethelargecarnassialteeth),wefindthatwolvesareessentiallynodifferentintheirproportionsfromnormaldogs,andthatSaintBernardshavejawswhicharefullyaswide(Fig.2.4).Thebulldogbreedsareoffinaclassbythemselveswithabroaderthannormalupperjaw,buttwootherbreedsareevenmoreextreme,theGreatDaneandGermanshepherd.Thesearethemostbroad-jawedofanybreedsandfarexceedthewolves.Itisinterestingthatthesetwobreedshavebeendevelopedinthesamepartoftheworld,andtheypossiblyhavesomecommonancestry.
Quiteadifferentpictureresultswhenwegraphthesizeofthemolarteethinrelationtothesizeoftheskull(Fig.2.5).Ontheaverage,wolvesnotonlyhavebiggerteeththananydogbreedstudied,buttheyarelargerinproportion.Inthemajorityofdogbreeds,toothsizeisverynicelycorrelatedwiththesizeofthe
majorityofdogbreeds,toothsizeisverynicelycorrelatedwiththesizeoftheskull,eveninthosebreedswithdeformedskullssuchasbulldogs.Thefewexceptionsarethosebreedswhichhavesomewhatsmallerteeththantheaverage.ThismeansthatWagner'swolfpopulationdifferedfromalldogpopulationsinonlyonerespect,theaveragesizeoftheteeth.Aswehaveseen,individualsinotherpopulationsoverlap.LittleRedRidingHood'sclassicremarktothewolf,"Whatbigteethyouhave,Grandma,"seemstobepartiallyjustifiedbythefacts.Itfollowsthatoneoftheearliestselectionproceduresfollowedbytheearlydomesticatorsofwolvesmayhavebeentopickoutanimalswithsmallteeth.
Thesemeasurementsalsobringoutthefactthatthereareonly
BEHAVIORPATTERNS
60
80
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120140160180200BASALLENGTH(MM)
220240
Fig.2.3.—Skullwidthacrosscheekbonesasrelatedtoskulllength.Notethatbreedswithbulldogheads(havingshort,wideskulls)fallofftooneside.Wolveshavewideskulls,andcoyotesandjackalsnarrowones,butbothareexceededbyvariousdogbreeds.(MostdatafromWagner.)
KeytoBreeds(Figs.2.3-2.5)
BBA
BEABO
BOLBU
BUA
COCS
DDIDODP
Borzoi
Basenji
Beagle
Boxer
Bolognese
Bulldog
Bulldog,oldtype
CoyoteCockerspaniel
DachshundDingoDobermanDwarfpinscher
EG=Englishgreyhound
FBFT
Frenchbulldog
Foxterrier
CD=zGreatDaneGS=Germanshepherd
I=Icelandicdog
IW=Irishwolfhound
J=Jackal
L=Laplanddog
M=Mops(pug)
N=NewfoundlandNH=:Norwegianharehound
P=rPointerPE=PekinesePU=Poodle
RP=Rattlepinscher
S=SetterSB=SaintBernardSCH=:SchnauzerSH=Sheltie(Shetlandsheepdog)
W=WolfWH=Whippet(largeandsmall)
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DOGS,WOLVES,ANDMEN41
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BASALLENGTH(MM)
Fig.2.4.—Greatestwidthofupperjawrelativetoskulllength.NotethatGreatDanesandGermanshepherdshaveunusuallywidejaws.Coyotesandjackalshavenarrowjaws,butarenotasextremeassomebreeds.(MostdatafromWagner.)
140
120
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BASALLENGTH(MM)
Fig.2.5.—Sizeofmolarteethrelativetoskulllength.Toothsizeandskullsizearehighlycorrelated,butinlargenorthernwolvestheteetharelargerthaninanydogsofsimilarsize.(MostdatafromWagner.)
42BEHAVIORPATTERNS
afewrealdeparturesfromnormalproportionsoftheskullinthedogbreeds.Oneoftheseisthebulldogtypeofhead,anditisinterestingthatthisdeformityappearsevenindwarfbreedslikePekingeseandpugs.AnotheristhebroadjawsoftheGreatDanesandGermanshepherds.Theheadsofthegreyhoundgroupareinbetterproportionthanonewouldexpect,andtheirbiggestvariationfromthenormisinthewidthbetweenthecheekbones.ThenarrowheadoftheborzoisandEasterngreyhounds,orsalukis,istheanatomicalresultofhavingnarrowcheekbonesandlessspaceforjawmusclesratherthanhavingthebrain
narrowcheekbonesandlessspaceforjawmusclesratherthanhavingthebraincasesqueezedtogether,asisoftenthought.
Anotherinterestingpointisthatthedwarfbreedshavebraincaseswhicharealmostaslargeasthoseofthebigbreeds.Reductioninbodysizehasaffectedthebrainverylittle,butthejawsandskullthicknesshavebeenreducedagreatdeal.Selectionforsmallsizehaschieflyreducedthosepartsoftheskullwhichareattachedtotheoutsideofthebraincase.Thisagainarguesthatthedogbreedsallcomefromonespecies,forifthedwarfanimalscamefromasmallspecies,onewouldexpectthatthepartsoftheirskullswouldbeingoodproportiontoeachother.
Stockard(1941)studiedtheskullsofvariousmodernbreedsofdogsandcametotheconclusionthatthebreedscouldbedividedintotwotypes,thosehavinglongskullsandthosehavingshortones.Theproportionsofthesaluki,GreatDane,SaintBernard,Germanshepherd,bassethound,anddachshundvarysomewhatfromeachotherbutareverydifferentfromsuchanimalsastheEnglishbulldog,Frenchbulldog,Bostonterrier,Pekingese,andBrusselsgriffon.Thelattergroupofanimalsaretheproductofageneorgeneswhichproducesabnormaldevelopmentofthehead.
Adifferentgeneorgroupofgenesmayshortenanddeformthelegs,ashappensinthedachshund.Itisprobablethatthemutationsfordeformedheadsanddisproportionatelyshortlegsoccurredseparatelyandwereusedindifferentcombinationsforthedevelopmentofvariousbreeds.Thuswehavetheboxerwithabulldogheadandnormallegs,aswellastheshort-leggedEnglishbulldog.Suchanimals,however,donotthrowmuchlightontheancestryandrelationshipsofthedog,excepttoindicatethatbreedswithbulldogheadsmayberelated.Eventhisisnotdefiniteproof,asthebulldogmutationmayhaveoccurredmorethanonceatdifferenttimesandplaces.
Thesestudiesshowthattherearenodistinctskull"types"excepttortheobviousdistortionsfoundinbulldogheadsandthenarrow
DOGS,WOLVES,ANDMEN
skullsofthegreyhoundbreeds.Wolvesoverlapwithdogsineveryskullmeasurementwiththepossibleexceptionofthesizeoftheteeth,andevenherelargedogsandwolvesoverlapasindividuals.Givenanunknownskull,abiologistcanidentifyitonlyintermsofprobabilitywithrespecttothemeasurementsofaknownpopulation.Someskulls,likethoseofChihuahuasand
measurementsofaknownpopulation.Someskulls,likethoseofChihuahuasandbulldogs,canbeidentifiedasdogswithverynearly100percentprobability,althoughevenherethereisalwaystheveryunlikelypossibilityofasimilarmutationinawildspecies.Onewaytoincreaseaccuracyistodetermineprobabilityonseveraldifferentmeasurements.Sofar,tinsmethodhasonlybeenusedtostudytherelationshipsbetweenpopulations.Jolicoeur(1959)studiedwolfpopulationsinthiswayandfoundthattheamountofoverlapwasinverselyproportionaltogeographicaldistance,andheconcludedthatmanyofthesubspeciesofNorthAmericanwolveswhichhavebeenidentifiedbythe"type"methodshouldbeconsideredpartofthesamepopulation.Suchananalysisisyettobeappliedtorelationshipsbetweendogbreeds,butwehaveeveryindicationthatthereisalargeamountofoverlapbetweenbreedsofthesamegeneralsize(Fig.2.6).
Tables2.1and2.2summarizetheresultsofmeasuringtheskullsofsampleanimalsfromthefivedifferentbreedsusedinourexperi-
TABLE2.1
AverageSkullMeasurementsofDifferentBreedsofDogs(tonearestmm.)*
Measurement
Condylobasallength
Basallength
Braincavitylength
Bizygomaticbreadth
Greatestjawbreadth
Smallestjawbreadth
Snoutlength
Lengthofmolartoothrow,Sizeofmolarteeth
FoxTerrier(2c7,29)
161152
161152
80
83
53
31
83
65
65
*Notethatsheltiesandfoxterriershavelongerskullsthantherest,andthatthesheltiesshowthesmallestmeasuresofanyinskullbreadth.
ments.ThesemeasurementschieflybringoutthefactsthattheShetlandsheepdogs(shelties)andwire-hairedfoxterriershavelongskullscomparedwiththeotherbreeds,andthatsheltieshavenarrowjawsinproportiontoskulllength.Thereisagreatdealofindividualvariabilitywithinbreedsandnoclearcutseparationbetweenthemexceptforthenarrow-jawedconditionofshelties(Fig.2.6).
BEHAVIORPATTERNS
TABLE2.2
RatiosofSkullMeasurementstoLengthofSkull(basallength)
Measurement
Braincavitylength
Bizygomaticbreadth
Greatestjawbreadth
Smallestjawbreadth
Snoutlength
LengthofmolartoothrowSizeofmolarteeth
FoxTerrier(4)
.53
.55.35.21.55.43.42
Anothermethodofdeterminingrelationshipsbetweenpopulationsistostudythereactionofbloodserumfromoneanimaltothatofanother(Boyden,1942).Thetechniqueistotakeserumfromoneindividualandinjectitintoanother,whichinduecoursedevelopsantiserum.Iftheserumofafoxisinjectedintoachicken,theanimalwilldevelopantiserumagainstfoxblood.Theexperimenterbleedsthechickenandextractstheantiserum.Henowtakesmoreserumfromthefox,mixesitwiththeantiserum,andmeasurestheamountofprecipitate.Thisgivestheamountofreactionagainsttheoriginalfoxserum,orantigen.Ifhemixesdogserumwiththeantiserum,thereisasmalleramountofprecipitate.Comparisonofthetwofiguresprovidesanestimateofhowalikethetwospecies
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40
30
30
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COYOTES
X,--
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JACKALS(AUREUS)
feife)I70"[fel
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100110120130140I
BASALLENGTH
Fig.2.6.—Relativebreadthofupperjawinfivemodernbreeds.NotethatstraightlinewillcutoffallShetlandsheepdogsfromtherestbutthatthereagreatdealofoverlapbetweentheotherfourbreeds.
DOGS,WOLVES,ANDMEN45
maybe.Usingthismethod,PaulyandWolfe(1957)comparedthreecaninespeciesandobtainedthefollowingfigures:dogwithwolf,88percent;dogwithfox,50percent;foxwithwolf,52percent.Dogsareobviouslymorelikewolvesthanfoxes.Duerst(1942),however,experimentingwithonewolfandonejackal,foundthatthetwoweresimilarlyrelatedtodogs.
Thelimitationsofthemethodarethatitmustbedonewithextremecare,assmallamountsofcontaminationcanproduceverygreatvariationinresults.
smallamountsofcontaminationcanproduceverygreatvariationinresults.Also,mostresultsnowavailablearebasedonantiseraandseraobtainedfromonlyonememberofeachspecies.Thepopulationapproachisstilltobeappliedtothistechnique,anduntilthisisdoneitprovidesonlytentativeevidence.
HISTORICALEVIDENCE
Byandlarge,historianshavebeenlittleinterestedindogsandrefertothemonlyinpassing.Forexample,Trevelyan,inhisEnglishSocialHistory(1943),saysthatacomplaintwasmadeinParliamentin1389thatlaborersandservantskeptgreyhoundsandotherdogsandwerewastingtheirtimehunting.Asaresultalawwaspassedtopreventpeoplewithlowincomesfromkeepingsportingnetsordogs.Suchcasualrecordsindicatethatdogswerepopularandoftenusedinhunting,particularlybythegentry.
InthesamecenturyChaucerwrotehisCanterburyTales,whichcontainvividdescriptionsofcontemporarycharactersandtheiroccupations.ThePrioresskept"smallhounds''ascompanions,andtheMonkwasahuntingman—"greyhoundshehad,asswiftasfowlsinflight."TheWifeofBathmetaphoricallydescribesawoman'sover-fondnessforaman:"Forasaspaynelshewillonhimlepe,"indicatingthatexuberantaffectionwasascharacteristicofthespanielsofthefourteenthcenturyasitistoday.
TheearliestEnglishbookondogswaspublishedin1576,duringthereignofQueenElizabethI.ThiswasactuallyatranslationofapaperinLatinwrittenbyJohannesCaius,a"DoctorofPhisickeintheUniversitieofCambridge,"forwhomthepresentCaius(pronounced"Keyes")Collegeisnamed.ThepaperwasoriginallywrittenattherequestofConradGessner,theSwissnaturalist,whowantedinformationregardingtheEnglishbreedsofdogs.
CaiuswasobviouslyinfluencedbythecontemporaryEnglishsocialsystem,forhesaysthattherearethreekindsofdogs,agentlekindservingthegame,ahomelykindfornecessaryuses,andacurrishkind,"meeteformanytoys."Huntingwasreservedfortheno-
46BEHAVIORPATTERNS
bilityindogsaswellasinpeople.However,Caiusdescribesmanydogswhicharethecounterpartsofmodernbreedsaswellasmanywhichhavedisappeared.
Classifyingdogsaccordingtotheiruse,hefirstdescribesthehoundsashunting
Classifyingdogsaccordingtotheiruse,hefirstdescribesthehoundsashuntingbyscentandhavinglargebagginglipsandhangingears.Heplacesthebloodhoundinaseparategroupbecauseitwasusedtochasebeaststhatwerewoundedandtotrackdownthieveswhohadstolenmeat,particularlyontheScottishBorder.Evenatthattimebloodhoundshadanunusualreputationforbeingabletofollowatrail.
Instillanothergroupwerethe"gasehounds,"usedforhuntingbysight,andhencethename.Suchbreedshaveapparentlydisappeared.Greyhoundswereusedsomewhatdifferently,incoursing,orpursuitbysight,actingandappearingverymuchliketheirmoderncounterparts.
Terriers,derivingtheirnamefromtheFrench"terre,"werebredtocreepintothegroundanddriveoutsmallanimalslikefoxesandbadgers.The"Spaniells"originallycamefromSpainandwereusedbothforhawkingandhuntingbirdswithnets.Agroupofcloselyrelatedbreedswerethesetters.AsCaiussays,asetterwassupposedtofindbirds,lieontheground,andcreepforwardlikeaworm,lyingdownnearthem.Thenetwasthenpreparedandthedog,onsignal,wouldriseandfrightenthebirds,whichthenflewintothenet.Thisdescriptionofsettingbirdsforthenetissomewhatdifferentfromthatgivenbyotherwriters,andperhapstheywereused
inseveraldifferentwavs.
j
Hementionsthe"Spaniellsgentle"asneat,prettydogs,probablyreferringtosomeofthetoybreedsliketheKingCharlesspaniel.Asectionisreservedforthe"homely"dogs,includingshepherddogsandmastiffsorbandogs.Thislastnamereferstothefactthataguarddogwasusuallykepttiedupbyabond,orchain.Finally,thereweremongrels,whichCaiussaid"keepnottheirkind,"includingthe"turnspits,"usedonatreadmillwhichturnedthemeatbeingroastedoverafire.
Amongbreedswhichhavenowdisappearedwerethe"lvemmer,"whichwasmidwaybetweenharriersandgrevhounds,the"tumbler,"usedforhuntingrabbits,andthe"thecvish"dog,whichdidnotbarkandwasusedbypoachersforhuntinginthedark.Ifthisreportiscorrect,barklessnesshasoccurredinbreedsotherthanthemodernbasenji.
Wecanseefromtheserecordsthatsonicoftheprincipalbreedsofmoderndogs
Wecanseefromtheserecordsthatsonicoftheprincipalbreedsofmoderndogswerealreadyestablishedfourhundredyearsago,
DOGS,WOLVES,ANDMEN47
andthattheEnglishwerealreadyimportingbreedsfromothercountries.Howthebreedswererelatedtoeachotherandhowmuchcrossingwasdonebetweenbreedswehavenowayofknowingexceptbyinference.
Anotherbookondogswaspublishedin1686,overacenturylater.RichardBlome'sTheGentleman'sRecreationwasasortofencyclopedia,thefirstpartcoveringtheartsandsciencesfromgrammarandrhetoricthroughhorography,or"sundialling,"tofortificationandheraldry,andthesecondincludingarticlesonvarioussortsofhuntingandotherspecialoccupationsofacountrygentleman.Aswasthecustominthosedays,theexpenseofprintingwasbornebywealthybenefactors,andBlomehonoredthembypicturingtheircoatsofarms.ThebookwasauthorizedbyCharlesIIin1682,butdedicatedtoJamesII,whowasoneofthesponsors.Amongthe228others,thereappearsthenameofGeorge,LordJeffries,heofthe"BloodyAssizes"thatfollowedtheDukeofMonmouth'sshort-livedrebellionin1685.
ButBlomewasnotinterestedinpolitics.Inhisbookhedescribesseveralvarietiesofbeagles:thesouthernbeagle;the"fleet,northern,orcat"beagle,somewhatsmaller;and,finally,averysmalltype,thesizeofalady'slapdog,sometimesusedforhuntingconeys(theoldwordforrabbits)andhares.
LikeCaius,hedescribesterriersassmalldogsusedforfollowingthefoxorbadgerintotheearthandsaysthatadogbredoutofabeagleandamongrelmastiffmakesagoodterrier.Healsomentions"tumblers"and"lurchers,"forhuntingconeys;greyhounds,forcoursing;andbloodhounds,usedfor"harbouring"astag,i.e.,locatingtheplacewherethestagspentthenight,or"harboured."
Hisgreatestenthusiasmwasreservedforspaniels,whichwereemployedfor"springing"andretrievingoffowl.
SpanielsbyNatureareveryloveing,surpassingallotherCreatures,forinHeatandCold,WetandDry,DayandNight,theywillnotforsaketheirMaster.TherearemanyProdigiousRelations,madeinseveralGraveandCredibleAuthors,ofthestrangeAffectionswhichDogshavehad,aswelltotheirDeadandlivingMasters;butitisnotmybusinessoftakenoticeofthemhere;buttoapply
Masters;butitisnotmybusinessoftakenoticeofthemhere;buttoapplymyselftotheSubjectinHand.
Wecanconcludethatdogstorieswereaspopularinthosedaysastheyareatpresent,andmanyofthemjustasdifficulttobelieve.Blomegoesontowritechaptersontheuseofwaterandlandspanielsinthesportoffowling.Hisdescriptionsoftrainingwoulddocredittoanymoderndogbook.
48BEHAVIORPATTERNS
Ofalldogsthereisnonesofitandpropertobemadeasettingdogasalandspaniel,byreasonoftheirnaturalinclinationtorangingandbeatingaboutafield;butanydog,whetherawaterspanieloramongrelbetwixtboth,oralurcherortumbleroranydogthathathaperfectgoodscent,andnaturallyaddictedtothehuntingoffowl,maybebroughttobeasetter.
Thelandspanielwasfirsttaughtto"couchandlieclosetotheground,"thentaughttoliestillwhileabirdnetwasdraggedacrosshim,thentaughttoassociatelyingdowmwiththescentofapartridge(whichBlomesayscanbeduplicatedbyaboiled"bullock'sliver").Intheactualhunt,thespanielfirstquarteredtheground.Whenheindicatedbyhiseagernessandwagginghissternthathehadlocatedthebirds,hewasorderedtoliedownandremainuntilthenetwasthrownoverbothhimandthebirds.Inhuntingpartridge,thetechniquedescribedbyBlomeinvolveddrawinganetoverthecoveybeforeittookflight.
Blomecallstheactualdiscover}'ofthebirds"makingapoint"andremarksthat"somedogswillstandupintheirsetting,wrhichisagreatfault."Aftershotgunswereinvented,birdswerenolongertakenwithanetandnewdogsweredevelopedfromthelandspanielswhichsimplystoppedandpointedwhentheylocatedbirds.Thuscrouchingbecameafaultinitsturn,andallmodernsettersarereallypointers.Onlyinthecockerspanielsdoestheoriginaltendencytocrouchremain,andthesebreedsreadilycrouchandcrawlontheirbellieswhenthreatened.Themodernspringerspanielsweredevelopedto"spring,"orflushbirds;andcockers,whentheyareusedforhunting,areusuallytaughttoflushthebirdsratherthantopoint.However,theystillretaintheiroldcapacityforlearningtocrouch.
Incontrasttospaniels,thebasenjibreedhasashortwrittenhistory.AccordingtoVictoriaTudor-Williams(1946),aprominentEnglishbreeder,basenjiswerefirstsuccessfullvimportedintoEnglandin1937.ThetwoanimalsusedtoformthefoundationstockfortheJacksonLaboratorywerebothdescendedfromfive
thefoundationstockfortheJacksonLaboratorywerebothdescendedfromfivebasenjisimportedintoEnglandinthatyear.Comparedwithmostpurebreddogs,theircoefficientofinbreedingwassurprisinglyhigh(.23,ascalculatedfromtheirpedigreewhichextendsbacktotheirfiveimportedancestors).ComparativefiguresforthefoundationstocksoftheotherfourbreedsareshowninTable2.3,basedonavailablepedigreerecordscoveringatleastfourgenerations.
WeareindebtedtoDr.JamesP.Chapin(1958)oftheAmerican
TABLE2.3
CoefficientsofInbreedingofFoundationStock*
Basenji23
Beagle00
Cockerspaniel01
Sheltie06
Foxterrier00
•Cockersincludeonlythoseanimalsusedinthecrosswiththebasenji.
MuseumofNaturalHistory,whoobservedthisbreedwhileontheMuseum'sCongoexpeditionsin1909-15andlateryears,foradescriptionofbasenjisintheirnativehabitat.Theyoriginallyhadawidedistribution,fromtheFrenchCongoandcentralCongobasinintothesouthernSudanandUganda,andperhapsfurther.TheywereownedandusedinhuntingbvPvgmiesandseveralotherAfricantribes.RecentlytheyhavebeguntocrosswithdogsbroughtinbyEuropeanresidents,andpurestrainsmaybedifficulttofindinthefuture.ThereisnoindicationofcrossingintheJacksonLaboratorystock,inwhichinbreedinghasneverrevealedconcealedrecessivesbelongingtootherbreeds.
Thename"basenji"intheLingalatradedialectofthecentralCongomeans"peopleofthebush."Evidentlytheearlyexplorersaskedthenativesthenameofthebreed,andtheyrepliedthatthoseweredogsbelongingtothebushpeople.ChapinsaysthatthePygmiesoftheIturiforestusedbasenjisforhuntinginmanyways.Thesetribesfrequentlyhuntedwithnets.Menanddogswouldgothroughtheunderbrushanddrivesmallantelopesalongthegametrailstowhereanethadbeenset.Sometimesbasenjiswereusedforflushingbirds,which
anethadbeenset.Sometimesbasenjiswereusedforflushingbirds,whichwouldthenflyintothetreeswheretheycouldbeshotwitharrows.Theywerealsoemployedintrackingsmallgame,andadogwhichhadakeensenseofsmellwashighlyvalued.Thusthebasenjisareageneral-purposehuntingdoganddonotfitintoanyoftheconventionaldivisionsoftheEuropeanbreeds.
Accordingtothebreedstandards,basenjisarebarklessdogs.ThoseinAfricaoccasionallybark,butonlywhenextremelyexcited.Atnightinthenativevillagestheyoftenmakeatremendousnoise,whichChapindescribesasyodellingandwailing.Similarbehavioroccurredinourkennels.
WehavenotbeenabletogetanyauthenticinformationregardingthebreedingseasonintheirnormalhabitatneartheEquator,and
perhapsthereisnoneinthisregionofalmostconstantdaylength.Inthenorthtemperatezone,basenjisbreedonlyonceayear,closetothetimeoftheautumnalequinox.
Livinginthesameregionsasjackals,basenjishavehadamuchbetteropportunityforcrossingwiththemthanhavemostotherbreeds.Thepeculiarvocalizationofbasenjislendssomeweighttothishypothesis.However,jackalnoisesaremuchmoreelaboratethanthoseofthebasenjianddifferentinmanyways.VanderMerwe(1953)saysthattheAfricanblack-backedjackal"yelpslikeadogwhenstartled,"butgivesanundoglikesoundwhencornered:"ke-ke-ke-kek."Thedangersignalwhenpupsarepresentisasoft"wuf."Inthematingseasonthefemalegivesa"shrillbutheartylaugh/'andthemaleanswerswithalonghowl.Thejackalhasahuntingcryorhowldescribedas"ieaaaa-iea-iea-iea"or"nieaaaaa-niea-niea-niea."Whetherjackalandbasenjinoiseshavesomesimilarityremainsanopenquestionthatwillbeansweredonlywhendetailedanalysisofthesesoundscanbemadewiththesoundspec-tograph.
Inotherrespects,thebehaviorofbasenjisandjackalsisquitedifferent.Jackals,likecoyotes,arenotstronglysocialanimals,andtheusualadultgroupisamatedpair.Theyarerarelyfoundinpacks.Basenjis,ontheotherhand,runinco-ordinatedgroupswhenraisedinlittersandbehavemorelikepackanimals.
UsinghistoricalinformationandsuchmodernhistoryasisincludedintheAmericanKennelClubDogBook,wecansaythatmodernbreedshaveoriginatedinfourprincipalways.Thefirstoftheseisthemoreorlessaccidentaldevelopmentoflocalvarieties,suchasthedevelopmentoftheLabradorretrieverinmoderntimes(Smith,1945).Asecondwayinwhichbreedshaveoriginatedis
inmoderntimes(Smith,1945).Asecondwayinwhichbreedshaveoriginatedisbyimportinglocalvarietiesfromdistantparts.ThusthefirstchowwasbroughtfromChinaabout1780(White,1842),andthefirstbasenjiswerebroughttoEnglandin1937.Third,manymodernbreedshavebeendeliberatelydevelopedbycrossbreedingandselection.Amongthesearethefoxterrier,developedtohelpgetfoxesoutoftheirdenswhenthesportoffoxhuntingbecamepopular,andthegoldenretriever,whosebasicstockreportedlywasbroughttoEnglandbyagroupofRussiancircusperformers.TheShetlandsheepdogs,orshelties,wereoriginallysmallnondescriptdogslivingintheShetlandIslands.ThesewerecrossedwiththelargeScotchtolliestoimprovetheirappearanceandlatercrossedwithsomesmallerbreedsinordertoreducethesizeagain(Coleman,1943).Thesheltiebreedersarenowselectingforasmalldogwith
thegeneralappearanceofacollie.OthernewlydevelopedbreedsaretheAiredaleandDobermanpinscher.Finallytherearethebreedswithknownancienthistories,suchasthesalukisoftheMiddleEast,whichtheCrusadersprobablybroughtbacktoEnglandtobetheancestorsofEnglishgreyhoundsandtheirrelatives.Spanielsandhoundsalsohavehistoricalrecordsdatingbackmanycenturiesandhavebeensubdividedintoseveralmodernbreeds.
Incidentally,theclassificationschemeoftheAmericanKennelClub,aswellasthesomewhatdifferentoneoftheKennelClubofGreatBritain,isnotbasedoncommonancestry,butonsimilaruses(Scott,1963Z?).Forexample,thenon-sportingbreedsincludesuchanimalsofwidelydifferentancestryasthepoodles,descendedfromhuntingdogsofwesternEurope,andthePekingese,whicharetoydogsimportedfromChina.ThusthemoderndogfanciersfollowCaiusinclassifyingbreedsbyfunctionratherthanorigin.
EVIDENCEFROMGENETICS
BeginningwithDarwin,studentsofheredityhavewonderedhowthedomesticdogcouldbesovariable,andDarwinhimselfthoughtthatdogsmusthavebeendescendedfromatleasttwospeciesinordertoaccountforthevariationofmodernbreeds(Darwin,1859).
AtthattimetherewasverylittleaccurateinformationaboutthenatureofwolvesandnoneconcerningthepossibilityofvariationprovidedbysimpleMendeliangenetics.Recentstudiesshowthatthewolfisahighlyvariablespeciesinthewild.Murie(1944)couldrecognizeindividualsasbeingdistinctlydifferentevenwithinthesamepack.Jolicoeur(1959)findsgreatvariationinthecolorandskullmeasurementsofCanadianwolvesfromonelocalitytoanother.Youngand
skullmeasurementsofCanadianwolvesfromonelocalitytoanother.YoungandGoldman(1944)pointouthowdifferentwolvescanbeinphysicalmeasurements.TherewereendlesslocalvarietiesbeforewolveswereexterminatedovermuchofNorthAmerica,andthenorthernwolvesweremuchlargerthanthesouthern.Thismeansthatwolvesarenaturallyhighlyvariableandcanbetrulycalledapolymorphicspecies.Theoriginaldomesticatorsofthewolfthushadplentyofvariabilityfromwhichtochoose,exceptintheproportionsoftheskeleton,whichappeartobehighlyuniform(Hil-debrand,1954).
Aswehaveseen,thewidevariationinstructureindogbreedsisproducedbyarelativelysmallnumberofmutationssuchasthebulldoghead,shortlegsandlopears.Inadditiontothese,thereareallthevariationsincoatcolorandhairlengthandtexture.
52BEHAVIORPATTERNS
Finally,thereisagradedseriesinbodysize,fromthedwarfthroughmiddle-sizeddogstothegiantbreeds.Ifweassumethattherearefivedifferentmutationsofbodyformandperhapstenofcoatcolor,wecouldobtainfromthematotalof215combinationsoftraits.Thisamountsto32,665.Evenwithonly10mutations1,024combinationsarepossible,farmorethanthefewhundredknownvarietiesofdogs.Itisnotunreasonabletosupposethatasmanvas10to20majormutationshaveoccurredandpersistedindogsinthelasttenthousandyears,especiallvinviewofthetendencyofpeopletobeinterestedinandattempttopreservenewandfreakishanimals.Inshort,mutation,selection,andMendeliangeneticswillaccountforthevastamountofvariationindogswithouttheneedtosupposeadualancestry.Asamatteroffact,thedifferencesbetweenspeciesinthegenusCanisarenotthesortwhichdifferentiatedogbreeds.Therearenowildspecieswithlopears,curlytails,orshortlegs.Acrosswithanewwildspecieswouldbringinrelativelylittlevariationofthistype.
Amoreprecisewayofobtainingevidenceonbasicgeneticrelationshipswouldbetomakeadetailedstudvofchromosomesindifferentdogbreedsandwildspecies.Chromosomestructureandnumberaffectthecapacitytohvbridize.Ifanimalsfromtwospeciesmate,theiroffspringreceivesasetofchromosomesfrombothparents.Theembryomaybeabletodevelopevenifthetwosetsdonotmatcheachother,butwhenitsgermcellsareformed,thechromosomesmustpairexactlyintheprocessofmeiosisorthegermcellswillnotdevelop.Thusinacrossbetweenthehorseandthedonkey,thehvbridmulesareusuallysterile.
acrossbetweenthehorseandthedonkey,thehvbridmulesareusuallysterile.However,onceinaIons;whilechromosomeswillbelostoraccidentallvarrangedinacompatibleorder,sothatsomemuleshavebecomeparents(Anderson,1939).SterilitvoftheFihvbridisthusanindirectindicationofchromosomeincompatibilityandthefactthattheparentsreallybelongtotwodifferentgeneticpopulations.
InthegenusCanis.Iljin(1941N)crosseddogsandwolvesandcarriedtheiroffspringtothesecondgenerationwithnoindicationofsterility.Thisistheonlvcontrolledgeneticexperimentwithhybrids,butaccordingtonaturalists'reports(Grav.1954),dogshavebeencrossedwithbothcovotesandjackalstoproducefertileFihybrids.TheresultwithjackalsisinconsistentwithMatthey's(1954reportofchromosomedifferences,andthisreportneedstobeverifiedbydirectexperiment.
Whiledogshavebeencrossedwitheven-othermemberoftheiiisCanis,wolveshavenotbeencrossedwitheithercoyotesor
DOGS,WOLVES,ANDMEN53
jackals,probablybecauseofdifferencesinsize.Seitz(1959)madeasuccessfulmatingbetweenacoyoteandjackalbutdidnotdeterminethefertilityoftheFihybrid.Atthispointwecannoteliminatethepossibilitythatatsomepointdogshavebeencrossedwithaspeciesotherthanwolves,andthatsomeoftheintroducedgeneshavepersisted.
TABLE2.4HybridsReportedbetweenSpeciesortheGenusCants
Withthemethodsofstudyingchromosomesrecentlydevelopedinstudiesofhumangenetics,itshouldbepossibletomakeaccuratecomparativestudiesofthegenusCanis.Suchinformationshouldthrowconsiderablelightontherelationshipsbetweenthedoganditswildrelativesaswellasthosebetweenthedogbreeds.However,thismustbedoneonpopulationsratherthanonscatteredindividualsinordertoprovideworthwhileevidence.
Littleinformationonthispointisnowavailable.Thedogitselfhasaverylargenumberofchromosomes,78inall,butnoonehasexaminedthechromosomesofthewolf.Theyellowjackal(C.aureus)ofAsiaandNorthAfricahasonly74chromosomes(Matthey,1954),whichindicatesthatitcouldnotbecloselyrelatedtothedogbreedsthathavebeenstudiedsofar.Ahmed(1941)studiedthechromosomesandtheirbehaviorinSealyhamterriers,spaniels(breednot
chromosomesandtheirbehaviorinSealyhamterriers,spaniels(breednotreported),andacrossbetweenspanielsandManchesterterriers.Alltheanimalshadthesamenumberofchromosomes,78,butAhmedfoundindicationsofdifferencesinappearanceandbehaviorofthechromosomesinthedifferentbreeds.ThesewereallbreedsfromtheBritishIsles,anditispossiblethatlesscloselyrelateddogsmightshowmoreextremechromosomaldifferences.
OtherspeciesofCanidaearequitedifferentfromthedog(Matthey,1954).Theredfoxhas38chromosomes,andanotherspeciesoffox(Vulpesruppelli)has40.Therare"raccoondog"ofEuropehas42,whilethefennec,asmallfoxlikeanimalofAfrica,has64chromosomes.Summingupthepresentevidence,wecanonlysaythatthereisnonecessitytopostulatemorethanonewildancestralspecies,andthemostlikelycandidateisalocalvarietyofthewolf,Canislupus.
54BEHAVIORPATTERNS
CONCLUSION
Noonecanaccuratelyreconstructthepast,andparticularlytheprehistoricpast.Themostthatwecandoistotaketheavailableevidenceanddrawaprobableconclusion.Fromwhatwehaveseeninthischapter,alltheevidencepointstowardthewolfasthemostprobableancestorandclosestrelativeofthedomesticateddog.
Wecannotsayexactlywheredomesticationfirstoccurred,forthearcheologicalstudyofprehistorichumanremainsanddomesticanimalsisfarfromcomplete.However,theoldestauthenticskeletonsofdogsarefoundinDenmark,anditseemslikelythatthefirstdomesticdogswereproducedsomewherenearbyinCentralEurope,orpossiblyinthe"fertilecrescent"ofMesopotamia.Oncedomesticated,theyspreadslowlyovertheworld.Thefirstdogwasavaluableinventionforaprimitivepeople,andwecansupposethatneighboringtribesheardofthesenewanimalsandgraduallyacquiredthem.
Presentknowledgedoesnotgiveusanaccuratedateforwhenthisoccurred.ThedogsofDenmarkhavebeendatedasearlyas8000B.C.,butnotbymodernradiocarbonmethods.Eventhistechniqueisstillinitsinfancy,andmanymorefactsareneededbeforewecometofinalconclusions.Assumingthattheabovedateiscorrect,itwasfifteenhundredyearsbeforedogsspreadtoMesopotamia.In6750B.C.,theprimitivefarmingvillageofJarmoinIraqhaddomesticatedgoats.Atthesamesitewasfoundadoglikefigurinewithacurlytail.IntheruinsoftheJerichoof6500B.C.,therewereactualdogbones.Afteranotherthree
oftheJerichoof6500B.C.,therewereactualdogbones.Afteranotherthreethousandyears,dogshadspreadtoneighboringEgypt.
FromEgyptthedogspreadsouthwardandeastwardintotropicalregions,becomingadaptedtoexistenceinahot,humidclimatewhichtheirwolfancestorshaveneverseen.Werth(1944)arguesthatthebasenji,dingo,andcertainmedium-sizeddogsofPapuaandtheEastIndiesaredescendantsoftheseearlysoutherndogs.Theyareoutwardlysimilarinappearance,beingusuallyyellowincolorwithshorthair,prickears,andcurlytails.Whilesuchsuperficialsimilarityisnotperfectproof,thehypothesisisaplausibleone.
FromCentralEuropedogsspreadnorthwardandgotintothehandsofhuntingtribes.TherearenodogremainsfromtheEnglishhuntingvillageofStarCarrdatedat7200b.c,butdogseventually
DOGS,WOLVES,ANDMEN55
wereacquiredbyEskimosandtheireasterncousinswhowentovertheBeringStraitintoNorthAmerica.
Wecanconcludeonthebasisofpresentfactsthatthedomesticationofthedogtookplaceabout8000b.c.Thismeansthatthedoghashadadomestichistoryofsometenthousandyears,andthatsomefourtoeightthousandgenerationsofdogshavelivedupontheearthwithabundantopportunitiesformutationsandgeneticvariationstooccur.
Astohowdomesticationfirsttookplace,wecanonlyguess.Probablyithappenedverysimply.InAlaskaandothernorthernareaswherepeoplestillliveclosetowolves,wolfcubsareoftencapturedeventoday.Someofthembecomeacceptableaspetsorsleddogs.Primitivepeopleseverywhereintheworldfrequentlyadoptyoungbirdsormammalsaspets.WecansupposethatwolveshungaroundtheprimitiveagriculturalvillagesofEuropescavenginganywastefoodorbonesthatwerethrownaway,andthatthehumaninhabitantsmightfrequentlycomeacrosswolfcubsinthespring.Menseemtohavedomesticateddogsaboutthesametimethattheybegantoliveinpermanentvillages.Contrarytowhatonemightexpect,thereisnoevidencethatearlierhuntingtribeshaddogs(Werth,1944),andtheusefulnessofthedogasahuntinganimalwasprobablydiscoveredlater.
Wecanimagineawolfpuppygrowingupinavillage,fedatfirstandlaterexistingonscraps.Aswolvesanddogsstilldotoday,itbecameadoptedinto
existingonscraps.Aswolvesanddogsstilldotoday,itbecameadoptedintohumansocietyandestablishedaterritoryarounditshome.Itssensitivitytotheapproachofstrangeanimalsandpeopleatnightmusthavebeenimmediatelyvaluable.Later,whengoatswerealsodomesticated,itsdog-likedescendantscouldwarntheirownersoftheapproachofwildwolveswhichmightattacktheherd.
Atfirsttheremusthavebeensomeconfusionbetweentamewolvesandwildones,butveryearlyindomesticationamutationforcurlytailmusthaveoccurred.Wildanddomesticwolvescouldthenbeeasilytoldapart.Also,theremusthavebeenanearlyselectionforanimalswhichcouldbemoreeasilycontrolled,andthismeantthedevelopmentofsmallormedium-sizedwolveswithsmallerandlessdangerousteeth.
Thusthebasictraitsofdomesticdogswereestablished.Asdogsspreadfromvillagetovillagethroughouttheworld,therewasanidealopportunityforwhattheevolutionistscalladaptiveradiation,aphenomenonwhichalwaysoccurswhenagroupofanimalsmoves
intoavacanthabitat(Fig.2.2).Suchconditionsareidealforthesurvivalofvariationsbecausewholenewpopulationscanarisefromafewvariableindividuals.
Asaresult,eachvillagehadasmallpopulationofdogssomewhatdifferentfromthoseoftheothers.Subdivisionsintosmallpopulationswouldbeidealforfurthergeneticchange.Allthis,coupledwiththehumantendencytoselectandsaveanimalswithindividualpeculiarities,couldaccountfortheoriginofdifferentbreeds.Therearemanyearlyhistoricalreferencestolocalitiesfamousfordifferentdogs,suchastheMolossianhoundsofclassicalantiquity.
Atthesametime,wecannotconcludethateachbreedwascompletelypureandseparatefromthetimeofitsorigin.Onthecontrary,thepromiscuoushabitsofdogs,aswellasthedeliberatecrossesmadebytheirowners,tendedtomakealldogsinagivenareasomewhatrelatedtoeachother.Itisonlywithinthelastcenturythatbreeders'clubshaveattemptedtoproducepurebreedsofdogs.Evenso,thehistoryofthemodernEuropeanbreedsshowsthatmanyofthemweredeliberatelyproducedbycrossingseveralbreedstogethersothatwhileeachbreedmayhavecertaindistinctivecharacteristics,Europeandogsareactuallyinterrelatedinmanyways.
Sizepreventslargedogsfrominterbreedingwithverysmallones,butwhenwe
Sizepreventslargedogsfrominterbreedingwithverysmallones,butwhenweplacesizemeasurementsonagraph,weseethatthereiscontinuousvariationfromtheChihuahuatotheGreatDane,withthepossibilityofcrossinganywherealongthelinebetweenanimalsofsimilarsize.
Allthismeansthatdogsbelongtoonlyonespecies,asLinnaeusoriginallysupposed,inspiteoftheirenormousphysicalandbehavioralvariability.Theonlyotheranimalwhichshowsanythinglikethesamedegreeofvariationismanhimself.Dogsaredogsandarebasicallyrelatedtowolves.Thisistrueoftheirbehavioraswellastheirphysicalstructure,aswillbeseeninthenextchapter.
THESOCIALBEHAVIOROFDOGSANDWOLVES
INTRODUCTION
Anyonewhoownsadogisimpressedwiththeextraordinarydegreetowhichsuchananimalbecomespartofahumangroup—docile,affectionate,andprotective.Onemaywellwonderwhetherthefamilypetisreallydescendedfromawolfand,evenifso,whetherselectionhasnotchangedhisbehaviorsocompletelythatitisnowalmosthuman.
Weattemptedtoanswerthisquestionbyobservingwhatgroupsofdogsdidwhenoffbythemselveswithnohumanbeingsaroundthem(Scott,1950).Wewerefortunateinhavingplentyofspace,andforequipmentwehadthreeone-acrefieldssurroundedby7-footwoodenfences.Thedogsinsideonlysawpeoplewhocamecloseenoughtobevisiblethroughthecracks,andwemadesurethishappenedasseldomaspossible.Webuiltsomeobservationplatformsintheneighboringtreesandfromthesevantagepointswatchedwhatthedogsweredoingforoverayear.Inonepenweputalitterofyoungfoxterriers,inanotheralitterofScottishterriers,andinathirdalitterofbeagles.Asthemonthspassed,puppieswerebornintwoofthegroups,andwewereabletowatchthebehaviorofthedogsandtheiroffspringastheylivedunderconditionsofconsiderablefreedom.
Oneofthedifficultieswithstudyingdogsisthateveryoneknowsdogs.Eachofustriedtowritedownwhatthedogsdid.Beingwell-trainedscientists,wetriedtobeasaccurateandconscientiousaspossible.OurfirstnotesusuallyindicatedthatdogBimovedacrossthefield,whiledogB2moveddownthefield,withverylittle
57
57
otherinformation.Weweresofamiliarwiththedetailsofdogbehavior,suchastailwagging,sniffingtheground,etc.,thatweoverlookedthementirely.Astimewenton,however,webegantonoticethesedetailsandrealizedthatthesewerepreciselythekindofinformationwewanted.Wedidnotcaresomuchwhereadogwentashowhedidit.Andsoinsubsequentnoteswebegantodescribesuchdetailsashowamalemightapproachafemaleandsniffhertailwhileshegrowledathim.Togiveanactualexample:"B7againplayswithpup.Puprollsover—cries.B7sniffspup—pupruns—pupwagstail—criesloudly.B7playingwithit—chasingit.PupgrowlsatB7."
Thuswehadthebeginningofacollectionofthekindsofbehaviorpeculiartodogs.Indeed,thisisthefirsttaskinstudyingthebehaviorofanyanimal.Itisdonethroughobservationandisprimarilyacollector'sjob,agooddeallikecollectingspecimensofthevariouskindsofinsectsorotheranimalsinanarea.Insteadofmakingabiologicalsurveyofaregion,weweremakingapsychological(orethological)surveyofbehavior.
THEUNITOFBEHAVIORSTUDYISTHEBEHAVIORPATTERN
Asweleafthroughthenotesweoftenfindsuchitemsas:"DogTiscratched."Usuallytheobserverdidnothavetimetodescribethisindetail,butthephraseconjuresupapictureofthedogliftingonehindlegandscratchingitsshoulder,neck,oranyregionthatitcanreachinthisway.Anyonewhohashadapetdogknowsthatyoucanproducethisbehaviorbyticklingthedogalongitsside,settingoffasimplereflexwhichthedogcannotcontrolinanyvoluntaryway.Thisappearstobeasimpleandunifiedpieceofbehaviorhavingthegeneralfunctionofgrooming.
Anobservantdogowneralsoknowsthatthisisnottheonlywayinwhichadogrespondstoanitchingspot.Ifitisonhishindleg,hemayattackitwithhisteeth;ifitisonhisback,hemayrolloverandoverontheground.Thuswehavealistofthreealternatewaysinwhichdogsrespondtothesamegeneraltypeofstimulus.
Inanothernotewefindthat"someonewalkeddowntheroad.Bi>rantothefenceandbegantobark."Hereisanothersimplepieceolbehavioi—barking.Theeffectwastoarousealltheotherdogsinthegroup,whichrushedoverandbegantobarkalso.Itlooksasifbarkinghasthefunctionofanalarmsignal.AnothertimetheScottishterriersbeganchasingbutterflies,leapingintotheair
AnothertimetheScottishterriersbeganchasingbutterflies,leapingintotheairand
SOCIALBEHAVIOR59
snappingatthemastheyhoveredoverthefield.Andsowecontinuedtocollectalonglistofcaninehabitswhichmakeupadog'srepertoryofbehavior.
Intheend,wehadaninventoryofpatternsofbehavior(Table3.1).By"behaviorpattern"wemeanauniqueandindependentpieceofbehaviorhavingacompleteadaptivefunction.Itmaybeasimplereflexlikethescratchingreflex,oritmaybeapieceofvoluntarybehaviorsuchasinvestigatinganotherdogwiththenose.
Behaviorisageneralandelastictermwhichcanincludealmostanysortofactivityexhibitedbyanentireindividual.Abeliaviorpatternmeanssomethingmoredefinite—anaturalunitofbehaviorwhichhasafunctionbyitself.Onetestforcompletenessoffunctionistoattempttosubdividethebehavior.Forexample,thescratchreflexcanbedividedintoliftingthehindpawanddrawingitdownward.Liftingthehindpawisasubdivisionofbehavior,anditmayhaveanyoneofadozendifferentfunctionsaspartofdifferentpatternsofbehavior.Asweattempttoreducebehaviortoitssimplestparts,weknowthatwearenolongerdealingwithabehaviorpatternwhenspecificfunctiondisappears.
Oncewehaveisolatedsimplepatternsofbehavior,wecanseethattheycanbecombined:eitherinseries,aswhenadoggoesthroughthepatternsofbehaviorleadingtomating,or(morerarely)simultaneously,byperformingtwoactionsatthesametime.Onetestoftheindependenceofabehaviorpatternistoseewhetherornotitcanbecombinedwithothersindifferentsequences.Inhigheranimalslikedogstherearecharacteristicallyanumberofbasicbehaviorpatternswhichcanbecombinedandrecombinedinanumberofways.Weseldomfindlongsequencesofstereotypedbehaviorsuchasarecommonintheloweranimals.
Behavioralsystems.—Anycollectorisfacedwiththeproblemofclassification.Ifhecollectspostagestamps,theyhavetobesortedbycountryandbyyear.Ifitisinsectspecimens,hesortsthemaccordingtotheirresemblancestooneanother,placingallsimilarspecimensinthesamepileandcallingthemaspecies.Behaviorpatternscanbeclassifiedinmanyways,butthemostbasicandimportantmethodisbyfunction—theadaptiveeffectofbehavior.Whenwedothiswefindthatalmostallbehaviorpatternscanbesortedintoninegroups(Scott,1950).TheseareessentiallythesameaswhatKrushinskii(1962)hascalled"generalbiologicalformsofbehavior."
Onebasicfunctionofbehavioristoprovidefortheintakeofnutritivematerialsintothe!>ody.Thisincludesbothsolidsand
60BEHAVIORPATTERNS
liquids.Adogcharacteristicallylapswaterandliquidfoodswithhistongue,standingwiththetaildown.Ontheotherhand,hedealswithsolidfoodbybitingandchewing.Onecharacteristicpatternistolieflat,holdinghisfoodwithhisforepawswhilehetearsoffsmallpieceswithhisteeth.Thepatternsofdrinkingandeatinghaveacommonfunctionandarecalledingestivebehavior.
Averydifferentsortoffunctionisinvolvedinagonisticbehavior,i.e.,adaptationtoasituationofconflictwithanotheranimal.Thedog'sresponsesmayincludethepatternsofbarking,growling,biting,runningaway,orrollingonthebackandyelping.Eachofthesebehaviorpatternshasaspecificfunction,buttheyallhaveacommongeneralfunctionandbearatleastalooserelationshiptoeachother.Takentogether,theyformabehavioralsystem,bywhichwemeanagroupofrelatedbehaviorpatternshavingacommongeneralfunction.
Thesearenotthesameastheorgansystemsofphysiology,althoughtheymayberelatedtothem.Ingestivebehavioriscloselyrelatedtothealimentarysystemwithinthebody,but,aswithallbehavior,itinvolvesthenervoussystemandmuscularsystemaswell.Asystemofbehaviorisnotsomethingwhichcanbedissectedoutofthebody,butratheranattributeofthebodyasawhole.Eachoneincludesagroupofrelatedbehaviorpatternswithunderlyingphysiologicalreactionsinvariousorgansystems.Inshort,thesearefunctionalsystemsatahigherleveloforganization—thatofbehavior.Scientificallyspeaking,thisisthedomainofthetwinsciencesofpsychologyandethology.
domainofthetwinsciencesofpsychologyandethology.
Instinct.—Theseconceptsofthebehavioralpatternandthebehavioralsystemarereplacingtheolderandlessexactideaofinstinct.Peopleusedtosaythatadoghadaninstincttoscratch,ortoherdsheep,ortofight.Aninstinctmightthusrefertoeitherasimplebehaviorpatternoranorganizedgroupofpatternsoreventheunnamedandunknownimpulseswhichcausedananimaltoact.Whileithadconsiderableutilityforearlybiologists,theconceptistooinexacttobeofmuchvalueinmodernscientificworkinthedescriptionofbehavior.Itemploysthesamewordforeitherthepart,thewhole,orthecauseofanorganizedpieceofbehavior.
Inaddition,instinctwasoftenusedasafinalexplanationofbehavior.Atonetime,scientistsclassifiedbehavioraseitherInstinctiveorlearnedandoftenfeltthatifbehaviorcouldbelabeledinstinctivetheyhadexplainedit.Incontrasttothisolderusage,theterms"patternofbehavior"and"behavioralsystem"donotimplyexplanations,butaresimplynamesforwhatweobserve.Explain-
ingtliemisamatterofworkingouttheircauses,andwefindthatitisveryseldomthatanypieceofbehaviorcanbeexplainedonthebasisofonesimplecause.
Therelationshipbetweenbehavioralsystems.—Anyonewhoobservesdogsrunninginthestreetsknowsthateliminativeandsexualbehaviorarerelatedtoeachotherintheseanimals.Malesarehighlystimulatedbysmellingtheurineofareceptivefemale,andamaleabouttomatewithafemalemaygothroughanelaboratepatternofeliminativebehaviorbeforedoingso.Arewedealingherewithonebehavioralsystemorwithtwo?Theansweristhatinotheranimalspecieseliminativebehaviormaybeentirelyunrelatedtosex,asitisinbirds,andhencedefinitelybelongstoaseparatesystem.Evenindogs,mosteliminativebehaviorhaslittletodowithsexualbehavior.Abehavioralsystemisagroupofbehaviorpatternswhichisinmostspeciesunrelatedtoothersystems;however,thepossibilitythatanewrelationshipbetweenbehaviorpatternscanbeformedthroughtheevolutionofbehaviorisalwayspresent.
Anotherexampleofassociatedbehavioralsystemsindogsistherelationshipbetweenagonisticbehaviorandeating,sincedogsfightwiththeirteeth.Allbehaviorsystemsaretosomeextentrelatedtoeachotherbybelongingtoacommonsystem,theindividualorganismwhichdoesthebehaving.
MODIFICATIONOFBEHAVIORALSYSTEMSOFTHEWOLFIN
MODIFICATIONOFBEHAVIORALSYSTEMSOFTHEWOLFINVARIOUSBREEDSOFDOGS
Thenaturalsocialgroupofthewolfisthepack,whichcanbeassmallasasinglepairoraslargeastwenty-fiveorthirtyindividuals.Forthemostpart,thegroupsaresmall,thewolfpackobservedbyMurie(1944)hadsixmembers—fourmalesandtwofemales.Inoneyeartherewasonlyonelitter,butinthenextbothfemaleshadyoung.Thepackhuntedarangeatleastfiftymilesacross,usuallygoingouttogetherintheeveningandreturningthenextmorning.Thecubswereraisedinaden,andtheadultsguardeditandtheimmediatelysurroundingareaasaterritory.
Inourlargeoutdoorfieldsweestablishedartificialpacksofdogs,butsincetheirrangewaslimitedbyfences,theycouldnotshowallthebehaviorofwildwolves.Sometimestheywouldwanderoverthefieldasindividuals,apparentlyinvestigatingeachcornerandtuftofgrass.Atothertimestheymightbeexcitedbyasoundfromoutsidethepenandallrushtowarditasapack.Nostrangedogs
:ZBEHAVIORPATTE=
couldenter,butifastrangepersoncamein,thegroupwouldretreatashortdistanceandrunbackandforth,barkingattheintruder.Inalaterexperiment,Kin^19-54)introducedstrangedogsintosuchagroupandsawconsiderablehostility.Theentirefieldwasevidentlyhometerritorytothepack,itssizebeingpossiblyslightly-smallerthanthehometerritorydefendedbyMurie'swolfpack.Exceptwheretheyareallowedtorunwild,domesticdogsrarelyformstablepacks,althoughdogsinaneighborhoodsometimesjointogetherandrunintemporarygroups.Ahousedogusuallyhasitsclosestsocialrelationshipswithitsowners,sothattheycorrespondtothewolfpack.Thedenareaisthehouse,andthedogsdefendtheyardarounditasaterritoryjustasdowolvesaroundtheden.Mostdogsarewellfedandhavenoneedtohunt,butwillneverthelessmakeregularjourneysawayfromthehouse,markingscentpctheygo.Theirrangeisusuallymuchsmallerthanthatofwolves,oftennotmorethanamileortwoacross,althoughsomedogsmoveovermuchgreaterdistances.
Thusdogsinseneralshowthesamebasiclivinghabitsastheirwildancestors.Wemaynowraisethequestionwhetherselectionanddomesticationhaveimportantlymodifiedbehaviorinthevariousdogbreeds.Toobtaintheanswerwemaycomparethebehaviorofdomesticdo^swiththatofwolves,chieflvasdescribedbvMurie1944)andCrisler1958inAlaska,by'SchenkelU947^inthezoologicalgardenofthecityofBaselinSwitzerland,andmorentlybyGinsburg
zoologicalgardenofthecityofBaselinSwitzerland,andmorentlybyGinsburg(1963)intheBrookfieldZooinChicago.Table3.1comparesdogandwolfbehavior,butalsoincludestheiorpatternsoffoxesandcoyoteswhenthesehavebeendescribed.Foxesshowallthebehaviorpatternsofdogsandwolves,atlea^tina^li^htlymodifiedformITembrock,1957\withthecantexceptionofattitudesofdominanceandsubordination.Itwillberecalledthatfoxesdonotruninpacks.Bothfoxe^tesshowanagonisticpatternnotfoundindogsorwolvhtheanimalstandswitharchedbackandloweredhead,likea>pittingcatexceptthatthetailisdown.
behavior.—Thecourtshipandmatingbehaviorofwolvesrbeencb>ervedindetailinthewild,butobservationsoncaptiveanimalsshowessentiallythesamebehaviorpatterns
Littlesexualbehaviortakesplaceexceptduringtheperiod
ptive.Thefirstphvsiologk>festrus
tbleedingfromthevagina,whichmayappeara-earlyas
er.Theentireperiodfromthispointuptothetimewhen
stobereceptivemaybeaslongasforty-fivedays.
TABLE3.1BehavioralSystemsandKnownBehavioralPatternsintheFamilyCanldae
SystemandPattern
(I=Infantileonly)
Dog
Investigativebehavior:
Walkingorrunningwithnosetoground,
sniffing
Headinair,sniffing,mayrunfromsidetoside
Sniffinganaland/orgenitalregion
Sniffinganaland/orgenitalregion
Sniffingnoseorface
Headraised,earserect(listeningandlooking)
Nosingandsniffingurineorfeces
Crawlingforward,movingheadfromsideto
side,sniffing(I)
Epimeleticbehavior:Shelterbuilding:
Turningaroundbeforelyingdown
Diggingbedindirt
Diggingenlargementofden
Grooming:
Scratchingself
Rubbingagainstobject
Rubbingorrollingonground
Bitingownfur
Shakingself
Lickingowngenitaloranalregion
Lickingpuppies,chieflyingenitalandanal
regions(eatingexcreta)
Feeding:
Allowingpuppiestonurse
Vomitingfoodforpuppies
Vomitingfoodforpuppies
Carryingfoodtopuppies
Foodcaching(buryingfood)
Miscellaneous:
Carryingpuppiestonest
Pushingpuppieswithnose
Whining(possiblywarning)
Et-epimeleticbehavior(attentiongettingorcaresoliciting):
Whining
Yelping
Tailwagging(specialkindsalsoseenwith
agonisticbehavior)
Lickingfaceorhandsofperson,usuallywith
tailwagging
Touchingwithpaws_
Allelomimeticbehavior(oftencombinedwithet-epimeletic,investigative,andagonisticbehavior):
Walkingorrunningtogether
Sittingorlyingdowntogether
Gettinguptogether
Sleepingtogether
Howlinginunison
Howling,solitary(loneliness)
F,NF
F,NF,N
F,N
F,N
N
F,N
F
F,NF
E
F,N
F
F,N
N
F,N
N
N
NNN
F,NN
F,N
F,N
N
F,N
F,NF,NF,NN
N
Wolf
Coyote
Fox
M
Y,S
M,S
M
Y,S
M?
MM
M,Y
Y
M,YM,C
YYY
M
S
M.Y.S
M
S,CM
MMMM
M,Y,S,CM,Y
M
M
ivr
F=Field;N=Nursery;K=Kennel;E=Elsewhere(whereobservedindogs)
M=Murie;Y=Young;S=Schenkel;C-Crisler;T=Tembrock(wherereportedinothercanid?)?=Behaviorimplied,notdirectlydescribed..
•Characteristicallydifferentfromwolvesordogs—higherpitched,interspersedwithbarking.
C4
BEHAVIORPATTERNS
TABLE3.1—Continued
SystemandPattern(1=Infantileonly)
Dog
Woif
Agonisticbehavior(patternsassociatedwithconflict):Fightingandpredation:
ChasingF
BitingF
SnappingteethK
Pawing(sometimesinstandingposition)....N
Snarling(showingteeth)F,X
F,NF,NK
Growling
Barking
Waggingtipoftail
Tailswitching
Playfulfighting,similartoabove,butlessintense,includespanting
Pouncingorspringing
Tossingsmallgameintoair
Herding
Defenseandescapereactions:
Sitting
Crouching
Runningaway
Yelpingandshowingteeth
Tailbetweenlegs
Rollingonback,pawingandextendinglegs..Attitudesofdominance:
Forepawsonback,growling,tailerect(maybiteneck)
Standingoverdogonground,growling
Standingorwalkingstiff-leggedwithtailerect
Headdown,backarched,taildown
Mounting,taildown,neckbiting,without
pelvicthrusts
Attitudesofsubordination:
Allowingdominantanimaltoplacefeetonback,tailerect
Taildown
Tailbetweenlegs,crouching,earsdepressed..
Rollonback,legsextended,tailbetweenlegs
Miscellaneous:hairraising
Sexualbehavior:Male:
Runningwith?.
Forepawsextended,bodythrownbackonhaunches,headtooneside
Licking9genitalia
Mounting
Clasping
Pelvicthrusts
Copulatorytie...
Female:
Runningwithcf
Forepawsextended,bodythrownbackonhaunches,headtooneside
F.N
N
F,XF,XXF,N
F,X
X
X
X
M,VM.Y.Y,S
M,Y,M,Y.M.YS
s
M.SM
M
Y.C
YMMS
v.s
M
S
M-.S
M.-S
C
sy?
Y?
Y
If?,C
Coyote
MM
Fox
M
M
T(follow)
F=Field;N-Nursery;K-Kennel;E=Elsewhere(whereobservedin
M-Murie;V=Young;S-Schenkel;C-Crisler;T-Tembrock(wherereportedinothercanids)■implied,notdirectlydescribed.
differentfromwolvesordogs—higherpitched,interspersedwithbarking.Notedifferencesfromwolvesanddogsindominance-subordinationbehavioroffoxesandcoyotes.Informationincomplete.
SOCIALBEHAVIOR
TABLE3.1—Continued
SystemandPattern(I=Infantileonly)
Mounting
Clasping
Pelvicthrusts
Standingford"
Tailmovedtooneside
Both:
Both:
"Wrestling."forepawsaroundeachother's
necks
Lliminativebehavior(seecloselyrelatedpatternsofinvestigativebehavior):Male:
Micturitionwithall4legsextended(I)
Micturitionwithliftingofhindleg,usually
inplacesusedbyotherd"'s
Female:micturitioninsquattingposition
Bothsexes:Wandering,nosinggroundbeforedefecation
Defecation
Scratchinggroundwithall4feetfollowing
defecation(rarein9)
Defecationandurinationinplacespreviously
used
Ingestivebehavior:
Lapping,tailoutanddown
Chewingandswallowing,sametailposition..
Gnawing,holdingfoodwithpaws
Eatinggrass
Sucking,pushingwithhead,alternatelypushingwithforepaws,hindfeetpushing,tail
outanddown(I)
outanddown(I)
Comfort-seekingbehavior(shelter-seeking):
Lyinginaheap(I)
Lyingclosetogether
Curlingup
Miscellaneousmotoractivities:
Twitchingwhileasleep(I)
Stretching
Yawning
Rollingover
Dog
N
N
N
F,N
F
KF,N
F,N
F,N
K,N
F,N
F,NNKF
F,NNKF
N
NFF,N
NF,N
F,NF,N
Wolf
Y,S
Y
Y
Y,SS
M
M
M,C
M
Coyote
M
Fox
F=Field;N=Nursery;K■=Kennel;E=Elsewhere(whereobservedindogs)
M=Murie;Y—Young;S=Schenkel;C■=Crisler;T=Tembrock(wherereportedinothercanids)
?=Behaviorimplied,notdirectlydescribed.
*Characteristicallydifferentfromwolvesordogs—higherpitched,interspersed
*Characteristicallydifferentfromwolvesordogs—higherpitched,interspersedwithbarking.
orroughlysixweeks(YoungandGoldman,1944).AcaptivewolfdescribedbyMurie(1944)hadacyclethreeweekslong,beingreceptiveonlyinthethirdweek.MostcubsareborninMay,whichmeansthatactualmatingbehaviorusuallytakesplacetwomonthspreviously,inFebruaryorMarch.
Thepatternsofsexualbehaviorassociatedwithcopulationarerelativelysimple,beginningwithmutualinvestigationofthegenitalandanalregions.Thefemalesoonstandsstill,holdinghertailtooneside,andhervaginamaymoveslightlywhentouched.The
66BEHAVIORPATTERNS
malemountsthefemalefromtherearandattemptstoinserthispeniswhileclaspingthefemalewithhisforepaws.Rapidpelvicthrustsfollowinsertion,andstimulationofthebaseofthepeniscausesrapidenlargementofthisregion(thebulbusglandis)throughengorgementwithblood,sothatthetwoanimalsbecomelockedtogether.Themalethenturnsaroundsothatthetwomaystandtailtotailforsomeminuteswhileejaculationgoeson.Allthisbehaviorisessentiallythesameasinthedog.
Beforethefemalebecomesreceptivetheremaybeconsiderablecourtshipbehavior.Atypicalpatterninvolvesextendingthefore-pawsonthegroundwhilekeepingtherearlegssemi-erectandthrowingtheheadtoonesidewiththetongueout.Bothanimalsmayexhibitthispatternofbehavior,thenonedartstooneside,andtheotherfollows.Anassociatedpatternconsistsofthrowingtheforelegsaroundeachother'snecksinasortofplayfulwrestling.AccordingtoCrisler(1958),thesepatternsofbehaviorareverysimilarinwolvesanddogs,exceptthatthewolvesappearmoreseriousanddignified.
Thesexualbehaviorpatternsofwolvesanddogsarerelativelysimple,andtheyarenotlinkedinsequencesbyanystrongdegreeofgeneticorganization.Courtshipbehaviorisnotnecessaryforcopulation,foramalemeetingareceptivefemalewilloftenmatewithverylittlepreliminarybehavior.Thiscontrastswiththebehaviorofsomespeciesofbirdsinwhichelaboratecourtshipisnecessaryinordertosynchronizethelaterparentalcarebythetwosexes.However,thephysiologicalchangeswhichproducesexualreceptivityinthefemalearesuchastoproduce,undernaturalconditions,alongcontinuedassociationbetweenapair.Theodoroussubstancewhichstimulatesthemaleis
associationbetweenapair.Theodoroussubstancewhichstimulatesthemaleisproducedlongbeforethefemaleisreceptive,sothatthemalestaysincloseattendance.Thegeneralcourseofmatingbeginswithaperiodinwhichthefemaleisattractivebutasyetrepulsesthemale.Sheisapparentlyalsoattractedtohiminthisstage,sinceshewillsometimesinitiatecourtshipbehavior,butsherejectsthemalewhenheattemptstomount.Shefinallybecomesreceptiveforaperiodofdaysorweeks,sothatsexualbehaviorcanberepeatedoverandoveragain.Thislonj^associationandconstantinteractionwouldbeexpectedtoproduceastrongattachmentbetweenthepair.
Whetherwildwolvesarcmonogamousisstillamatterofcon-jecture.Certainlydogsarcnot,underthehighlyartificialconditionsinwhichtheyliveandarcusuallybred.Atanyrate,thereisnothinglikethesituationinaflockofbighornsheeporherdofelk,inwhich
SOCIALBEHAVIOR67
femalescomeintoheatforonlyadayorsoandasinglemalenormallymateswithalargenumberoffemales.Inthewolfpack,allthefemalesarereceptiveforlongperiods.Thereisconsiderableevidencethateachmaleisquitepossessiveofonefemaleandmaymateonlywithher.Ginsburg(1963)findsthatalthoughwrolvesincaptivityarepolygamous,consortshipsmaybeformedbyeithermember'sabilitytokeepothersawayfromitsmate.
Wolfanddogpatternsofsexualbehaviorarethusquitesimilar.Theprincipalmodificationproducedbyselectionisintheseasonalnatureofthesexualcvcle.Innearlyalldogbreeds,thefemalescomeintoheatatapproximatelysix-monthperiodsduringanyseasonoftheyear.Furthermore,thefemalesusuallymatureinthelatterpartofthefirstyear,whereaswolvesdonotcomeintoestrusuntilthesecondoreventhethirdyear.Therehasobviouslybeenselectiontowardearlymaturityandincreasedfecundityindomesticdogs.Thistraitmayalsobeassociatedwithselectionforsmallersize,asrapidgrowthusuallyceaseswithsexualmaturity.
Onebreedofdog,theAfricanbasenji,stillshowsaseasonalcycleofsexualbehavior.IntheseanimalsthemajorityoffemalesrearedinthelatitudesofEnglandandtheUnitedStatescomeintoheatinSeptemberandproducepuppiesinDecember.TheAustraliandingo,whicliisusuallyassumedtobeadomesticdogthatwentwild,showssimilarseasonalbreedinginnorthernlatitudes,butinitsnativeSouthernHemisphereitbreedsinthecorrespondingautumnseason,which,ofcourse,isMarchinAustralia.Thebreedingperiodsofboththebasenji
which,ofcourse,isMarchinAustralia.Thebreedingperiodsofboththebasenjiandthedingoareobviouslycontrolledbychangesinseasonalconditions,andFuller(1956b)hasshownexperimentallythatartificiallyshorteningthelengthofdayinthespringwillproduceheatperiodsinthebasenjiasearlyasJuly.
Itispossiblethattheseanimalsaredescendedfromveryearlydogbreedswhichoriginatedbeforetheseasonalhabitwaslost,andthatthetimeofbreedingwasmodifiedbyselectiontocorrespondtotropicalconditions.Thebreedingcycleofbasenjisattheequatorisasyetunknown.Herethelengthofdayisconstant,butthereareseasonalrisesintemperatureattheequinoxes.
Theunderlyingphysiologicalbasisforthesexualcycleoffemaledomesticdogsconsistsofbalancedreactionsbetweenthehormonesofthepituitaryglandinthebrainandthehormonesoftheovary,orfemalesexgland.Hormonesofthepituitarystimulatetheovariestoproduceandexpeleggs.Atthescarleftbyeachegg,amassofcells(thecorpusluteum)continuestogrowandproducesprogesterone,ahormonewhicliactschiefivontheuterustomaintainpregnancy,
BEHAVIORPATTERNS
butalsosuppressesthehormonesofthepituitary.Thecorpusluteumcontinuestofunctionforaboutfourmonths,afterwhichitgraduallydisappears,permittingthepituitaryhormonestoactagaintostartanewcvcle.Inwolves,basenjis,anddingos,thepituitarymustbestimulatedbvchangesinthelightcyclebeforeitwillact,evenwhenprogesteroneisabsent.
Tosummarize,sexualbehaviorindogshasbeenchieflymodifiedawayfromseasonalbreedingandtowardearlysexualmaturity,bothchangesresultinginincreasedfecundity.Whiledomesticdogsrarelyhaveanopportunitytoexhibitallthepossiblepatternsofsexualbehaviorundertheusualconditionsinwhichtheyaremated,thebasicpatternsofbehaviorarethesame,withnoobviousdifferencebetweenvariousbreeds.
EHminativebehavior.—Asthevtravelovertheirhuntingrange,malewolvesregularlyvisitcertain"scentposts,"whichmaybesmallstonesorbushesaswellasactualpostsortrees.Heretheyliftthelegtourinateorsquattodefecate,andscratchthegroundthereafter.Similarbehaviorisfamiliartotheownerofanydomesticdog.However,weweresurprisedtofindthatdogskeptinourlargerunsandfieldswithboardfencesshowedeliminativebehaviorquiterarelycomparedtohousedogs,whichseemtospendmostoftheirtimegoingfrombushtobush.Inthemalethetvpicalpatternofmicturitionistoapproachascent
bushtobush.Inthemalethetvpicalpatternofmicturitionistoapproachascentpost,smellthiscarefully,thenliftonehindlegandspravasmallquantityofurineontheobject.Dogsconfinedinapenorfieldthatisnotenteredbyotheranimalsrarelydothis,andmalesraisedinsuchanenvironmentmaycontinuetoshowthepuppypatternofsquattingurinationwellintomaturity.Theprimarystimulusorreleaser'fortheleg-raisingpatternisapparentlytheodorofastrangedog'surineincombinationwithavisuallandmark.Dogsinastrangelocalitywhichotherdogshavenotpreviouslyvisited,willapproachandurinateonanyobjectswhichareslightlyelevated,suchasstones,bushes,andtreetrunks.Onceliehasurinatedonanobject,thedogisinhibitedbythesmellofhisownurinefromdoingsoagainuntilanotherdoghasusedthesite(vonUexkiillandSards,1931).
Thepatternofbehaviorassociatedwithdefecationisdifferentandmuchlessfrequent.Themalesquatstodefecatenearascentpostandmayfollowthisbyscratchingthegroundcloseby.Thisscratchingneverhasth<ofcoveringthefeces,asitdoesin
cats,andifithasanyfunction,itisprobablytoaddanothervisualmarktothesite.
Scentalsonportant.All*>thmaleandfemale,have
SOCIALBEHAVIOR69
apairofglandsjustinsidetheanus.Itispossiblethattheseimpartacharacteristicodortothefeces.ThisisinadditiontothescentglanddescribedbySeton(1925)onthedorsalsideofthebaseofthetail.Atanyrate,dogscharacteristicallysnifffreshfeces,andpartoftheinvestigatorybehaviorbetweendogsisamutualsniffingofthetailregion.
Theeliminativebehavioroffemalesisquitedifferentfromthatofmales.Inhousedogs,afemalewillvisitscentposts,butonlynearherownhome,andusuallyinonlyoneplace.Shecharacteristicallyurinatesinasquattingposture,butsomefemalesalsolifttheirlegs.Thefemaleusesmuchthesamedefecationpostureasthemale,butrarelyifeverscratchesafterward.
Intheperiodofsexualreceptivity,thebehaviorofthefemalechanges.Shenowwandersmorewidelythanusual,visitingseveralscentpostsandurinatingoneach.Whenmalessubsequentlyvisitthesepoststheybecomehighlyexcited,pursuethefemale,andremaininthevicinity.Thehouseholderwhoownsa
pursuethefemale,andremaininthevicinity.Thehouseholderwhoownsafemalemayexpecttofindhalfadozenmalesregularlycampedonhisdoorstepassoonasthefemalecomesintoheat.Apparentlyallthemaleswithinmilesbecomeawareofthefactwithinashorttime.
Wehadexpectedtohavetroubleofthissortwithourdogcolonyandweresurprisedtofindthateventhoughseveralfemalesmightbeinheatinsideourpens,weneverhadmorethancasualvisitsfrommalehousedogsintheneighborhood,andthattheymadenoattempttostaynearby.Thissuggeststhatthemaleshavetocomeintoclosecontactwiththeurineofafemaleinordertobesexuallystimulated,andthatthescentisnotcarriedontheairforanydistance.Onceinclosecontact,malescanreadilydistinguishonetypeofurinefromanother.BeachandGilmore(1949)placedtwosamplesoffemaleurineinanexperimentalroomandallowedonemaletoenteratatime.Everymalespentmoretimeexaminingthatofafemaleinestrusthantheurinefromanotherfemale.
Theprincipalsocialfunctionofeliminativebehaviorindogsisthereforetobringareceptivefemaletogetherwithamale.Ithasneverbeenexperimentallystudiedinwolves,buteliminationcertainlydoesnotfunctionasterritorialmarkinginanystrictsense,sincewolvesmakenoattempttodefendanythingbuttheareaclosetotheirdens.Nordoesitseemtohaveanyterritorialsignificanceindomesticdogs.Aslongastheresidentmaleisawayfromhome,strangemaleswillfreelyentertheyardandmarkit;themalereturningtothesceneshowsnosignsoflookingforanintruder.Asidefrombreeding,thebehaviorseemstofunctionsimplytokeep
animalsawarethatothersexistandindicatewheretheycanbefound.Forwolveslivinginpacksthereisordinarilynoreasonforonestrangewolftotrytofindanother,andthesescentpostsareprobablyusefulonlytoyounganimalsnotattachedtoapack.Suchsignswouldhelpthemeithertofindapackorformanewonewithsimilarisolatedindividuals.
Thisissomewhatconjectural,becausethebehaviorhasneverbeenfullyobservedinwildwolvesnorhastheirmatingbehaviorbeenadequatelystudied.Whathappens,forinstance,whenafemaleinapackcontainingseveralmalescomesintoheat?Observersoftenassertthatafemalemateswithonlyonemale,butouronlydirectevidencecomesfromobservationsoncaptiveanimals.Inanycase,undertheconditionsofawildpackwewouldexpectthatthefemalewoulddepositherurineonlycloseenoughtoattractthemalesinherowngroup.
Anotherpeculiarityofeliminativebehaviorindogsandwolvesisthattheyneversoiltheirsleepingplaces.Thisis,ofcourse,highlyadaptiveforanimalswhichliveindens,andthedevelopmentofthistraitinyounganimalswillbediscussedinalaterchapter.
Thepatternsofeliminativebehaviorhavebeenevenlessmodifiedbyselectionthanthoseofsexualbehavior.Althoughsomeminorpeculiaritiesmayexist,therearenowidespreaddifferencesbetweenthebreeds.
Epimeleticbehavior.—Thisisthegivingofcareandattention.Indogssuchbehaviorisprincipallydirectedtowardyoungpuppies,withsomeself-care.Thereisalmostnoepimeleticbehaviorbetweenoneadultandanother.
Thetypicalbehaviorofafemaletowardheryoungpuppiesaftershehasbeenawayistowalktowardthem,nosethem,andliedownonhersidewithherfeettowardthem.Thenshebeginsnosingandlickingeachpuppy,whichstimulatesurinationanddefecation.Theresultsarecleanedupbythemother'stongue,thuskeepingthenestclean.Inthemeantime,arousedbythetactilestimulation,thepuppiesworktheirwaytowardthemotherandattempttonurse.Inthis,themotheriscompletelypassive,notattemptingtoplacethepupsinanyparticularposition.However,ifapuppygetsawayfromtheothersandbeginstowhineoryelp,themotherwillusuallygotoit,pickitupcarefullywithherjawsandcarryitbacktotherest.Thepuppyisalwayscarriedwithitswholebodyinhermouth,feetdanglingdown,ratherthanbytheskinascatscarrytheirvoung.
Thisbehaviorisstronglyinfluencedbythematernalhormone
prolactin,whichalsostimulatestheflowofmilk.Oneyoungbasenjimotherhadherfirstpuppiesanddroppedtheminvariousplacesalloverthenurseryroom.Shewashighlyexcitedbutpaidnofurtherattentiontothemevenwhenwebroughtthemalltogetherinthenestboxandtriedtogethertoliedownbesidethem.Finallywegaveheraninjectionofprolactin.Withinanhourshehadsettleddownwiththepuppies,andpeacereigned.
Asthepuppiesgrowolderthesepatternsofbehaviorbegintofadeandotherstaketheirplace.Whenthepuppiesareaboutthreeweeksofage,themotherbeginsvomitingfoodforthem.Manymotherswilleatthisthemselvesifthepuppiesdonotfinishitall.Themotherallowsthepuppiestonurselessoften,andtheysometimesdothiswhilesheisstanding.Themothersstillcleanthepuppiesiftheysoilthemselves,althoughbythistimethepuppiesurinateand
puppiesiftheysoilthemselves,althoughbythistimethepuppiesurinateanddefecatebythemselvesoutsidethenestbox.
Inthedomesticdog,malesrarelyshowanyinterestinpuppies,butinwolvesmalesaswellasfemalesvomitfoodforthecubs.LoisCrisler(1958),whoraisedandobservedtwosetsofcapturedwolfcubsinAlaska,reportedthatheryearlingmaleandfemalebothfedtheyoungercubs,eventhoughsexuallyimmaturethemselves.Wecanconcludethatthepatternsofcare-givingbehaviorexhibitedtowardolderpuppiesarecommontobothsexesandarenotproducedbyhormones.
Theprincipaldifferencesbetweendogsandwolvesinthesepatternsofbehaviorarethattheyarelesswelldevelopedindogs.Humanownershavelargelytakenoverthecareofolderpuppies,whichmeansthatthepatternofvomitingcanbeweakenedwithoutseriousconsequences.Itseemstohavebeenmuchreducedinmales,althoughthismaysimplybebecausemaledomesticdogsarerarelygiventheopportunitytodeveloprelationshipswithyoungpuppies.However,inourlimitedobservationsofpuppiesrearedinlargefieldsbybothparents,weneversawthemalecaringfortheyoung.
Anothersetofpatternsofepimeleticbehaviorisconcernedwithself-grooming.Dogswilllickthemselvesintheanalandgenitalregionsandwillalsolickwounds.Theyscratchareaswhichareirritatedorattempttobitethemwiththeirteeth.However,thereisnoelaboratecleaningandgroomingsuchasoneseesincatsandmice.Groominganotheradultanimalisveryrare,althoughonedogwilllickanopenwoundonanother'sbody.Thesepatternsofbehaviorareessentiallythesameindogsandwolves,withnoobviousspeciesorbreeddifferences.
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Et-epimeleticbehavior.—Theepimeleticbehaviorofthemothersisassociatedwiththeet-epimeleticbehaviorofpuppies—callingforcareandattention.Forthemostpart,thisconsistsofdistresscallsbyyoungpuppies,thatis,whinesandyelpsofdifferentdegreesofloudness.Similarnoisesaremadebyyoungwolfcubs,althoughpossiblynotsoreadily.
Asthepuppiesgrowolder,theywillruntothereturningmother,waggingtheirtailsrapidlyandleapinguptopawandlickherfaceandbreast.Themotherfrequentlyvomitsfoodforthemontheseoccasions,andthepatternofbehaviorofthepuppiesprobablyhasthefunctionoffoodbegging.Thisisthesamesort
ofthepuppiesprobablyhasthefunctionoffoodbegging.Thisisthesamesortofbehaviorwhichpuppiesexhibittowardtheirhumanmasters,andtheremaybesometendencytoprolongitintoadultlifeincertainbreedswhichareuncommonly"playful"asadults.This,however,isjustanimpressionandstilllacksanyobjectiveproof.
Ingesiivebehavior.—Thepatternsofbehaviorassociatedwithtakinginsolidfoodandliquidsarequitesimilarindogsandwolves.Liquidsareingestedbylapping.Thedogorwolfstandswithhistaildownandscoopsupwaterorliquidfoodwithhistongue,makingconsiderablenoiseintheprocess.Semi-solidfoodsaremanagedinasomewhatsimilarway,thedogseizingpartofthefoodinhisteeth,releasingitandloweringhisheadsuddenlytoshiftthefoodintothebackofhismouth,andgulpingitquickly.Hedealswithbonesortoughpiecesofmeatbylyingdown,holdingthefoodinhispaws,andeithertearingoffstripswithhisfrontteethorgnawingontheobjectwithhisheavybackteeth.
Anotherpatterniscarryingfoodinthejaws,theanimaltrottingalongwithheadheldhighandrollinghiseyesineitherdirection.Wolves,withtheirstrongerjawsandneckmuscles,areabletoaccomplishprodigiousfeatsinthisway.Awolfwillpickupapieceofboneandmeatweighingtwentypoundsormoreandcarryitwithlittleeffort.Anothercommonhabitofwolvesistoburyfoodaroundtheden.Inacoldclimate,thispreservesthemeatfrombirdsandothercarrioneaters,butinwarmweatherthefoodspoilsrapidly.Thistraitpersistsinmosthousedogs,whichburyfoodaroundtheyardsoftheirowners.Inourlaboratory,somedogspersistentlyusedtheirnosestoburytheirfooddisheswithshavingsfromthefloor.
Beingfairlysimple,thesebehaviorpatternscanbeusedwithmanydifferentkindsoffood,andmaybecombinedandmodifiedinvariousways.Physiologicallythedogisprimarilyadaptedforameatdietandahuntingexistence.AccordingtoMcCay(1946),dogsunderordinaryconditionscangoforatleastaweekwithoutfoodor
SOCIALBEHAVIOR73
waterandsuffernoseriousharm.Whenfoodisavailable,theyeatrapidly,makinglittleefforttochewtheirfood.Theyhavealargegulletwhichpermitsthemnotonlytoeatbigchunksbuttovomititbackeasilyforthebenefitofpuppies.Theingestivebehaviorofdogsandwolvesissoorganizedthattheanimaleatsagreatdealwhenfoodisavailable,butisabletogoforlongperiodswithoutit.Consequently,theideaofa"hungerdrive"measuredbytheamount
withoutit.Consequently,theideaofa"hungerdrive"measuredbytheamountofhourssinceeatingdoesnotapplytothedog.Thedogis,inasense,alwayshungry,butheisnotdriventoeat.Oneofourinvestigatorsgaveadoganelectricshockwhenitcamenearitsfooddishandthenwaitedtoseehowlongitwouldtakebeforethedogcamebacktoeat.Thedognevercameback.Afterwaitingseveraldaysforthedogtoeat,theexperimenterstoppedtheexperimentsforfearofharmingtheanimal.Thisagreeswithtrappers'reportsofwolfbehavior.Ifawolfgetsintoatrapandescapes,itishopelesstousethistypeoftrapagain,asthewolfalwaysavoidsit.
Wefoundthatoneofthebestwaystousefoodmotivationinanexperimentalsituationwastogiveapuppyatasteofsomespecialfoodeachday(weusedsardines).Bythethirdday,thepuppywashighlymotivated.ElliotandKing(1960)foundthat,whentheyfedpuppiesatregularmealtimes,theanimalsateeagerly,evenwhensogrosslyoverfedthattheycouldnothavebeenphysiologicallyhungry.The"habitofeating,"orfoodreinforcement,isthusaveryeffectivemotivatingforce,evenintheabsenceofphysiologicalhunger.Thiscontrastswiththesituationinotheranimalslikeratsorsheep,whichnormallyeatcontinuouslyforlongperiods.Inthesespecies,ahighstateofmotivationcanbeproducedsimplybykeepingthemfromfoodforafewhours.
Therearefewbreeddifferencesinthesebasicpatternsofbehavior,andmostofthemareconnectedwithfoodchoice.Beforescientificinformationconcerningnutritionwasavailable,dogownersfedtheirchargesalmostanything—porridge,crustsofbread,orperhapsnothingbutbones.Theremusthavebeenselectionforanimalswhichwerenotfussyaboutfood,andmanyoftoday'shuntingandworkingbreedswilleatandthriveonfoodwhichotherswillreject.Forexample,wefoundnodifficultyingettingyoungpuppiestostarteatingordinarydogfood,exceptbasenjis,althoughthebasenjisreadilyaterawmeat.
Shelter-seekingbehavior.—Thisisnothighlydevelopedinwolves.Wolfdensareusuallyformedbyenlargementofnaturalcavesorofholesstartedbyburrowinganimals.Thewolfdoesalittlediggingtomaketheareacomfortablebutmakesnoefforttobuildanest.In
coldweather,wolvessleepinacurledpositionwiththeirnosesburiedinthelonghairoftheirtails,andtheywillalsosleepneareachotherforwarmth.However,theirmechanismsformaintainingheataremuchbetterthanindogs,andwolveshavebeenseenasleeponthesnowwithlegsoutstretched(AllenandMech,1963;Gins-burg,1963).
InourlargeoutdoorrunsattheJacksonLaboratoryweconstructedartificialdens(seeFig.1.3).Littersraisedtogetherwouldsleeptogetherintheseenclosuresandstayinsidewhentheweatherwasbad.Awell-knownpatternofbehaviorconnectedwithsleepingisthetendencyofdogstoturnaroundseveraltimesbeforelyingdown.Thisprobablyhastheadaptivefunctionoffeelingwiththepawsforasmoothareaonwhichtorest.
Thesefundamentalpatternsofbehaviorarenotgreatlymodifiedinthedifferentdogbreeds.Perhapsthemostnoticeablevariationisinthemodificationofsleepingattitudesincertainbreeds.Manydogswillsimplylieontheirsideswithfeetoutstretched,butsomewilllieontheirbellieswithforeandhindfeetextended,orsometimesevenlieontheirbacks.Theseposturesprobablyrepresentadjustmentstoanatomicalpeculiaritiessuchaslegstructureordistributionofbodyhair.
Allelomimeticbehavior.—Thisbehaviorisdefinedasdoingwhattheotheranimalsinagroupdo,withsomedegreeofmutualstimulation.Puppiesfirstdothisataboutfiveweeksofage,whenthelitterbeginstoruninagroup.Thisforeshadowsrunninginapack,oneoftheoutstandingcharacteristicsofdogandwolfbehavior.Todoso,theanimalsmustmaintaincontactwitheachother,primarilythroughvision,butalsothroughhearingandtouch.
Aswellasrunning,dogsandwolvesarefoundlyingdowntogether,gettinguptogether,andevenbarkingandhowlinginunison.Allelomimeticbehaviorisalsoimportantinpredationwhenapackmakesacombinedattackonalargeanimal.
Wehadexpectedtofindmoreofthisbehaviorinbreedswhichhuntinpacks(as,forexample,beaglesandfoxhounds)thaninbreedswhichhuntinamoresolitaryfashion.However,itturnedoutthattheprincipalmodificationofbehaviorinhoundsisnotapositiveincreaseofallelomimeticbehaviorbutsimplyalesseningofagonisticbehavior,sothatstrangeanimalscanruntogetherinthesamepackwithoutfighting.
Allelomimeticbehavioristhusabasicpartofthesociallifeofdogsandwolves.Ifananimalkeepsinconstantcontactwithothersofitskind,behaviorofthissortwillinevitablyresult.Thetendencyto
staywithothersisespeciallystronginyounganimals.Adultwolvesanddogswilloccasionallygooffonsolitaryhuntingexpeditions,aswhenapackwillsplit
willoccasionallygooffonsolitaryhuntingexpeditions,aswhenapackwillsplituptofindgame.Eventhen,theyusuallymaintainvocalcontact,sothatifoneanimalissuccessful,theotherssoonfindit.Allelomimeticbehaviorisusefulinhunting,sinceagroupisabletoattacklargeanimalsmoresuccessfullythanisanindividual,butitsprimaryfunctionistoprovidesafety.Aslongasthemembersofagroupkeepinconstantcontact,theycanreacttogetherinemergencies.Whensomethingthreatenstheden,thewholepackdefendsit.
Agonisticbehavior.—Sincewolvesareprimarilycarnivorousanimals,alargepartoftheirbehaviorisconcernedwithpredation.Gettingfoodinvolvesthreesystemsofbehavior:investigatorybehaviorinfindinggame,agonisticbehaviorinattackingit,andin-gestivebehaviorineatingit.Undernaturalconditions,wolvesarethechiefpredatorsoflargehoofedanimals:deer,moose,mountainsheep,orcaribou.Thesefoodpreferencesareeasilytransferredtodomesticstock,andwolvescanbehighlydestructivetodomesticcattleandsheep.Murie(1944)hasdescribedhowwolveshuntmountainsheepinAlaska,andLoisCrisler(1956)theirhuntingofcaribou.Adultanimalsingoodconditioncaneasilyescapefromwolves,whicharerelativelyslowrunners.Thebestopportunityforthewolfistofindayoungorlameanimalawayfromtherest.Inattackingalargeanimal,awolfavoidstheheadandmakesquickdashesatthehindlegs,springingbackifunsuccessful.Ifananimaliscornered,severalwolvesmayjointogetherintheattack.Usuallythepreycannotsuccessfullyavoidallofthem.
Theexactmethodofhuntingdependsuponthepackanditsusualprey.AllenandMech(1963;Mech,1962and1963)watchedapackofwolvesforseveralyearsasithuntedmooseonIsleRoyaleinLakeSuperior.Thispackwasunusuallylarge,containing15or16members,andalwaysattackedinagroup.Inanattackthewolveswoulddartinandback,avoidingthehoovesofthemoose,thenswarminginforamassassaultiftheanimalattemptedtorun,clingingtoitsrumpandflanksandeventuallyitsnose.Onlyoneoutofeverythirteenmooseapproachedwaskilled,asthepacksoonleftanyanimalwhichfoughtbackvigorously.Outof68kills,20werecalves,andonlyoneoftheremainingadultswasundersixyearsofage.
Wolvessometimesappeartoherdtheirprey.Sincethewolvesoftenseparate,ahuntedanimalmayunwittinglycomeclosetoonewolfwhileavoidinganother.Thispatternofpursuingherdanimalsisusedinthedomesticherdingdogs,butthesheeporstockdogis
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notallowedtoactuallyattack.Theherddogmustbeaggressiveenoughtochasesheepbuttimidenoughtobeinhibitedfromattackingthembyadistantshoutorgesturefromtheherder.
Wolves,ofcourse,donotalwayshavelargegameavailableandeatavarietyofotherfoodsincludingberriesandcarrion.Theyoccasionallyshowaspecialpatternofbehaviorforhuntingmeadowmice,inwhichtheyleaponthemousewithallfourfeet,pinningittotheground.ThispatternisseeninmanywildCanidae,suchascoyotesandfoxes,butisrarelyseenindomesticdogs,whichusuallypouncewithoutleapingofftheground,asdowolvesonmostoccasions(Murie,1944).
Thepatternsofagonisticbehaviordirectedagainstotherwolvesaresomewhatdifferentfromthoseusedagainstprey,possiblybecauseofthedifferentsize,shape,andbehaviorofwolvesascomparedtothepreyanimals.Forexample,twofightingwolveswillshowmuchin-and-outfighting,slammingtheadversarywiththehips,andthendivingforhislegs(Ginsburg,1963);buttwodogsmaycometogetherheadtohead,eachattemptingtogetpastthesnappingjawsoftheotherandslashingatthenearestavailablepart,usuallytheneckorshoulder.Ifoneanimalgetsagoodholdontheother'sneck,hewillusuallyhangonastheotheranimalcannotbitehiminthisposition.Meanwhileeachtriestoforcetheothertotheground.Muchlearningandadaptationareinvolvedinfighting,butthebasicpatternsofbehaviorareessentiallythesameindogsandwolves.
Thereareseveralcommonsituationswhicharouseagonisticbehaviorinwolvesanddogs.Oneoftheseisthepossessionoffood.Ananimalfeedingonabonewillgrowlatanyotherwhichcomesnear,andwillsometimesmakeashortrushandsnap,whichtheintrudereasilyavoids.Wehaveseenthispatternbeginninginyoungpuppiesasearlvastwoorthreeweeksofage,whenaridiculouslysmallpuppywillgrowloverafreshbone.
Anothersetofbehaviorpatternsisassociatedwiththeintrusionofstrangersintotheterritorvneartheden.Thefirstreactionisbarking,whichseemstobeprimarilyawarningsignal.Thewholepackjoinsin,andthecontinuousnoisemayinitselfhaveanaversiveeffect.Iftheintruderkeepsadvancing,thedefendingwolfpackwillusuallyfirstinvestigatehimandthenattack.Theintruderruns,tailbetweenhislegs,andtheothersrushafter,bitingathisflanks.
IItwostrangeanimalsapproacheachotheronneutralterritory,
hwalksslowlyandstiff-leggedlytowardtheother,tailheld
straightupandwavingslightlyfromsidetoside.Theytouchnoses
andthenmaycautiouslynoseeachother'stailandgenitalregion.Suchbehaviormayleadtomutualacceptancebutmoreoftenresultsinanattackbyoneanimalortheother.
Withinanaturalsocialgroup,agonisticbehaviorisreducedtoarelationshipofdominanceandsubordination.Thismaytakeseveralforms,dependingonthedegreeofdominance.Somedogssimplygrowlateachotherandmoveapart.Moretypically,thedominantdogplaceshisfeetonthebackoftheother,growlingashedoesso,whilethesubordinateonekeepshisheadandtaillowered.Astillmoresubordinateanimalmayrolloveronhisbackwhilethedominantonestandsoverhim,headtohead;thesubordinateanimalrapidlysnapshisteethandyelps.Sometimesthedominantanimalmakesafewthreateningsnapsatthesubordinateone.WolvesintheBrookfieldZoo(Ginsburg,1963)showapatternofbehaviornotcommonlyseenindogs,wherethedominantanimalpinstheothertothegroundwithhisjawsaroundtheother'sthroat.
Anotherpatternisexhibitedbyastrangeanimalapproachinginasubordinateway.Thestrangerturnshisheadaway,hiseyesclosedandearsheldback,andattemptstomakeclosecontactwiththeotheranimalbyweavingaroundhimandleapingintheairwiththebackcurved.Thisbehaviorisoftendescribedas"courting"andindicatesafriendlyapproach.
Whiletheabovepatternsofbehaviorcanbeseeninalmostanybreedofdog,thefrequencyoftheirexpressionhasbeenhighlymodifiedbyselection.IntheoldEnglishsportofbullbaiting,dogswereurgedtoattackabull.Thebulldogbreedwasselectedforatendencytoattackthenoseofthebullandhangoninsteadofusingtheslashingattackfromtherearpreferredbywolvesandmostdogs.Again,inattackingsmallanimalstheusualbehavioristodashin,snap,andwithdraw,avoidinganyriskofinjury.Theterrierbreedshavebeenselectedfortheircourage,i.e.,thetendencytoattackpreyandkeeponattackingregardlessofanyinjurysuffered.Thisbehaviordependsinpartonthepossessionofunusuallytoughandinsensitiveskinontheneckandshoulders.Thesametendencyappearsintheirfightswithotherdogs,sothatfightsbetweenterriers
tendencyappearsintheirfightswithotherdogs,sothatfightsbetweenterriersoftengoontothedeath.
Otherbreedshavebeenselectedintheoppositedirection.Thescenthoundsareremarkablypeaceableanimals,rarelygettingintoseriousfightsevenamongstrangers.Thistraitisusefulinmanagingalargepackandenablesthemtobekeptingroupsinakennel.Thehoundsalsohavelong,bagginglipswhichcouldeasilybebittenbytheanimalhimselfinthecourseoffighting.Thesemaybearesult
ofselectionforgreaterpowersofscent,theanimaltastingaswellasscentingtheair,buttheyshouldalsotendtoinhibitfighting.
Thebird-dogbreedsarelikewiseunusuallypeaceableanimals,havingbeenselectedforpeacefulcoexistenceinkennellife.Inaddition,thesettersinmedievaltimeswereselectedforshowingthepatternofcrouchingbehaviorusefulinhuntingbirdswithanet,ratherthanthatofattack.Retrieversarestillselectedfora"softmouth,"aninhibitedbitesuchthatbirdswillnotbedamagedwhencarriedbacktothehunter.Inthemodernpointers,thehuntingdogisstillnotallowedtoattackthebirdsbutmuststandstillwhenhefindsthem.Inallbirdhuntingbreeds,thedoghastoberestrainedwhileatadistancefromitsmaster.Alltheseselectedtraitsresultinagreatreductionofagonisticbehavior.
Aspreviouslymentioned,theherdingdogshavealsobeenselectedfortheirabilitytobetrainedtorestraintheirattacks.Atthesametime,makingathreatenedattackisanessentialpartofgettingthesheeptomove.Inmanypartsoftheworld,herddogsalsoguardagainstlargepredators,includingwolves,sothattheolderherdingbreedswereoftenlargeandaggressiveanimals.Inthisrespecttheywerecloselyrelatedtotheguarddogsonceusedtoprotecthousesanddwellings.Shepherddogsstillservethisfunctiononmanyfarms.
Inancienttimes,guarddogsandwardogswereselectedfortheirferocityaswellassize.MastiffsandGreatDanesaremoderndescendantsofsuchbreeds.Theirancestorswereusedforattacksonthievesandmarauders,butinrecenttimesthesegiantbreedshavebeenselectedintheoppositedirection,andmostofthemareunusuallygentle.
Thepatternsofagonisticbehaviorhavethusbeensubjectedtogreatmodificationsinthedifferentdogbreeds.Comparedwithwolvestheyarehighlyspecializedintheirchoiceofpatternsofagonisticbehavior.Mostofthisspecialization,however,hasactedtointensifyordiminishthepatterns,rather
specialization,however,hasactedtointensifyordiminishthepatterns,ratherthantoalterthebasicorganizationofthebehavior.Theresultisthat,althoughalldogsshowsimilarpatternsoffightingwhensufficientlyaroused,itiseasytoincitesomebreedstofightandextremelydifficulttostimulateothers.
Investigatorybehavior.—Wolvesanddogsareprimarilyhuntinganimals.Theyfindtheirpreybysearchingforitratherthanbywaitingforittocometothem,andsincetheyfrequentlyspendmostoftheirdaysandnightsinhunting,theyshowthepatternsofinvestigatorybehaviormorefrequentlythanthoseofanyothersystem.
Wolvesarcunspecializedanimals.Theyhuntalargevarietyof
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gameandeatalmostanythingavailablewhenfoodisscarce.Inhuntingtheyusealltheirsenses;eyes,ears,andnose,whicheverisappropriate.Bycontrast,variousdogbreedshavebeenselectedfortheircapacitytolearnspecialkindsofhunting.Thescenthoundshavebeenselectedfortheirabilitytofollowatrail,althoughinactualfieldworkthehoundswillusetheirearsandeyesaswellanddoagreatdealofrandomexploration.Forexample,abeaglehuntingforaparticularobjectwillcircleoveragreatdealofgroundwithitsheadheldhighbeforeitfinallystrikesastrongairscent,thendropitsnosetothegroundandgooveritinchbyinchuntilitfindstheobjectwhichithassmelled.Suchdogsrarelyfollowascenttrailstepbystepbutrimrapidlyalongit,weavingbackandforthacrossthetrailwiththeheadheldmoderatelyhigh.Iftheylosethescent,theycircleuntiltheypickitupagain.
Attheoppositeextremearethesighthounds.Theselong-leggeddogswerefirstbredintheMiddleEast,wheretheArabsstillusesalukisforhuntinggazelles.Theyareprimarilyadaptedforrunningafterswiftpreyinopencountry,wherescentisoflittleimportance.AsimilarbreedistheRussianwolfhound,orborzoi,whichcanactuallyoutrunwolves,tiringthemuntiltheycanbecorneredandkilledbyahunter.
Thebirddogsusetheirsensesmuchmoreequally.Sincebirdsleavefewtracksontheground,thebirddogfindsitspreybyrapidquarteringoftheground,oftenunderdirection,andusuallylocatesitbyscentwhenafewpacesaway.Retrievershavetomarkthespotwherebirdsfall,andthisrequiresusingtheeyes.
Inadditiontohuntingandenvironmentalinvestigation,therearespecialpatternsofsocialinvestigationindogsandwolves.AsSchen-kel(1947)pointsout,therearetwoareasofparticularinterest,theheadandthetail,althoughsomeobserversreportthatwolvespaymoreattentiontotheheadthandodogs(Crisler,1958).Oneofthemostprominentpatternsisthemutualinvestigationoftheanalandgenitalregionswiththenose.Unlikethevariedinvestigatorybehaviorconnectedwithhunting,socialinvestigationisverysimilarinallbreeds.
Ingeneral,theinvestigatorybehaviorofthedogbreedsisnotstrikinglydifferentfromthatofwolves.Thechangeshavebeenchieflyproducedbyemphasizingordiminishingcertainpatternsandparticularlybystrengtheningorreducingtheeffectofcertainkindsofstimulation.Forexample,theshepherdbreedsseemtobehighlystimulatedbythesmellofsheeporevendeer,andtheyoccasionallybecomesheepkillersordeerhunters.Likewise,thebirddogsare
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highlystimulatedbybirdsandsometimesbecomechickenkillers.Bycontrast,manyterriershavelittleinterestinscent.Weputalivemouseinaone-acrefieldandthenletinagroupofbeagles.Theyfounditinlessthanaminute.Ittookagroupoffoxterriersaquarterofanhourtoaccomplishthesametask,andScottishterrierswereneversuccessfulatall.Atonepoint,oneofthemactuallysteppedonthemousewithoutnoticingit.Howthesedifferencesinbehaviorwerebroughtaboutisnotknownexactly.Fromtheiractions,foxterriersappeartobenotsomuchdeficientinthecapacityforscentassimplyuninterested.Theyare,however,highlystimulatedbysounds.
Conclusion.—Behavioralpatternsinthedogandwolfareessentiallythesame.Selectionhasparticularlymodifiedtheagonisticandinvestigatorysystemsofbehaviorandtosomeextentthesexualsystem.Thesemodificationsareusuallyquantitativeratherthanqualitative,andmostoftheminvolvethediminutionorexaggerationofanexistingpatternwithoutcreatinganythingessentiallynew.
Theninebehavioralsystemsofdogsandwolvesarerelatedtoeachotherincharacteristicways.Sexualandeliminativebehaviorareassociated,thelatterassistinginthelocationofmates.Likewise,inthesepredatoryanimals,investigative,agonistic,andingestivebehaviorarecloselyassociatedwitheachother.Thelastthreecanbeperformedinunisonaswellasindividually,sothatallelomimeticbehaviorisoftenalsoassociatedwiththem.Thuswehavea
allelomimeticbehaviorisoftenalsoassociatedwiththem.Thuswehaveapictureofthebasicbehavioralorganizationofdogandwolf.Essentially,thisisasystematicandobjectivewayofdescribingwhatiscommonlycalled"personality."
COMPARISONWITHHUMANBEINGS
Wecanusethemajorsystemsofsocialbehaviorasanoutlineforcomparinghumananddogbehaviorpatterns,foritisobviousthatallninebehavioralsystemsarealsowelldevelopedinhumanbeings.Whenwedothis,weimmediatelyfindthatthedetailedpatternsofbehaviorareverydifferent.Afterall,thedogisafour-footedanimalwithawell-developedtailandnohands.Particularbehaviorpatterns,therefore,areboundtobedifferent.Nohumanbeingcanwaghisnonexistenttail,andnodogcanpickupthingswithhispaws.Humanbeingsanddogsarcbasicallydifferentinanatomy,physiology,andbehavior.Atthesametime,socialbehaviorpatternsaresimilarenoughsothatmanyofthemaremutuallyrecognizableand
eachspeciescangiveappropriateresponsestotheother'sbehaviorinmanysituations.
Inattemptingtoascertainthepossiblebehaviorofprehistoricman,muchhasbeenmadeofthefactthatmanyprimitivehumansocietiesstillexistinginhistorictimesgettheirfoodbyasortofpackhunting(Etkin,1954).Thisisdifferentfromdogbehaviorinthatitisdoneentirelybymales,thefemalesandinfantsmakingtheircontributioneitherbyfoodgatheringorbyhelpingpreparemeatonceithasbeenobtained.Indogsandwolvesbothsexestakepart.Dogsreadilyjoininhumanpackhuntingwithoutanyparticulartraining,andevenpetdogswilljoininafightbetweentwochildren.Thislastisacasewherethedogrecognizesthehumanformofagonisticbehavior.Likewise,itiseasyforhumanstorecognizethefunctionofcaninegrowlsandbites.
Otherpatternsofbehaviorarenotsoeasytounderstand.Whenadogjumpsupwithextendedpawsandwaggingtail,mostadultsrecognizethisas"friendly"behavior,butasmallchildmaybefrightenedbyit.Evenanadultcanbemisled.Whenadogadvancesslowlywithtailheldstifflyerectandwaggingslowlyfromsidetoside,aninexperiencedpersonmayconcludethatthedogistryingtobefriendly.Onlycloseobservationofsuchbehaviorbetweendogsrevealsthatthislatterpatternusuallyprecedesafight.
Onegeneralcharacteristicofbehaviorwhichmakesdogshighlyadaptableas
Onegeneralcharacteristicofbehaviorwhichmakesdogshighlyadaptableasdomesticanimalsisthetendencytotreathumanbeingsasthoughtheywerefellowmembersofapack,evenifthe"pack"isreducedtooneothermember.Withthisgoesallelomimeticbehaviorandthetendencytojoiningroupattacks.Asecondisthedog'stendencytousethehumanhomeasadenanddefenditagainststrangers.Thelatterbehaviorisalmostuniversalinhumans,andmaygobacktoprimitivelifewhentheonlycommonlyavailableshelterswerecaves.
Wecanseethattherearecertainbasicsimilaritiesbetweendogandhumanbehaviorpatternsandsystems,andwemaynowconsidertheproblemofwhetherthereareresemblancesinthegeneticsystemswhichunderliethese.Inhumanprehistory,andindeedinmuchofhistoricaltime,themajorityofhumansocietiesweretribalvillages,eachconsistingofafewhundredindividuals,andeachvirtuallyisolatedfromothersbydistance,language,andsocialorganizationregulatingmarriage.Thiskindofpopulationisidealforgeneticchange,anditmayaccountfortherapidevolutionofthehumancapacityforlanguage.Thebeginningsofurbancivilization,
82BEHAVIORPATTERNS
some10,000yearsago,markedthebeginningoftheendofthesesmallisolatedgroups,andmodernhumanpopulationswiththeirenormousnumbers,greatmobility,andincreasingtendencytowardcrossbreeding,representasituationdesignedtoproducerelativegeneticstability.Dogsfirstbecamedomesticatedaboutthetimeurbancivilizationbegan,butforcenturiesafterwardeachtownandvillagehaditsowngroupofdogs,somewhatcutofffromothersbythesamesortofbehavioralmechanismsastheirhumanmasters,butwithpopulationsevensmallerandgenerationsturningovermuchmorerapidly.
Thiswasanidealsituationforgeneticchange,witheachvillagetendingtoproduceitsownvarietyofdog.Inadditiontothis,therewasthefactorofhumanselectionforwhatwereconsideredattractive,useful,orfashionabletraitsofappearanceandbehavior.Someofthethingswhichwereselectedwereobviouslynon-adaptivetoananimallivingundernaturalconditions,suchasbulldogheadsandshort,thinhair.Suchselectionmadegeneticchangemuchmorerapidindogsthaninhumanpopulations.Undermodernconditionswithscientificmethodsofselectionandartificialisolationofbreeds,suchchangescanproceedevenmorerapidly.
Aswehaveseenpreviously,thediversityofphysicalformproducedbythesemethodsisverygreat,muchgreaterthanthediversityinbehaviorpatterns.All
methodsisverygreat,muchgreaterthanthediversityinbehaviorpatterns.Alldogbreedsshowthesamefundamentalgeneralpatternsofbehavior.Thismeansthatbehavioralorganizationisrelativelyresistanttogeneticchange.
Thedogbreedshavesometimesbeencomparedtohumanraces.Theyare,however,basicallydifferentinthatthehumanraceshaveneverbeensubjectedtocontrolledsystematicselectioninfavorofparticularkindsofindividuals.Thereareafewphysicalcharacteristicswhichareadaptivetotheclimaticconditionsinwhichtheraceswereoriginallyfound.Forexample,apersonwithadarkskinandtightlycurledhaircancontrolhisbodytemperaturebetterunderhot,humidconditionsthancanapersonwithlightskinandstraighthair(Baker,1958),butmanyotherphysicaldifferencesseemtobeaccidental.BoththetallestandshortestofhumanbeingsarefoundinequatorialAfrica.
Onewouldexpectthatpopulationdifferencesinbehaviorpatternswouldbeevenlessmarked,andthisindeedseemstobethecase.Basichumanbehaviorpatternsaremutuallyrecognizablebetweenallhumanraces,eventhosewhicharemostdiversephysically.Inshort,wewouldexpectthatbehavioraldifferencesbetweenhumanraceswouldbemuchlessthanthosebetweendogbreeds.Inother
words,thisisnotausefultypeofcomparison.Thedogbreedsdonotcorrespondtohumanraces.
Ontheotherhand,inanyhumanpopulation,evenfromasupposedlypurerace,thereisanenormousamountofindividualvariability,bothinformandbehavior.Heretheconceptofpolymorphismisausefulone.Itwasoriginallyappliedtocasessuchascertainbutterfliesinwhichtwodifferentcolorvarietiesexistedinthesamespecies.Thehumanraceisobviouslypolymorphicwithregardtothetwosexes,andbetweenmatureandimmatureindividuals.Inaddition,thereareallsortsofdifferencesbetweenindividualsofthesamesexandage.Inahumansocialgroup,itisanobviousadvantagetohaveindividualsofdifferentabilitiesandskills.
Whenwelookatwolves,thewildancestorsofdogs,weseethattheyarealsopolymorphicinthattheyshowagreatdealofvariationinsizeandcolor(Jolicoeur,1959).Wecanalsoseethatitwouldbetheoreticallyadvantageousforawolfpacktobebehav-iorallypolymorphic:tohaveonememberwhichwouldbehighlytimidandreacttotheslightestsuspicionofdangerandthuskeepthepackonthealert,andanotherwhichmightbeboldenoughtogoinandobtainfoodwhendangerwasslightandtheneedforfoodgreat.
obtainfoodwhendangerwasslightandtheneedforfoodgreat.
Whatselectionhasdoneistotakethisindividualvariabilityofwolvesandaccentuateitinthedogbreeds.Wecanthinkofeachbreedasrepresentingoneofmanypossibleindividualbehavioralvariations.
Thisisthemostusefulcomparisonwecanmake.Adogbreedrepresentsalargegroupofgeneticallysimilarbutnotreplicatedindividuals.Humanfamiliesarealsogroupsofgeneticallysimilarindividualsbutareunlikedogbreedsbothintheirsmallsizeandinthefactthatoutbreedingisenforcedratherthanprevented.Inshort,wecanlearnrelativelylittleaboutthedifferencesbetweenhumanpopulationsthroughastudyofthedogbreeds,butagreatdealaboutthepossibilitiesofindividualvariationofhumanbehavior.
CHAPTER4
THEDEVELOPMENTOFBEHAVIOR
Sincethebasicbehaviorpatternsofdogsaresosimilartothoseofwolves,wewonderedhowsoonthedifferenceswouldappear.Wouldyoungpuppiesbelikelittlewolves,orwouldtheyshowdoglikecharacteristicsfromtheveryfirst?Again,howsoonwouldbreedcharacteristicsappear?Wouldallyoungpuppiesbeessentiallyalike,orwouldtheybegindevelopinginadifferentfashionfrombirth?Thesequestionsarerelatedtotheimportantpracticalproblemofthepredictionoflaterperformancefromearlybehavior.Weexpectedthatbywatchinganimalsastheygrew,wewouldseetheinteractionofhereditaryandenvironmentalfactorsastheymoldedbehavior,withtheprocessoflearningproducingamoreandmoreimportanteffectonbehaviorastheanimalgrewolder.Werealizedmanyoftheseexpectationsfromourobservations,buttheresultsalsoturnedupsomefascinatingfactswhichwehadnotforeseen.
Inordertogetourinformationondevelopment,webegansystematicdailyobservationsofeachlitter,asdescribedinChapter1.Theresultwassomeninety-sixpagesofnotesoneverylitterraised,andweanalyzedtheseaccordingtotheageofthepuppies.Aswewatchedtheanimalsfromdaytoday,theyhardlyseemedtochange.Butwhenwebegantoassembleournotesandobservations,wesawthattherewerecertaintimeswhenthebehaviorofapuppywouldchangeovernightandthatdevelopmentfellintodistinctnaturalperiods,eacliwithitsowncharacteristicbehavior.
THENEONATALPERIOD
THENEONATALPERIOD
Socialbehavior.—Whenwetakeapuppytwoorthreedaysoldawayfromitsmotherandplaceitonthefloorashortdistanceaway,
DEVELOPMENTOFBEHAVIOR85
itbeginstocrawlslowly,throwingitsheadfromsidetosideandwhiningoryelpingasitgoes.Thisvocalizationis,ofcourse,caresolicitingoret-epimeleticbehavior,andusuallyattractstheattentionofthemother.Ifshedoesnotrespond,thepuppykeepsoncrawling.Itdoesnotorientitselftowardthemotherandmaygoinacircleaftermovingafewinches.However,ifitsswingingheadtouchesthemotheroroneoftheotherpups,itstopsandcrawlstowardthem.
Wehavehereaninfantilepatternofinvestigativebehaviorwhichseemstobebasedentirelyonthesenseoftouch.Comparingthiswithadultbehavior,wenoticetwothings:eachmovementisextremelyslow,andthebehavioritselfisquiteinefficient,dependingchieflyonaprocessoftrialanderror.Itworkswellenoughifthepuppiesareconfinedtoanestboxorsomeden-likeenclosure,butiftheyarekeptinalargeroom,apuppyseparatedfromtherestislikelytomoveinanydirectionandendupfarawayfromthemother.Ofcourse,maternalbehaviorwillordinarilytakecareofthesituation,asmostmotherswillpickupyoungpuppiesandreturnthemtothenest.
Asecondsortofsituationoccurswhenthemotherhasleftthepuppiesforatime.Thepuppiesareheapedtogetherinaballinthecenterofthenest,restingquietly.Themothercomestowardthem,liesdownbesidethem,andstartspokingthemwithhernose,turningthemoverandlickingtheunderpartsoftheirbodies.Thisstimulatesthepuppiestourinateanddefecate,andthemotherkeepsonlickingthemuntiltheyarecompletelyclean.Fortheseyounganimals,eliminativebehaviorisareflexstimulatedbyanythingsimilartothemother'stongue.Puppiesraisedawayfromtheirmothersgetintoserioustroubleunlesstheyareproperlystimulatedwithawarmwettowel.Thenetresultofthesepatternsofbehaviorbymotherandoffspringisthatthenestareaisalwaysentirelyclean,showingnotraceofurineorfeces.
Meanwhile,thepuppieshavebeguntocrawl;andastheydoso,theycomeintocontactwiththemother'sbreastandbeginsuckingmovements.Inthemostcompleteformofthispatternofbehavior,thepuppypushesonthemother'sbreastwithalternateforepawsandoccasionallypullsbackwithitshead,bracingwithitsforefeetandpushingwithitshindfeet.Thisactivityprobablystimulates
withitsforefeetandpushingwithitshindfeet.Thisactivityprobablystimulateslactation,anditalsodisturbsanypuppieswhichhavenotbeenawakened,sothattheyalsopushforwardtoeat.Thisistheinfantileformofingestivebehavior.
Newbornpuppiesactuallyshowverylittleactivityotherthan
86BEHAVIORPATTERNS
thesesimplepatternsofet-epimeletic,investigatory,eliminative,andingestivebehavior.Theyreacttopain,cold,orhungerwiththesamelimitedrepertory,yelpingandmovingatrandom.Weseethatallbehavioratthisageisadaptedtoinfantilelifeandthatthecharacteristicpatternsofadultbehaviorarecompletelymissing.Infact,ifonehadonlybehaviortogoby,onemightassumethattheneonatalpuppybelongedtoanentirelydifferentspeciesfromadultdogs.
Sensorycapacities.—Theseobservationsstimulatedustostudythebasiccapacitiesunderlyingthedevelopmentofbehavior.Thefirstofthesewasobviouslythesenseorgans.Mostpeopleknowthatpuppiesarebornwiththeeyesclosed,whichmeansthattheycannotseeanything,intheusualsenseoftheword.Somepuppiesreacttoaverystronglight,particularlythosewithlightskinpigmentandwhoseeyelidsarethereforemoretransparent.
Whenweexamineanewbornpuppyclosely,wefindthatitsearsarealsotightlyshut,sothatthereisnoexternalopeningthroughwhichsoundcanenter.Whenwetestitwithsuddenloudnoises,thereisnoreactiontoeitherhighorlowtones.Thenewbornpuppyappearstobecompletelydeaf,inspiteofthefactthatitmakesconsiderablenoiseitself.Itprobablydoesnotevenhearitsownyelps.Inkeepingwiththis,wehaveneverobservedmotherscallingorvocalizingtotheiryoungpuppies.
Sinceadultdogsmakesomuchuseoftheirnoses,wemightexpectthatthesenseofsmellwoulddevelopearly.However,puppiescannotlocatetheirownmothersbyodorfromanydistance(James,1952),althoughTroshikhin(1955)gotresponsestoodoroussubstancesfromafewcentimeters.TheneurologistP.J.Harmanexaminedthebrainsofsomeofournewbornpuppiesformvelinationandconcludedthattheolfactorynervesandregionofthebrainconnectedtothemweresoundevelopedastomakeitunlikelythatthetruesenseofsmellhadanyimportantfunction.Wetestedthiswithacommercialcompounddevelopedtorepeldogsfromfurnitureandbushes.Theactiveingredientisrelatedtooilofcitronellaandisalmostodorlesstomosthumanbeingsalthoughthereisaslightlynauseatingaftertasteinthethroat.Itispossiblethereforethatthis
slightlynauseatingaftertasteinthethroat.Itispossiblethereforethatthissubstanceprimarilyaffectsthetastebudsratherthanthenose.Newbornpuppiesreacttoitbyacharacteristicwithdrawalreflex,drawingbacktheheadasfaraspossible.
Thesenseoftasteisobviouslypresent.Newbornpuppieswilllickaglassrodsmearedwithfishormeatjuiceormilkbutrejectabittersubstancesuchasquinine.Theywillsuckonanysmoothwarmob-
jectsuchasthehumanfingerbutkeepthisuponlyifmilkisforth-
ung.
Astotheothersensorycapacities,thepuppiesreactstronglytocold(^VYelker,1959)andpain.Givenachoicebetweenawarmheatingpadandacoldonenexttoit,theycometorestonthewannerone.Theyalsoreactnegativelytoextremeheatbuthavepoortemperaturecontrol,sothatonemusttakecare,inkeepingyoungpuppieswarmbyartificialmeans,nottoraisetheirbodytemperaturetoohighandkillthem.Anotherwell-developedsenseisthatofbalance,orresponsetogravitv.Turnedonitsback,thepuppyimmediatelystrugglestoturnover,andifitcrawlstotheedgeofatablesothatpartofitsbodyisunsupported,ityelpsindistress.Asshownbyresponsestothemother,reactionstotoucharewelldeveloped.
Comparedwithanadult,theneonatalpuppyisgreatlydeficientinsensorycapacities,beinginfactmostdeficientinthosesenseswhicharemostimportanttoanadultdog,i.e.,hearing,sight,andsmell.Fromasensorvviewpoint,theyoungpuppyisprimarilyatactileanimal,respondingtotouch,pain,andcold.Eveninhischemicalsenses,heislargelylimitedtotaste,whichiseffectiveonlyondirectcontact.Thepuppyisintouchwithonlythatpartofhisenvironmentwhichactuallytoucheshim.
Motorcapacities.—Themotorcapacitiesofthenewbornpuparelikewiselimited.Itsonlymethodoflocomotionisaslowcrawl,theactionofthefrontlegsbeingbetterdevelopedthanthatofthehindones.Thereisnotailwagging,andsuckingandlickingaretheonlyoralactivitiesotherthanvocalization.Thelatterconsistschieflyofdistressvocalization,aseriesofrapidwhinesoryelps.Neonatalpuppiesfrequentlymakethesenoisesataratefasterthanonepersecondwhilebeingweighed(Fig.4.1).Thepuppyisthusquitehelplessatbirth,althoughmoreadvancedthannewbornhumanbabiesinthatitisatleastabletocrawl.
crawl.
Capacitiesfororganizationofbehavior.—Earlyinourobservationsofnewbornpuppies,wenoticedthattheydidnotseemtolearnbyexperience.Apuppvwouldcrawltotheedgeofthescaleplatform,falloff,andbegintoyelpindistress.Whenplacedinthemiddleoftheplatform,itwoulddothesamethingoveragain.Likewise,theonlychangewesawinsuckingbehaviorwasthatthepuppiesbegantonursemorestronglyandefficientlyafteraweekorso,whichcouldhavebeencausedsimplybydevelopmentofthemuscularsystem.Somerecentexperiments(Stanleyetah,1963)indicatethatthepuppyiscapableofsomedegreeofslowlearningwithregardtosucking.Apuppywhichisgivenmilkaftersucking
88BEHAVIORPATTERNS
arubbernipplewilleventuallybegintosuckmoreoftenthanapuppywhichisnotsorewarded,andonewhichisgivenquinineinsteadofmilkwilleventuallyrefusetosuckthenippleatall.
Observingbehaviorisnottheonlvwayofinferringthefunctionofthecentralnervoussystem.Anothermethodistomakeamicroscopicexaminationofbraintissue.Nervefibersofyounganimalsfrequentlylackthemyelinsheathcharacteristicofadulttissue.Thissheathisanouterlayeroffatlikematerialassociatedwithspeedytransmissionofstimuli.Thefactthatanervefiberisunmyelinateddoesnotmeanthatitcannotfunctionbutonlythatitfunctionsmoreslowly.Myelinatedfibersinadultstransmitstimuli50to100timesfasterthantheunmyelinatedfibersofthesympatheticnerves.
Harman's(1958)investigationofthebrainofnewbornpuppiesshowsthattheonlvareaswhicharewellmyelinatedarethoseconnectedwiththetrigeminalnerve—whichgoestothemouthandincludesthesensorynervesoftasteaswellasthemotorfiberstothejawmuscles—andthenon-acousticportionoftheauditorynerve,whichisthepartconnectedwiththeorgansofbalance.Inthecerebralcortex,theconvolutionsaresimpleandtheunderlyingfibersalmosttotallvunmyelinated.Thedevelopmentofmyelinationthereforeseemstobecorrelatedwiththedevelopmentoffunction.Wewouldexpectthatstimulipassingthroughtheunmyelinatednervesofpuppieswouldmoveslowly,andcanconcludethattheslowactionsanddelayedresponsetimesofnewbornpuppiesresultfromthis.
Theundevelopednatureofthebrain,senseorgans,andmotororgansallresultinagreatlyreducedcapacityforlearningcomparedwiththatofolderpuppies.Theonlysenseorgansthroughwhichstimulicouldbeassociatedarethoseoftouchandtaste.Thesearelikewisetheonlyoneswhichcouldbeusedformakingdiscriminations.Thenumberofresponsesissolimitedthatthereareonlyafewactivitieswhichcouldpossiblybeaffectedbylearning:sucking,crawling,yelping,andelimination.Theresponsetimeisoftensoslow,occurringsecondsafterstimulation,thatapuppymighthaveconsiderabledifficultvinassociatingaresponsewithagivenstimulus.Wemustconcludethatthecapacityforlearninginthesenewbornanimals,ifitexistsatall,isquitelimitedandpossiblyofadifferentnaturefromthatintheadult.
Summary.—Thesocialbehaviorpatternsofthenewbornpuparelimitedtothoseconnectedwithneonatalexistenceandarequitedifferentfromthosefoundinadultanimals.Theentireneonatalperiodisprimarilydevotedtoonefunction,thatofobtainingnutrition
DEVELOPMENTOFBEHAVIOR
bynursing.Supplementingthebehaviorofthepuppiesisthatofthemothers,whorarelyleavethemevenforafewminutesduringthistime.Theneonatalpuppyisnotaself-sufficientorganism.Itstemperaturefluctuateswiththeenvironment,anditneedsthewarmthoftheotherpupsandthemother'sbody.Itevenneedsstimulationinordertofeedproperly,asnewbornpupswhicharekeptwarmwillliequietlyforhours,onlyattemptingtonursewhenstimulatedbythemother.
Anobserverofneonatalexistenceisstronglyimpressedbytheeffectivewayinwhichtheyoungpuppyisnormallyshieldedfromtheeffectsoftheexternalenvironment,bothbymaternalcareanditsownlimitedsensory,motor,andintellectualcapacities.Thepuppvcanbegreatlvdisturbedphysiologicallybyadverseconditions,buttherearefewwaysinwhichitcanbeaffectedpsychologically.
THETRANSITIONPERIOD
Duringtheentireneonatalperiodthepuppygrowsinsizeandstrengthbutstillretainsthesamepatternsofbehaviorasatbirth.Thefirstchangeinbehavioroccursaftertheeyesopen,whenthepuppyforthefirsttimecrawlsbackwardaswellasforward.Otherchangesfollowinrapidsuccession,sothatthepuppy
wellasforward.Otherchangesfollowinrapidsuccession,sothatthepuppyundergoesabehavioralmetamorphosiswhichisalmostasspectacularasthemetamorphosisofformfromatadpoletoafrog.Behavioralpatternsadaptedforneonatallifearedecreasedorabandoned,andthecharacteristicpatternsofadultbehaviorbegintoappear.Theperiodisoneoftransitionfromneonataltoamoreadultformofexistence.Thisprocessbeginswiththecompleteopeningoftheeyes,occurringontheaverageat13daysofage,withmuchbreedandindividualvariation(Table4.1).
Changesinsocialbehaviorpatterns.—Theneonatalpuppyischaracteristicallydifficulttofeedbyhand.Itsucksonlyhalfheartedlyonababy'snursingbottle,apparentlybecauseitisdifficulttoduplicatetheexactprimarystimuliorreleaserswhichtriggerthenursingpattern.Itcanbefedafewdropsatatimewithaneyedropper,thepuppymakingfutilesuckingmovements.Itdoesnotlapmilk,andtheeasiestwaytofeedaneonatalpuppyistoinsertasmallstomachtubeandinjectmilkdirectlyintothestomach.
Bycontrast,thepuppyat2weeksofageishighlyadaptable.Itwillreadilynursefromabottleandcanevenlapupmilkorsoftfoodfromadish,albeitinaclumsyfashion,usuallyplasteringitself
90BEHAVIORPATTERNS
TABLE4.1TimeofCompleteOpeningoftheEye
*Allbreeds(orhybrids)weightedequaDy.
tIncludesoneretardedlitter.
Openingoftheeyeoccursearlyinbeaglesandcockerspaniels,moreslowlyinbasenjis,andstillmoreslowlyinsheltiesandfoxterriers.Inthehybrids,BCSFi'sandFVsarerelativelyslow.Whenallhybridsaretakentogether,theaverageisintermediatebetweenthetwoparentbreeds.
withfoodandoccasionallychoking.By3weeksofagethepuppyisabletostandanddrinkmilkoreatinafairlyefficientfashion.However,itsfirstteethhaveonlyjustbeguntocomethrough,anditisstillincapableofdoinganyeffectivechewing.Whenherpuppiesareabout3weeksofage,themotherbeginstovomitwarm,semiliquidfoodfromherstomach,thisbeingthenaturalsupplementalfoodatthisage.
Wehaveextensiveevidence,obtainedbysuddenweaningatdifferentages
Wehaveextensiveevidence,obtainedbysuddenweaningatdifferentages(Scott,Ross,etal.y1959),ontheabilityofyoungpuppiesinthetransitionperiodtoeatinwaysotherthannursing.Artificialbitches'milkandpowdereddrydogfoodwasavailableatalltimestothepuppies,andwehelpedthemtofindthedishwhentheyweretooyoungtolocateitbythemselves.Beforeandafterweaning,wetestedthemtwiceadaybystickingafingerintotheirmouthsandrecordingtheamountandforceofsucking.Until19or20daysofage,thepuppieswouldsuckfingersreadilv,particularlywhenhungry.Afterthisage,therewasnodifferencebetweenexperimen-talsandcontrolsleftwiththemother,andby4weeksofageallthepuppieshadquitfinger-suckingentirely.Theymightgentlychew,butthebehaviorofsuckingonobjectswhichdidnotproducemilkhaddisappeared.Allofthisevidencemeansthattheonlypattern
ofingestivebehavioravailabletothenewbornpuppyissucking.Alternatepatternsoflappingandchewingbegintoappearinthetransitionperiod,andthepuppyiscapableofabandoningsuckingatanytimethereafter,providingthepropersortoffoodisavailable.
Aspartofthesameexperiment,partofalitterwastemporarilyremovedfromthemotherandplacedintheotherhalfofthesameroom,separatedbyawirebarrierthroughwhichdieanimalscouldseebutnottouchtheothers.Weleftthemforseveralhours,andthencamebacktoobserve.Duringthefirstweekoflife,theymightbefoundanywhereintheirhalfoftheroomandoftenseparatedfromeachother.Duringthesecondweek,weusuallyfoundthemtogetherinthesamespotwherewehadleftthem.Inthethirdweek,aftertheireyeswereopen,wealwaysfoundpuppiesclosetothefence,indicatingthattheywerenowabletoorientthemselvesintheroom.Thedevelopmentoftheeyesisthusaccompaniedbyachangeinthepatternofinvestigativebehavioratthestartofthetransitionperiod.However,themoststrikingchangeininvestigativebehavioroccurslater,atabout3weeksofage,whenthepuppiesbegintorespondtopeopleorotheranimalsatadistance.Allthisevidenceindicatesthattheearlypatternofinvestigativebehaviorbasedontouchisgivingwaytoadultpatternsofbehavioremployingothersenseorgans.
Et-epimeleticbehaviordoesnotdisappear,butsomeofthesituationswhichonceevokeditarenolongereffective.Forexample,theamountofvocalizationwhilethepuppiesarebeingweigheddropstoalowlevelby2weeksofage,andalmostdisappearsafter3weeks(Fig.4.1).Atthesametime,theybegintowanderaroundandyelpwhenmovedtoastrangeplace,eventhoughwarmandcomfortable.Untilthisage,theywouldbequietanywhereaslongastheywere
comfortable.Untilthisage,theywouldbequietanywhereaslongastheywerenotcoldorhungry.
Eliminativebehavioralsobeginstochangetowardtheadultpattern(Ross,1950).By3weeksthepuppiesarebeginningtowalkoutsidethenesttourinateanddefecate.Theynolongerrequirestimulationbythemother,althoughtheystillhavenotbeguntousespecificspots.Mostmotherscontinuetolickandcleantheirpuppies,buteliminationisnolongerdependentonthisstimulation.
Agonisticbehavioralsobeginstoappear.Somepuppieswillgrowlasearlyas2weeksofageifgivenabone;andafter3weeks,playfulfightingwithotherpuppiesbecomesincreasinglycommon.Thepuppiespawandmoutheachotherclumsily,apatternwhichwilleventuallybecomemoreandmorelikethefightingofadults.Before2weeksthereisverylittleindicationofescapebehavior.Thefirst
BEHAVIORPATTERNS
indicationisbackwardmovementinreactiontovisualstimulation,whichwecanthinkofasavisualstartlereaction.Later,at18to20daysontheaverage,thepuppiesfirstbegintoshowastartleresponsetosound.
Oneoftheneonatalpatterns,shelter-seeking,changesrelativelylittleexceptthatthepuppiesaremorelikelytobefoundseparated
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AGEINWEEKS
Fig.4.1.—Declineoftherateofdistressvocalizationduringthefirst4weeksoflife.Notebreeddifferences.Thesereactionswereobtainedwhilethepupswereweighedandprobablymeasurediscomfortresultingfromcontactwiththecoldmetalscaleplatform.
fromeachotherwhentheroomiswarm.Thisprobablyreflectsanincreasingabilitytomaintaintheirownbodytemperatures.
At3weeksofagetherearestillthreeimportanttvpesofadultbehaviorwhicharecompletelymissing:sexual,allelomimetic,andepimeletic.Thefirsttwowillappearinthenextfewweeks,butthethirdwillbeconfinedtoself-groominguntiltheanimalsbecomeadults.
Thisisthegeneralpictureofchangeinsocialbehaviorpatterns.Thepuppyat3weeksisafardifferentanimalfromaweekearlier.
DEVELOPMENTOFBEHAVIOR93
Sincesuchimportantchangesoccur,theirtimingbecomesquiteanimportantmatterforunderstandingbehavioraldevelopment,andoneofthebestwaystoapproachthisproblemistoexaminechangesintheunderlyingbasiccapacitiesoftheanimal.
Senseorgans.—Assoonastheevesopenwecandemonstratethattheyare
Senseorgans.—Assoonastheevesopenwecandemonstratethattheyarefunctionalbyshiningabrightlightintothemandobservingthecontractionofthepupils.However,insomepuppiesthisisslow,andthepupilkeepsfluctuating,indicatingthatthemechanismisnotcompletelydeveloped.Thepuppieswillshownystagmus,whichmeansthatifweholdapuppy'sheadandbodyfirmlyandswingthewholeanimalinahorizontalarc,hiseyeswillflickbackandforthasifhewerefixinghiseyesonanobjectandfollowingitasitmovespast.However,thismavmeanonlythatareflexinvolvingthesemicircularcanalsoftheearisfunctioningandnotthatthepuppyisrespondingtosight.Ahistologicalexaminationoftheeyesshowsthattheretinaattwoweeksofageisquiteundevelopedand,infact,isnotcompletelyformeduntilapproximately4weeksofage,indicatingthatcompletevisualfunctionhasnotyetbeenachievedduringthetransitionperiod(Blume,1956;Parry,1953).
Anotherindirectlineofevidenceisprovidedbythealpharhythmofthebrainwaves.Thiselectricalactivityofthebrainisassociatedwiththedevelopmentofvisualfunctionandindicatesactivityinthatpartofthecerebralcortexassociatedwithvision.CharlesandFuller(1956)measuredtheelectricaloutputofthebrainindevelopingpuppies,usingsurfaceelectrodes.Thenewbornshowalmostnobrainwavesandnodifferencebetweenthesleepingandwakingstates.Thenatapproximately3weeksofage,theelectroencephalo-graphicpicturechangesradically.Thebrainwavesincreaseinamplitude,andanEEGtakeninsleepbecomesdifferentfromthatrecordedduringthewakingstate.However,theEEGdoesnotshowitsadultformuntil7or8weeksofage,whenthenervoussystemisprobablylikethatofanadultasfarasvisionisconcerned.
Stillanotherwayofmeasuringthedevelopmentofperceptionisthe"visualcliff"testofWalkandGibson(1961).Theapparatusconsistsofa6-inchwideboardlaidacrossapieceofplateglass.Ononesideoftheboardtheglassislaiddirectlyoverasheetofcheckeredcloth;ontheothersidetheclothfallsaway,producingtheillusionofadrop-offfromtheboardtothefloorbelow.Disregardingtheglass,onesideappearsdeepandtheothershallow.Mr.FrankClarktestedpuppiesonthisapparatusfromthetimeofeyeopeninguntiltheyshowedanaversiontothe"deep"side.Untiltheywere
BEHAVIORPATTERNS
about30daysold,puppiessteppedfromtheboardindiscriminatelyontoeitherside.Afterthisage,mostpuppiesuniformlywenttotheshallowsideinspiteofprevioussafelandingsonthedeepone.
Summarizingthisevidence,wecanconcludethatwhilethepuppyrespondstolightassoonastheeyesopenandsometimesbefore,itisprobablynotfullycapableofobservingformuntilabout4weeksofage,andthatcompletevisualcapacityisnotpresentuntilabout8weeks.
Thestartleresponsetosound,whichisthefirstindicationthatthesenseofhearinghasbeendeveloped,appearsat19.5daysontheaverage(Table4.2).Whetherthesenseofhearingiscompletelydevelopedatthispointwedonotknow,butthepuppiesseemtorespondtoanyloudnoise,whetheritisarelativelyhigh-pitchedsoundoftheGaltonwhistleoralow-pitchednoisefromanyothersource.Thestartlereactiontosoundisadefiniteandeasilyrecognizedreaction,andsinceitiscloselyassociatedwithanumberofotherchanges,itcanbetakenasthebestmeasureoftheendofthetransitionperiod.
Changesinmotorcapacities.—Duringthetransitionperiod,the
TABLE4.2TimeofFirstFunctionoftheEar:AnimalsGivingaStartleResponsetoSound
*Allbreeds(orhybrids)weightedequally.
tIncludesoneretardedlitter.
Thedevelopmentofthiscapacityshowsmuchlessvariabilitybetweenbreedsthantheopeningoftheeyeor
eruptionoftheteeth.Thusthestartleresponsecanbetakenasanexcellentdevelopmentalmarker,closelyasso-iiatedwiththebeginningoftheperiodoisocialization.Contrarytootherindicators,foxterriersaremoreadvancedinthisrespeitthanotherbreeds.Thehybridsdevelopfasterthaneitherparentstrain,butthereisstillatendencyfortheBCSgroupofhybridstofallbehind,asinothermeasures.Thisdifferencebetweentheresultsofthereciprocalcrossesmightbeattributedtoeitheramaternaleffectoraccidentalselectionofslowandrapidlydevelopingparents.
DEVELOPMENTOFBEHAVIOR
95
puppybeginstogetuponhisfeetandwalkinsteadofcrawl(Fig.4.2).Themostaccurateobjectiveevidencewhichwehaveontheonsetofthisabilityisthe
accurateobjectiveevidencewhichwehaveontheonsetofthisabilityistherecordofthepostureofpuppieswhenweighedeachweek(Fig.4.3).Atbirthandforthenexttwoweeklyweighings,almost100percentofthepuppieslieflatwhenplacedonthescales.At3weeks,50percentofthemadoptsomeotherposture;andby4weeks,veryfewofthepuppiesstilllieflat.Thisdoesnotmean,ofcourse,thattheycannotstand,asobservationshowsthatallthepuppiescanwalkby3weeksofage,butonlythat
100
75
ui
o
tr50
25
10
15AGEINDAYS
20
25
30
Fig.4.2.—Developmentofwalkingandplayfulfightinginrelationtotheopeningoftheeyes,startleresponsetosound,anderuptionoffirstteeth.Thegraphsrepresentcumulativefiguresoffirstoccurrencesinanimalsobservedin10-minutedailyperiods.Thezeropointisthedaybeforethefirstanimalwasobservedwalkingorshowingplayfulfighting.
someofthemstillreactbylyingdownwhenplacedinastrangesituation.
Anotherimportantchangeinmotorcapacitiesarriveswiththeeruptionofthefirstteeth(Table4.3).Inpuppiesthesearetheuppercanines,whichcanfirstbefeltthroughthegumsatapproximately20daysofageontheaverage.Alongwiththisthepuppiesbegintobiteandchewaswellassuck.Allmovementsare
withthisthepuppiesbegintobiteandchewaswellassuck.Allmovementsarestillslowandclumsycomparedwiththoseofadults,butthepuppiescanatleastchewandmoveintheadultfashion.Anothermotorcapacitywhichappearsasoneofthenewpatternsofsocialbehaviorinthisperiodistailwagging.
BEHAVIORPATTERNS
100
80
bJId
u.
z60o
j-zu
o40tr
UQ-
20-
AGEINWEEKS
Fig.4.3.—Developmentofmotorabilityduringthetransitionperiod,asshownbythepercentageofanimalswhichstayedontheirfeetinsomeposture(standing,crouching,orsitting)whenfirstplacedonthescaletobeweighed.Notethathybridsdevelopedmoreslowlythanpurebreeds,possiblybecauselargerandheavier.
TABLE4.3
TimeofEruptionofUpperCanineTeeth
•Allbreeds(oihybrids)weightedequally.
tIncludesoneretardedlitter.
Thepun-breedsvarywidelyinthischaracteristic,basenjisandbeaglesbeing
Thepun-breedsvarywidelyinthischaracteristic,basenjisandbeaglesbeingfast,andtherestslow,particularly
folterriersInthehybridsthereisatendencyfurallpopulationsintheBCScross(startedfromcockermothers)todevelopmoreslowlyIftheretardedlitterisomittedfromtheCSBFi,thepercentageatiweeksis74,almostexactlythesameasthatinthebackcross,suggestingthatmaternalenvironment(perhapsprenatal)hasaneffectontheeruptionofteeth.
DEVELOPMENTOFBEHAVIOR97
Learningcapacities.—Oneofthebestwaystostudylearningobjectivelyisbythemethodofconditioning,originallydevelopedonthesalivaryreflexofthedogbyPavlov.Inthistypeofexperimentthedogisstimulatedinsomeway,usuallybyasoundorlight,andpresentedimmediatelyafterwardwithapieceofmeat.Beforelongthedog'smouthbeginstowaterassoonasthestimulusappears,andbeforehehasachancetoseethemeat.Thisprocessofforminganassociationbetweenaneutralorinitiallymeaninglessstimulusandaresponse,iscalledconditioning.Inordertodoiteffectivelytheremustbeaprimarystimulus,whichproducesaresponsewithoutpreviousexperience,andanothersecondaryorneutralstimulus,whichhasnosucheffect.Thelatterisdifficulttofindforayoungpuppy,sincetherearesofewstimulitowhichitcanrespond,andmanyoftheseproduceprimaryresponsesthemselves.
Changesintheabilitytobeconditionedcanbemeasuredinthefollowingways.Oneistotakethenumberoftimesthattheneutralandprimarystimulihavetobepresentedtogetherbeforearesponseisobtainedtothesecondarystimulusalone.Adultdogswillfrequentlymakesuchanassociationwithoneexperience.Asecondwaytomeasurethiscapacityistomeasurethenumberofpairingsnecessarybeforetheassociationwiththeneutralstimulusbecomesstable.Instableconditioningtheanimalrespondstotheneutralstimulusinverynearly100percentofthetrials.Stillathirdmethodistosetsomearbitrarystandardofaccomplishmentandseehowlongittakestheanimaltomeetthecriterion.
Inourownexperimentswefirstsetthearbitrarystandardofobtainingastableresponseaftertentrials(Fuller,Easier,andBanks,1950).Insteadofusingthesalivaryreflex,whichwouldbedifficulttomeasureinyoungpuppies,weemployedtheleg-withdrawalreactiontoamildelectricshockandappliedthistechniquetotwenty-fivepuppies,includingcockerspaniels,shelties,wire-hairedfoxterriers,springerspaniels,andabeagleXKerryblueterrierhybrid.Avarietyofneutralstimuliweretested,includingthesoundofabuzzer,light,touch,the
ofneutralstimuliweretested,includingthesoundofabuzzer,light,touch,thetasteofKarosyrup,andtheodorofadogrepellant.Noneofthepuppiesdevelopedstableconditionedreflexesaftertentrialsuntiltheywerebetween18and21daysold,althoughthereweresignsofunstableresponsesasearlyas14days.Ineachcasetheonsetofstableconditioningwasquitesudden.Onedaythepuppymightgiveoccasionalresponsesandonthenextitwouldgiveastablereactionaftertentrials.
Thetypeofreactionwhichthepuppiesgaveafter18daysistypicalofolderpupsandadults,andwecanconcludethatthere
isanimportantchangeinthecapacityforconditioningatthisage.Inalaterexperiment,weworkedwithalessextremecriterionforconditioning,withtheideaofobtainingabettermeasureoftheearlydevelopmentofthelearningcapacity(CornwellandFuller,1960).Inthiscasethepuppymetthestandardwhenitbegantorespondtotheneutralstimulusin50percentofthetrials.Wealsousedapuffofairastheneutralstimulus,thisbeingsomethingtowhichthepuppiescouldreactveryearlyindevelopment.Asampleoffivefoxterrierpuppiesmetthe50percentrequirementatanywherefrom10to19daysofage,withanaverageofabout15days(Fig.4.4).Thiskindofcriterionapparentlygivesamuchmore
Fig.4.4.—Developmentoflearningcapacitiesduringtheneonatalandtransitionperiods.Eachcurverepresentstheaveragescoreoffivefoxterrierpuppiesgiven10trialsperday.Notethatthereisnoevidenceofimprovementuntilatleast10daysofage(after50previoustrainingtrials)andthattheexperimentalanimalswerestillnotmakingperfectscoresat17days.Therewasconsiderableindividualvariation,andnumbersaretoosmalltogiveaclear-cutdevelopmentalpicture.
variableresultthanthemorerigorousone,butitneverthelessdemonstratesthatconditioningofanunstablesortdoesappearatsometimeinthetransitionperiod.
TheseresultsesentiallyagreewithworkbyRussianexperimenters(Klyavina,etah,1958).Workingwithauditorystimulationat15daysofage(atwhichtimeourresultsindicatethatonlyafew
DEVELOPMENTOFBEHAVIOR99
puppieswouldrespondtosound),theyfoundthattheleg-withdrawalresponse
puppieswouldrespondtosound),theyfoundthattheleg-withdrawalresponseappearedataboutthesixteenthpairingandbecamestablebytheeightieth.Thisisconsistentwithourresultsasthesepuppieswouldnothavepassedatentrialcriterion.Atonemonth,learningwasasrapidasthatobservedbyusbeyondtheageof3weeks.
80-SHOCK,STABLE
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TransitionPeriod
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FORMATION'^.^v
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NATION**««■*■».»««,..ZZZZZZ
FORMATION
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AGEINDAYS
AGEINDAYS
Fig.4.5.—Changeinresponsetoconditioningbetweenthetransitionandsocializationperiods.Thecapacityforformingaconditionedresponsetofooddevelopsbeforethatforelectricshock.(DatafromKlyavinaetal.,1958.)
TheRussiansalsofoundthatamotorresponsetofoodcouldbeconditionedmorerapidlythanthewithdrawaltoshock.At15daysthisresponseappearedontheaverageaftertheninthpairingandbecamestablebythethirty-seventh.Thesepuppiesstillwouldnothavemetaten-trialcriterionforastableresponse,buttheexperimentindicatesthattheabilityforconditioningingestivebehaviorappearssoonerthanthataffectingagonisticbehavior.Whilethesefindingsarenotasclear-cutaswemightdesire,allresultsindicatethatthepuppydevelopstheabilitytoquicklymakeanassociationconcerningapainfulexperienceneartheendofthetransitionperiod.
Thisraisesthequestionofwhetheranemotionalresponsetopainmightbelearnedearlierindevelopment.However,whenwetriedtoconditiontheincreaseinheartrateinresponsetopain,wefoundthatthisabilityactuallyappearedlaterindevelopment(FullerandChristake,1959).Ifthisistrue,itsuggeststhatthepuppyinearlydevelopmentishighlyprotectedfromthepsychologicalafter-effectsofunpleasantexperiences.
Stanley(1963)hasdevelopedanewmethodofstudyingchangesincapacitiesforconditioning,basedonoperantconditioning.Intheoperanttechnique,firstusedbySkinneronadultanimals,thepuppymustassociatewhathedoeswiththeresultingchangeinstimulation.Thisavoidstheproblemoffindingneutralstimuliandiscloselyrelatedtothenormalprocessofnursing.Thepuppyfirstsucksand,asaresult,isstimulatedbymilk.Thereisatheoreticaldifficultyarisingfromthepossibilitythatmilkitselfmaybeaprimarystimulusforsucking.Ifso,thenursingprocesscanbeexplainedasacircularreflex:suckingisstimulatedbycontactwithasoft,warmsurface;suckingproducesmilk;andmilkstimulatessucking.
Stanleyhasthereforedevisedanelectronicmother,orratheranelectronicbreast,whichcanbesettoreleasemilkafteranygivennumberofsucks.Thepuppiesrespondasiftheywerelearningthatthemachinegivesmilk,butwehaveasyetnoinformationonhowsoonthisabilitytolearndevelopsorhowitchangeswithage.
Summary.—Allourevidenceshowsthatthetransitionperiodisoneofprofound
Summary.—Allourevidenceshowsthatthetransitionperiodisoneofprofoundreorganizationofbehavior.Byselectingtheopeningoftheeyesasthebeginningofthetransitionperiodandtheappearanceofthestartlereactiontosoundastheend,wefindthatthewholeprocesstakeslessthanaweek,theeyesopeningcompletelyat13daysandthestartlereactionappearingat19.5days.Thesefiguresaretheaverageofthefivebreedsstudied.Amongthem,theprocessmaybefasterinsomebreedsthaninothers.Furthermore,agreatmanyofthesechangesseemtobeconcentrated—againontheaverage—around18to19daysofage,particularlythoseinvolvingachangeinbehavior.Thepuppythusbecomesaverydifferentorganismwithinthespaceofafewdays.
Themostessentialchangeinfunctionisfromtheneonataltotheadultformofnutrition.Thechangeisnotabsolute,asthepuppiesstillcontinuetonurse;buttheynowbegintoeatlikeadultanimalsaswell.Anotherfundamentalchangeisfromtheneonataltotheadultformoflocomotion.Thepuppiescannowwalkandarecapableofleavingthenestarea.Anotherimportantchangetakesplaceintherelationshipwiththemother.Previously,therelationshipwas
quitesimpleandinvolvedingestivebehavioralmostentirely.Nowitbecomesmorecomplexasotherbehaviorpatternsappear.Inaddition,thepuppychangesfromananimalwhichishighlyprotectedfromitsenvironmenttoonewhichisextremelysensitive.Asweshallsee,thischangeisassociatedwith,andperhapsnecessaryto,theformationofprimarysocialrelationships.Italsomeansthatanyonesortofenvironmentalstimulationhasaverydifferenteffectonthebehaviorofthepuppyatdifferentages.
PERIODOFSOCIALIZATION
Thisisaperiodofrapiddevelopmentofsocialbehaviorpatterns,incontrasttothetransitionperiod,whichischieflyoneofchangesinbasicsensoryandmotorcapacities.Mostofthenewpatternsofbehavioraredirectlyconnectedwiththemotherandlittermatesandformapartoftheanimal'srapidlydevelopingsocialrelationships.
Ingestivebehavior.—Intheneonatalperiod,themotherconstantlyattendedthepuppies.Nowshebeginstoleavethemforlongperiods,andwhenshereturns,shemayvomitfoodforthepuppiesaswellasallowingthemtonurse.Thisbehaviortypicallybeginsbetween3and4weeksafterthebirthofthepups.Frequentlyshewillnotliedownwiththem,andtheyhavetorunafterherandnurseasshestandserect.Thepuppiesreadilyeatthevomitedfoodandwillalso
nurseasshestandserect.Thepuppiesreadilyeatthevomitedfoodandwillalsolapupwaterormilkwhenavailable.
Weaningisagradualprocess,startingwithvomitingbythemotherandthetakingofsolidorsemisolidfoodbythepups.Whentheyareabout5weeksold,themothermaybegintogrowlatherpuppieswhentheytrytonurse.Thepuppieswalkuptoher,starttonurse,andthemotherquicklyturns,growls,andsnapsintheirfaceswithoutactuallytouchingthem.Thesurprisedpuppiesoftenrolloverontheirbacks,yelping,andsoonlearntostayaway.Somemothersstopproducingmilkasearlyas7weeksafterthepuppiesareborn,butafewstillproduceitat10weeks,sothatfinalweaningtosolidfoodnormallytakesplacesometimewithinthisperiod.
Thepuppyisstillnotcapableofeatinglikeanadult.Itssmallbabyteetharesharp,butincapableofproducinganyeffectonsolidbones.Likewise,thepuppyisstillincapableofdoingitsownhunting.
Eliminativebehavior.—Earlyinthesocializationperiod,thepuppybeginstoleavethenesttourinateanddefecate.Atfirstthisisdoneinanyspotcloseby,butby8.5weeks,thepuppyisbe-
ginningtousedefinitespotsfordefecation(Ross,1950).Itwillwanderaroundthepenwithitsnosetotheground,apparentlyfollowingatrail,butmoreprobablysmellingtracesofurineorfecessothataneliminativereflexissetoff.Thepuppyatthisagewillgoformanyhourswithoutsoilingitssleepingplacebutwillurinateanddefecatefrequentlywhileawakeandactive.Inmostcasesthechosenspotisasfaraspossiblefromthefoodareainthepen.Themalepuppystilldoesnotshowtheleg-liftingreaction.
Thesebasicpatternsofdevelopingeliminativebehaviorhaveconsiderablepracticalimportancetothedogownerwhoisattemptingtohousebreakapuppy.Theimportantfactsare:first,thatapuppywillnotsoilitsownsleepingplaceandwillnoturinateordefecateifshutupinitovernight.Thisprobablyhappensbecausepartofthenormalpatternofeliminationisthepreliminarymovingaroundwhichisnotpossibleinarestrictedarea.Thesecondfactistheresponseofthepuppytoodorsofpreviouseliminationinparticularspots.Thislatterbehavioristhepreliminarytothe"scentpost"behaviorofadultanimals.Oncethesespotsareestablishedandnotcompletelydeodorized,urinationanddefecationcanbereadilycontrolled.Thewisedogownerhelpsthepuppyestablishthesespots,eitheroutdoorsorindoorsonpapers,andleadsthepuppytothematfrequentintervals.Untilitis12weeksold,apuppyislikelytourinate
tothematfrequentintervals.Untilitis12weeksold,apuppyislikelytourinateordefecateeveryhourortwo,aslongasitisawake.
Et-epimeleticbehavior.—Thedistressvocalizationofpuppiesnowbecomesmoredifferentiated,thepuppiesmakingagreatervarietyofsounds.Theystillyelpwhenhungryorhurtbutarenotsolikelytobecomecoldandvocalizeforthisreason.Inaddition,certainnewreactionsappear.Oneisyelpinginreactiontorestraint.Wefirstnoticedthisinpuppieswhichaccidentallygotcaughtbehindanestboxandsoonfoundthatsimplyconfiningapuppyinasmallboxwouldproducethesamereaction.Removalofthemotherandlittermateswouldalsocausethepuppiestoyelp,butoneofthemosteffectivesituationswasastrangeplaceawayfromthehomepen.Puppiesplacedinacageinthehalloutsidetheirhomepenmadeanear-splittingracket.
Usingthisinformation,we(ElliotandScott,1961)madeadevelopmentalstudywhoseresultsareshowninFigure4.6.Puppiesleftaloneintheirhomepensdoonlyamoderateamountofyelpingat3weeksofage,andthistendstodecreaseastheygrowolder.However,apuppyleftaloneinastrangeplaceyelpsloudlyandcontinuously,producingthemaximumnumberofvocalizationswhen
DEVELOPMENTOFBEHAVIOR
103
1400
1200
1000
<n
800
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400
200
T-
10
II
12
WEEKSOFAGE
Fig.4.6.—Developmentofdistressvocalizationofbeaglepuppiesundertwoconditionsofisolation.Notethatthepeakofvocalizationinastrangepencomesat6-7weeksofage,whichotherevidenceshowstobethepeakofdevelopmentofthecapacityforrapidsocialization.
itis6to7weeksoldandgraduallydecreasingthemthereafter.By12weeks,itmakesverylittlenoiseinastrangeplace.Thistrendreflectsaprocessofmaturationalchangeratherthanbecominghabituatedtothesituation,becauseapuppygiventheexperience
forthefirsttimeatthelateragesshowsmuchthesameyelpingrateasthosewhichhavebeenisolatedbefore.
Wecaninterpretthisbehaviorasadevelopingemotionalreaction.Forahighlydependentandhelplessanimallikeayoungpuppy,themostdangerouspossiblesituationisoneinwhichitiscompletelyaloneinastrangeplace.Undernaturalconditionsalostwolfpuppywouldbevulnerabletoanypredatoraswellasindangerofeventuallystarvingtodeath.
Thisreactionalsoindicatesanotherfunctionoftheperiodofsocialization—thatofbecomingattachedtoaparticularlocality.Thepuppyisatfirstlittledisturbedbyachangeinlocality,becomesgreatlydisturbedaround6or7weeksofage,andstilllater,atatimewhenpuppiesnormallybegintoexploretheirenvironmentatadistancefromtheirsleepingplaces,becomeslessdisturbedbyit.
Investigatorybehavior.—Oneoftheoutstandingchangesinbehavioratthebeginningoftheperiodofsocializationisthetendencyofpuppiestorespondtothesightorsoundofpersonsorotheranimalsatadistance.The3-week-oldpuppyapproachesslowlyandcautiouslytowardahumanobserverseatedquietlyinitspen.Itfinallycomescloseandstartsnosinghisshoesandclothes.Afterthis,itmaystarttowagitstailrapidlybackandforth.Thetailwaggingitselfappearstohavenodirectlyadaptivefunction,butissimplyanexpressionofpleasurableemotiontowardasocialobject.Whateffectithasonotherdogsisdifficulttotell,butitseemstohavethesameeffectonhumanobserversasthesmileofachild;i.e.,itisarewardforthepersonwhohasinitiatedasocialcontact.Forthepuppy,thiswholepatternofbehavioristhetypicalmethodofinitiatingasocialrelationship,anditmaydevelopfurtherintotheplayfulbehaviordescribedbelow.
Thepuppywillinvestigateanynewinanimateobjectinitspeninmuchthesameway,exceptthatnotailwaggingisinvolved.However,thepuppyisinnosenseahuntinganimalatthisage.Evenwhenraisedinourlargeone-acrefields,puppiesstayedwithin10to20feetoftheirnestboxuntilapproximately12weeksold,whentheybegantospreadoutandinvestigatetherestofthefield.
Agonisticbehavior.—Thefirstevidencesofagonisticbehaviorarethestartlereactionstosoundandsuddenmovement.Frombeingananimalwhichdoesnotrespondtothesestimuliatall,thepuppynowrespondstoallloudsoundsandsuddenmovementsindiscriminately.Itsnewcapacitiesforlearningsoonenable
suddenmovementsindiscriminately.Itsnewcapacitiesforlearningsoonenableittodiscriminatebetweenthosesituationswhichareactuallydangerousandthosewhichhavenosignificance;andasthepuppygrowsolder,itno
longerrespondstoirrelevantsoundsandmovements.Themotherstimulatesfearresponsesinweaningherpups,andtheycanoftenbeelicitedbyahumanhandlerwalkingrapidlytowardthepuppy,eventhoughithasneverbeensteppedupon.
Thedevelopmentofthesefearresponsesdependsagooddealupontheenvironmentofthepuppy.Underournormalmethodsofrearing,manypuppiesbecomequitefearfulofhumanhandlersat5weeksofage.Thisfearalmostcompletelydisappearedinreactiontodailyhandlingthroughoutthenexttwoweeks.However,whenpuppieswereraisedinlargefieldswithfewhumancontacts,thefearresponsesbecameprogressivelymoreextreme.InoneexperimentFreedman,King,andElliot(1961)broughtpuppiesinfromsuchafieldatdifferentagesandplacedtheminaroomwithapassiveobserverfor10minuteseachday.At3weeksofage,thepuppiescametotheobserveralmostatonce;butby7weeks,ittooktwodaysontheaveragebeforethepuppieswouldmakeapositivesocialapproach.The14-week-oldpuppiesweresofearfulthattheynevercamecloseevenafteraweek.Theselastpuppieswerelikelittlewildanimalsandcouldbetamedonlyinthewayinwhichwildanimalsareusuallytamed,bykeepingthemconfinedsothattheycouldnotrunawayandfeedingthemonlybyhand,sothattheywerecontinuallyforcedintoclosehumancontact.
Instillanothersituation(Fisher,1955;Fuller,Clark,andWaller,1960),inwhichpuppieswerekeptisolatedinindividualpens2feetsquare,activeescaperesponsesneverdeveloped.Whenbroughtfromhispenforthefirsttimeat16weeksofage,thepuppymightcrouchinacorneroradoptbizarrepostures,orevenshow"fearbiting,"buthedidnotrunaway.
Playfulfightingappearsearlyinthisperiod(seeFig.4.2).Atfirsttheyoungpuppiesseemtobeactinginslowmotion,clumsilypawingandmouthingtheirlittermateswithoutproducinganyrealdamage.Astheygrowoldertheirteethbecomelonger,andapuppywhichgetsholdofasensitivespot,suchastheear,maybeansweredbyayelpofpain.Oneindicationthatfightingisnotseriousatthisearlyagecomesfromthedominancetests.At5weeks,lessthanone-fourthofthepairsofpuppiesshowedcompletedominance.
However,atabout7weeksofage(thetimewhenfinalweaningfromthebreast
However,atabout7weeksofage(thetimewhenfinalweaningfromthebreastbeginsandmothersbegintothreatentheiroffspring),puppiesleftwiththeirmothersbegintoattackeachotheringroups.Theanimalagainstwhomtheattackisdirectedissometimesasmallandweakindividual,butitalsomaybealargeandaggressiveone.Inmostbreedsthis"gangingup"istemporaryandplayful.Inthe
BEHAVIORPATTERNS
foxterrierbreed,however,suchgroupattacksarepersistentandbecomesoseriousthatthevictimhastoberemovedinordertopreventseriousinjury(Fuller,1953).Inonelitterofsixanimalstherewerethreemalesandthreefemales.Thegroupbegan"gangingup"onthesmallestfemale.Whenshewasremovedtheybegantoattackanotherfemale,andwhenshewastakenouttheyattackedthethird.Thefinalresultwastwoseparategroupsofthree,sinceonefoxterriercanapparentlystandofftwobutnotthreeotheranimals.Inlargergroups,onepuppywouldgetholdoftheearsandanotherthetail,stretchingtheirvictimbetweenthem,whilethethirdanimalattackedinthemiddle.Notevenafoxterriercantakemuchofthis.
Inotherbreedsthegroupattackswereneverserious,andindividualfightsusuallyresultedintheformationofsomesortofdominancerelationshipwithouteitherindividualbeingseriouslyhurt.However,suchrelationshipsarenotoftencompletelyformeduntilthenextperiodofdevelopment.
Allelomimeticbehavior.—Atfirstthemembersofalitterarequiteindependentintheiractivities,wanderingoverthepenindifferentdirections.Between3and4weeksofagetheybegintofolloweachotheraround,andby5weeksweoftenseethepuppiesrushingtowardthegateoftheirpenasagroup(Table4.4).Thisisthefirstappearanceofthepackbehaviorofadults.By7weeksthepuppieshavebegunthegroupattacksdescribedabove,whichareacombinationofallelomimeticandagonisticbehavior.
TABLE4.4
TimeofDevelopmentofAllelomimeticBehaviorasIndicatedbyCo-ordinatedMovement
Total
160
160
50
Sexualbehavior.—Mountingandclaspingmayappearsometimesasearlyas3or4weeksofage.SupportingapuppybyahandthrustbetweentheForelegsandunderthebellywillsometimesstimulatethrustingmovements.However,thesexorgansthemselvesarestillundeveloped,andsuchbehaviorisnevercomplete.Asourpuppies
DEVELOPMENTOFBEHAVIOR
107
grewolderwesometimesobservedtheplayfulattitudewhichisthecharacteristicpartoftheadultcourtshippattern.
TABLE4.5
OccurrenceofSexualBehaviorin160PurebredPuppies(0-16WeeksofAge)duringDailyObservationPeriods
Notethatsexualbehaviorisseenslightlymoreofteninmalesthaninfemales,hencesomewhatearlier.Resultsintheindividualpurebreedswerehighlyvariable.
Otherpatternsofsocialbehavior.—Epimeleticbehaviorisneverseenexceptwhenthepuppiesscratchorlickthemselves.Unlikeprimates,dogsshowverylitttletendencytowardmutualgrooming,andtheonlysituationwhichstimulatesitisanopenwound.Thecapacityforsomeofthepatternsofmaternalcaremayexistinolderpuppies,butundernormalconditionsthenewbornpuppieswhichmightstimulatethesepatternsareneveravailable.Shelter-seekingbehaviorcontinuesbutislikelytobelessened.Thepupsmaysleepoutsidetheirnestboxesandsleepapartfromeachothermoreoftenastheperiodprogresses.
Changesinbasiccapacities.—Theretinaoftheeyeisnotcompletelyformeduntilabout4weeksofage;andtheEEG,indicatingthefunctionofthevisualportionofthecortexofthebrain,doesnotassumetheadultformuntil7or8weeksofage.Thismeansthatthepuppydoesnothavesensoryfunctionscompletelycomparabletothoseofanadultuntilseveralweeksafterthebeginningoftheperiodofsocialization.
Astomotorfunctions,thepuppyassumestheadultformsoflocomotionandchewingattheoutsetoftheperiodbutstillhasnotreachedanythinglikeadultcapacitiesbyitsend.A7-week-oldpuppyiseasytocatchevenwhenrunningattopspeed,anditcandoverylittledamagewithitsimmatureteethandjaws.Evenat12weeksapuppyisaclumsyrunnerwithlittleendurance.
Withregardtolearningcapacities,thepuppyhasattheoutsetoftheperiodtheabilitytomakerapidassociationsbetweenstimuli,andinthisrespectitissimilartoanadult.However,itsmotorresponsesarestillnotcompletelydeveloped,andthismeansthatwhilethepuppymaylearnagreatdealfromtheoutsideworld,itisstill
notcapableoflearningcomplicatedmotoractswhichrequirespeedandgoodmuscularcontrol.
Conclusion.—Duringtheperiodofsocializationthepuppybeginstoshowmostoftheadultpatternsofbehavioratleastinaplayfulform.Ingestivebehavior,whichwasmostimportantintheneonatalperiod,isnowreduced,andthemostprominentaspectofbehaviorissocialplay.Thisisthetimeduringwhichsocialrelationshipsareeasilydeveloped,eitherwithotherpuppiesorwithhumanbeings.Thebehaviorwhichinitiatestheserelationshipsissocialinvestigation,followedbyplayfulfightingandsexualbehavior,bothinvolvingbodilycontact.Theserelationshipscanbedevelopedwithanyindividualwhostayswiththepuppies.Atthesametimeweseetheappearanceofbehaviorwhichlimitstheformationofrelationshipswithcasualstrangers.Thefirstreactiontoastrangerisoneoffear.Asapuppybecomesolder,fearandescapereactionsbecomestrongerandmoredifficulttoovercome,sothatacasualstrangernevermakescontact.
Thisis,therefore,acriticalperiodfortheformationofsocialrelationships.Weshallexaminethisconceptmorecarefullyinpages110-12.
JUVENILEPERIOD
Thisperiodbeginswiththefirstlongexcursionawayfromthedenornestboxandendsatsexualmaturity.Thusitrunsfromapproximately12weeksofageupto6monthsorlater.Thechangesarenotasstrikingasbeforeandwillnotbetreatedingreatdetail.
Changesinbasiccapacities.—Allthesenseorgansappeartobefullydevelopedattheoutsetofthejuvenileperiod.Permanentteethbegintocomeinatabout16
attheoutsetofthejuvenileperiod.Permanentteethbegintocomeinatabout16weeksofage,andallareusuallypresentby6months.Growthcurvesalsobegintoflattenoutat16weeks.Theperiodofrapidgrowthisover,andthepuppyisapproximatelytwo-thirdsofitsadultsize.
Thedevelopmentofmotorcapacitiesinthisperiodconsistsofincreasesinstrengthandskillratherthantheemergenceofnewpatterns.Muchdependsontheenvironment.Puppiesraisedinopenfieldsaremoreactiveandskillfulthanthoseraisedinkennels,althoughanypuppyat4monthsisstillanawkwardandganglingannual.By6monthsthemostadvancedpupsareverysimilartoadultsinsizeandmotorcapacities.Inawildspecies,wewouldjudgethemtobecapableofexistingindependentlyfromtheirpar-
DEVELOPMENTOPBEHAVIOR109
ents.Theycontinuetogrowslowlythereafterandusuallyreachcompletephysicaldeyelopmentabouttheageoftwoyears.
Astobasiclearningcapacitiesthepuppyappearstobefullydevelopedbeforetheoutsetofthejuvenileperiod.Atabout4monthsofagethespeedofformationofconditionedreflexesbeginstoslowdown.Thisisprobablynotbecausethenervoussystemdeterioratesbutratherbecausewhatthepuppyhaspreviouslylearnedbeginstointerferewithnewlearning.Aswillbeseenlater,thereissomeevidencethatthebehaviorofthepuppybeginstoreachastableorganizationaboutthisage;thatis,hehasestablishedthefoundationforwhathewilllearninthefuture.Ontheotherhand,puppiesstillcannotbetrainedindifficulttasks,partlybecauseofpoormotorskillandpartlybecauseofashortattentionspanandreadyemotionalexcitability.
Changesinsocialbcliaviorpatterns.—Puppiesraisedinalargefieldfirstbegantomoveawayfromthenestareaandexplorethesurroundingenvironmentatabout12weeksofage.Thisprobablyrepresentsthebeginningofthepatternsofhuntingbehavior.Wealsohavesomeevidencethatpuppiesmakeatransitionfromonephysicalenvironmenttoanothermoreeasilyatthisstagethananyother.Distressvocalizationinresponsetoachangedenvironmentreachesalowlevelat12weeks(ElliotandScott,1961).Guidedogpuppiesusuallymakeasuccessfuladaptationwhenplacedinhomesat12weeks,butthosekeptinakennellongerthan14weeksshowincreasinglypoorperformanceduringtheirlatertraining(Pfaffen-bergerandScott,1959).
Themalepatternofeliminativebehaviorappearssometimeduringthisperiod,varyingconsiderablyaccordingtothespeedofdevelopmentoftheanimals.Indogsraisedoutsideakennel,Martins(1947)foundthatthisfirstoccurredbetween5and8months.Thisincludestheleg-liftingreactionatscentpostsandscratchingafterdefecation.
Agonisticbehaviorhasdevelopedintoadefinitedominance-subordinationpatternby15weeks,andthepuppiesconcernedshowthepatternsofbehaviortypicalofadults.Thismeansthattheoccurrenceofactualfightingismuchreduced,althoughthegrowlsandyelpsofthreatandsubordinationreactionsmayfrequentlybeheardinalitterraisedtogether.
Thedominanceorderalsolimitscontactwithstrangeanimals,asthepuppiestendtoattackstrangersplacedwiththem.Thedegreeoftolerancetowardstrangersdependsuponthebreedaswellasthestateofdevelopment.Tinbergen(1958)observedthatpuppies
growingupinanEskimovillagebegantodefendterritoriesatthetimeofsexualmaturity,whichwouldbeattheendofthejuvenileperiod.
Allelomimeticbehaviorbecomesmoreandmorecommon,thelittertendingtoreactasagroupinmanysituations.Whenoneanimalmovestoinvestigateanoiseormovement,therestusuallyfollow.Playfulsexualbehaviorcontinues,buttheanimalsareusuallydistractedfromthisbyanvothersortofstimulation.Suchincompletesexualbehaviorisnotusuallyseenunlesstheanimalsarecompletelyunawareoftheobserver.Thisisverydifferentfromtheconcentratedattentiononsexualbehaviorseeninadults.Estrusofthefemalesandtheemergenceofthecompletepatternofadultsexualbehaviorbybothsexesmarkstheendofthejuvenileperiod.
Conclusion.—Comparedtothepreviousperiod,thejuvenileperiodisoneofgradualchange,chieflvinvolvingthematuringofmotorcapacities.Itendswiththematurationofsexualcapacitiesandtheconsequentabilitytoformcompletesexualrelationships.
Behavioraldevelopmentcontinuesthroughoutlife.Thenextimportantchangesfollowthebirthofpupsandincludetheoriginsofepimeleticbehavior.Thisbehaviorenablesthedevelopmentofthemother-offspringsocialrelationship.Alongandstableperiodofmaturityfollows,endingwiththecessationofreproductiveactivity.Thisoccursabouttheageof8inmostfemalesand
reproductiveactivity.Thisoccursabouttheageof8inmostfemalesandconsiderablylaterinmales.Manydogsbegintoshowadeclineoffertilityandphysicalvigoraftertheageof5,althoughtheyfrequentlylivetothreetimesthisage.
CRITICALPERIODSINDEVELOPMENT
Wehavedividedthedevelopmentofthepuppvintoperiodsbasedonmajorchangesinsocialrelationships.Immediatelyafterbirththepuppyestablishesthenursingrelationshipwithitsmother,markingthebeginningoftheneonatalperiod.Thetransitionperiodconsistsofrapidchangesinthisrelationship.Atitsend,thepuppyiscapableofforminganewtypeofsocialrelationshipwhichwillpersistintoadultlife.Atthispointthemotherceasesherconstantcareofthepuppies,sothatthestrongestrelationshipstendtobeformedwiththelittermatesratherthanwiththemother.Theserelationshipsformthefoundationofthetypicalsocialgroupofadults,thepack.Therelationshipwiththemotherisstillfurtherweakenedwhenfinalweaningfromthebreastoccurs,althoughinwildCanidaetheparentscontinuetofeedthevonngforsomemonthsbyvomitingor
bybringingthemmeat.Theolderanimals,neverthelessmayspendonlyafewminutesoutoftheentiredayincompanywiththeirpups,spendingtherestofthetimehunting.Thenextmajorchangeoccurswiththeformationofsexualrelationshipsasthepuppiesbecomeadults.
Thesefactssuggestamajorhypothesis:thattheperiodatwhicheachnewrelationshipisformedisacriticalonefordeterminingboththenatureoftherelationshipandtheidentityoftheindividualswithwhichtherelationshipisformed.Forexample,theneonatalperiodiscritical,forunlessthepuppynursessuccessfully,itwilldie.Theperiodofsocializationiscritical,sinceitdetermineswhatspeciesandindividualswillbecomethechiefadultrelativesofthepuppy.Apuppytakenfromitslitterearlyindevelopmentandraisedbyhandwillformitsparamountrelationshipswithpeople,becomingan"almosthuman"dogandpayinglittleattentiontoitsownkind.Removedalittlelaterintheperiod,itformsstrongrelationshipswithbothdogsandhumanbeings.Stilllaterithasalreadyformedstrongrelationshipswithdogsanditstieswithhumanbeingstendtoberelativelyweak.
Thisisthemostimportantcriticalperiodinthelifeoftheanimal.Inadditiontothedeterminationofsocialrelationships,theemotionalsensitivityandstillundevelopedmotorandintellectualcapacitiesofthepuppysuggestthatthismayalsobeacriticalperiodforpossiblepsychologicaldamage.Emotionalsensitivity
alsobeacriticalperiodforpossiblepsychologicaldamage.Emotionalsensitivityisapparentlyanecessarypartofthesocializationprocess,andthisautomaticallymakestheanimalsusceptibletopsychologicaldamageaswell.
Stillanothercriticalperiodbeginswithsexualmaturity,whenthematingrelationshipisdetermined,alongwithpoororgoodadjustmentinsexualbehavior.Bothoftheseadjustmentsmaybegreatlyinfluencedbywhathasalreadyhappened,particularlyintheperiodofsocialization.
Wehavedefinedthedividinglinesbetweenperiodsasmajorchangesinsocialrelationships.Theperiodsthemselvesarecharacterizedbycertainprocesses.Thatintheneonatalperiodistheprocessofneonatalnutrition,ornursing.Thesameprocessgoesoninthetransitionperiod,butthereisalsoanewmajorprocessgoingon,thistimeabiologicalone.Thegreatestmaturationalchangesinbasiccapacitiestakeplaceinthetransitionperiod.Atitsendthepuppycanmoveindependentlyofitsmotherandalsobegintotakesolidfood.Furthermaturationalchangescontinuetotakeplace,butnothingassuddenanddrasticasthese.
Themajorprocessofthenextperiodisthatofsocialization,the
112BEHAVIORPATTERNS
formationoflastingsocialrelationships.Thisagainisanongoingprocesswhichprobablyneverstopsentirelyinthelifeoftheanimal,buttheperiodofsocializationisthepointatwhichthebiggestchangesoccurandalsothetimewhenitiseasiesttoinitiatesuchrelationships.
Anothermajorprocesswhichtakesplaceduringthisperiodofdevelopmentisthatoflocalization,inthesenseofaprocesscomparabletosocialization.Thepuppybecomesstronglyattachedtoaplaceandisseriouslyupsetifheismovedawayfromit.Ourdatashowthatthisprocessreachesitspeakat6to7weeksofagebutthattheemotionalresponsestobeingmovedcontinueforsometime.
Theresultsofsocializationandlocalizationaresosimilarthatwewonderwhethertheymayrepresentthesameprocessappliedtodifferentobjects.Thiswouldmeanthatthepuppybecomesattachedtoboththelivingandnon-livingpartsofitsenvironmentatthisage.
SUMMARYANDCONCLUSION
Apuppycomesintotheworldwithitsbehaviororganizedforlifeintheneonatalperiod,centeringaroundthefunctionofobtainingnourishmentfromthemother.Itishighlyprotectedfromoutsidepsychologicalstimulationbothbvmaternalcareanditsownimmaturity.Theneonatalpuppyisblindanddeaf,anditisdoubtfulifeventheolfactorysenseisdeveloped.Itsmotorcapacitiesaresolimitedthatitcanmoveonlywithinaradiusofafewfeet.Itscapacitiesforlearningarehighlylimitedcomparedwiththoseofolderpuppies,anditshowsalimitednumberofemotionalreactions.
Between2and3weeksofageaprofoundreorganizationofbehavioralcapacitiesoccurs.By3weeks,thepuppyisabletomoveandeatbyadultmethods.Allsenseorgansarefunctional,anditiscapableofmakingquickandeasvassociationsbetweenoutsideevents.Manyofthepatternsofadultsocialbehaviorandtheiraccompanyingemotionsappearatthesametime.Theacquisitionofthesecapacitiesisfollowedbvarapidorganization,throughlearning,ofbehaviorinrelationtootheranimals,people,andplaces.Whateverhappensheresetsageneralpatternwhichwillaffectalmosteverythinginlaterlife,becausebytheendoftheperiodthepuppyhasformedpatternsofrespondingtothemajorinfluencesinanysortoffutureexistence.Therewillbeotherperiodsofrapidorganizationofbehaviorinlaterlife,atthetimeofsexualmaturityandbirthoftheyoung,buttheireffectswillbemorelimited.
\>researchworkers,wecanconcludethatthepuppyisinmany
waysanidealanimalforstudyingtheeffectsofearlyexperience.Theperiodsofdevelopmentaresowelldividedandeasilyrecognizedthatitshouldbepossibletogivepuppiesthesameexperienceatdifferentagesandcometodefiniteconclusionsregardingtherelationshipbetweenexperienceandmaturation.Puppydevelopmentisahappycompromisebetweenextremelyshortdevelopment,whichpermitsverylittleeffectofexperience,andextremelylongdevelopment,whichmayrequirealifetimetoanalyze.
Thesestudiesonthedevelopmentofbehaviorleadtotwogeneralprinciplesregardingouroriginalproblemoftheeffectofheredityuponbehavior.Oneoftheseisthatgeneticdifferencesinbehaviormustbeproducedthroughdevelopmentalprocesses.Wecannotthinkofbehaviorasbeingsomethingrelativelyfixedandunchangedsuchashaircolor,butrathersomethingwhichisrapidlydevelopingandchangingthroughoutearlylifeandwhichcontinuestochangeastheanimalgrowsolder.
Hereditaryfactorsmustthenactbyaffectingdevelopmentalprocesses,suchasthegrowthanddifferentiationofsenseorgansandorgansystems.Hereditymayalsoaffectongoingphysiologicalprocessesthroughoutlife,oneofwhichistheprocessoflearningitself.Thisinturnisthebasisforothermajorprocesses:thefoundationofsocialrelationshipsandrelationshipswiththeinanimateenvironment.
Asecondprincipleisthatthemajorityofhereditarydifferencesinbehaviorareexpressedascomponentsofsocialrelationships,eitherwithotherdogsorwithpeople.Evenwhenadogiscompletelyalone,hemayreacttotheabsenceofothers,andinfactusuallydoesso,showingeveryevidenceofemotionaldistress.Thiscomplicatestheproblemofmeasurementofhereditarydifferences,becauseanysocialrelationshipisaninteractionbetweentwoindividuals,andisthereforeaffectedbytheheredityofboth.However,itisjusttheserelationshipswhichcharacterizetheorganizationofadultbehaviorandformwhatweordinarilycallindividualityorpersonalityinahumanbeing.
HUMANCOMPARISONSANDAPPLICATIONS
Whenwetrytocomparethedevelopmentofapuppywithahumaninfant(Scott,1963a),wefindthatmuchoftheinformationwhichwewouldliketohaveismissing.Childpsychologistshavegenerallystudiedchildreninschools,wheretheyareeasytogetat,andveryseldominhomes,wheretheirmostbasicsocialrelationships
BEHAVIORPATTERNS
areformed.Thismeansthat,inspiteofitstheoreticalimportancetolaterbehavior,thestudyoftheperiodofearlyinfancyhasbeenrelativelyneglected.
TABLE4.6NaturalPeriodsofDevelopmentinDogandMan
Dog
Man
Wedoknowenoughtomakeatleastsomegeneralcomparisons.Likethatofthenewbornpuppy,thebehavioroftheneonatalinfantisprimarilyconcernedwithneonatalnutrition.Theinfanthasbetterdevelopedsenseorgansandrespondstobothsoundandlight.However,visionofthehumanneonateisnotperfectlydeveloped,astheEEGreachesitsadultformatabout8yearsinsteadof8weeks
developed,astheEEGreachesitsadultformatabout8yearsinsteadof8weeksasinthepuppy.
Inmotorcapacitiesahumanneonateislessdevelopedthanthepuppy,notevenbeingabletocrawl.Itsmajortransitiontotheseadultcapacitiescomesbetweenapproximately7and14months,beginningwhenthebabydevelopsitsfirstteethandbeginstocrawl,
andisendingwhenitislaterabletowalk.Inthisrespectthe14-month-oldbabyisquitesimilartothepuppyofthreeweeks.
Herewecometoamajordifference.Whilethecapacityforsocialresponsivenessinthepuppydevelopsafteritstransitiontotheadultformoflocomotion,thebabydevelopsthecapacityforrapidconditioningbyoneortwomonthsandbeginstosmileinresponsetosocialstimulationlongbeforeitsgeneralmotorcapacitiesdevelop.From2until6months,thebabyrespondsindiscriminatelytoallhumanfacesbutbytheendofthistimeisbeginningtodevelopfearresponsestostrangersandby8monthsofageshowswhatisoftencalled"8-monthsanxiety."Itisonlvthenthattheaveragebabybeginstocrawlanddevelopitsothermotorcapacities.
Thus,theperiodofhumanprimarysocializationprecedesthedevelopmentoftheadultcapacitiesoflocomotioninsteadoffollowingthem,asinthepuppy.Thismeansthatthebabydevelopsitsstrongestrelationshipswiththepersonorpersonswhotakecareofitatthistime,usuallythemother,butalsothefatherandsiblings.Thisalsoproducesanemphasisonthedevelopmentofstrongrelationshipsbetweenolderandyoungerindividualsratherthanthecanineemphasisonstrongrelationshipsbetweencontemporaries.
Wecanalsoseethatindifferentspeciesofmammalsdifferencesarenotsimplyamatteroflongerorshorterdevelopment;theorderofcertainmajordevelopmentalchangesisactuallyreversedinthetwospecieswehavecompared.This,ofcourse,raisesthequestionofhowmuchvariationofthissortcantakeplacewithinaswellasbetweenspecies.
Thesimilaritiesbetweenhumanandpuppydevelopmentsuggesttheexistenceofacriticalperiodforprimaryhumansocializationhavinggreatpracticalsignificancefortheproblemsproducedbythelossofparentalcareandchangesproducedbyadoption.Whiletheevidenceissomewhatunclearduetotheundesirabilityofmakingdeliberateexperimentswithsuchseriousconsequencesonhumanbeings,alloftheevidenceindicatesthatsuchaperiodexistssometime
onhumanbeings,alloftheevidenceindicatesthatsuchaperiodexistssometimeduringthefirstyear.
Thisconclusionisbolsteredbytheevidencefromotherspeciesofanimals.Everyhighlysocialspeciesofanimalwhichhasbeenstudiedsofarhasashortperiodearlyinlifewhenprimarysocialrelationshipsareformed.Inbirds,withtheirveryshortperiodsofdevelopment(asongsparrowprogressesfromhatchingtoadultflyingin4weeks),theprocessofsocializationtakesplaceextremelyrapidlyandsohasreceivedthename"imprinting."Inthebird,thecriticalperiodforsocializationmaybeamatterofafewdaysorevenhours;
116BEHAVIORPATTERNS
inthepuppyamatterofweeks;andinthehumaninfantamatterofmonths.Theselongerperiodspermitthedevelopmentofawiderandlessspecificsetofrelationships,butthebasicphenomenonappearstobethesame.
Whenwerealizedthetheoreticalandpracticalimportanceofthesediscoveries,wedidtwothings.Onewastocalltheseresultstotheattentionofaconferenceofscientistsinterestedincomparinghumanandanimalbehavior.(Scott,1952).Werealizedthatsuchageneralprincipleasthatofcriticalperiodscouldbeestablishedonlythroughtheco-operationofmanydifferentscientistsandinstitutionsworkingonmanydifferentspeciesofanimals,andcomparingtheresultswithobservationsonchildren.Theotherwastoinstitutearesearchprogramatourownlaboratory,inordertoverifytheobservationswehavedescribedinthischapterthroughexperimentalmeans,andalsotodiscoverthephysiologicalandpsychologicalcausesofthesephenomena.Theresultsofthisprogramaredescribedinthenextchapter.
THECRITICALPERIOD
Aswehaveseenintheprecedingchapter,ourstudiesofthedevelopmentofbehaviorshowthatapuppyentersintoaperiodofgreatchangeandsensitivitywithregardtosocialrelationshipsatapproximately3weeksofage,andthathisexperiencesatthistimedeterminewhichanimalsandhumanbeingswillbecomehisclosestsocialrelatives.Thisisatimeofmajordecisionaffectingalltherestofhislife,andtheperiodisthereforeacriticalone.
Inordertotranslatethisintoaworkablescientifictheory,wemustsharpenuptheconceptofcriticalperiods.Byacriticalperiod,wemeanaspecialtimeinlifewhenasmallamountofexperiencewillproduceagreateffectonlaterbehavior.
whenasmallamountofexperiencewillproduceagreateffectonlaterbehavior.Todrawananalogy,itisagreatdeallikepullingthetriggeronahigh-poweredrifle.Averysmallamountofeffortcausesthebullettotravelathighspeedandproduceasmashingimpactatagreatdistance.
Thisisthekindofscientificdiscoverywhichcanhaveimmensepracticalvalueifitturnsouttobecorrect.Agreatpartofscientificeffortisdirectedtowarddiscoveringpreciselythissortofcausalrelationships.Itisnotenoughtoknowacause,foriftheeffortrequiredtomanipulateitisequaltoorgreaterthanitsresult,thediscoveryhasonlylimitedusefulness.
Goingbacktotheideaofthecriticalperiod,wecanseethatitisarelativeratherthananabsoluteconcept.Thedifferencebetweentheamountofeffortneededtoproducethesameeffectatdifferentperiodsdeterminesjusthowcriticaltheperiodis.Inthecaseofthepuppy,itlooksasifasmallamountofcontactshortlyafter3weeksofagewillproduceastrongsocialrelationshipwhichcanbeduplicatedonlybyhoursorweeksofpatienteffortatlaterperiodsinlife—if,indeed,itcanbeduplicatedatall.
117
118BEHAVIORPATTERNS
Itmightbesupposedthattheeffectofthissortofcontactisinverselyproportionaltoage,i.e.,theyoungertheanimalthegreatertheeffect.Ifthisweresowecouldnotproperlyspeakofacriticalperiod.Inordertodefineaperiodtheremustbedefiniteandimportantchangesboundingitsbeginningandend.Oneimportantscientificproblemisdeterminingthenatureoftheselimits,forthisinformationmayinturnleadtothediscoveryofhowtomodifyorprolongtheperiod.
Theremaybemorethanonecriticalperiodinthelifeofanindividual.Theperiodwehavedescribedinthepuppyisacriticaloneforthedeterminationofprimarysocialrelationships,butthisneednotbetheonlyone.Therecouldbeavarietyofcriticalperiodsindevelopmentfordifferentevents.Forexample,wehavestatedthehypothesisthatthetimeinwhichanyimportantsocialrelationshipisbegunisacriticalonefordeterminingthenatureofthatrelationship.Thetimesofthefirstmatingandthebirthofoffspringshouldalsobecriticalperiodsfortheformationofsexualandparent-offspringrelationships.
Ontheotherhand,differentsortsofcriticalperiodsmightcoincide.The
Ontheotherhand,differentsortsofcriticalperiodsmightcoincide.Theemotionalsensitivityofthepuppyduringtheperiodofsocializationsuggeststhatthisperiodmightalsobeacriticaloneforpermanentpsychologicaldamage.Ifthenatureandimportanceofcriticalperiodscanbeestablishedfirstinanimalsandeventuallyinhumandevelopment,theconcepthasimmensepracticalpossibilitiesfortheimprovementofmentalhealth.Ifweknewthatarelativelysmallamountofeffortattherighttimeindevelopmentwouldstartachildtowardbeingabasicallyhappyandproductiveindividual,wecouldmakevaststridesintheimprovementinhumanbehaviorwithinageneration.Atthepresenttimeweknowthatdisorganizedfamilyconditionsappeartohaveabadeffectonyoungchildren.Ifthecritical-periodhypothesisturnsouttobecorrect,wecaninthefuturesaytoaparent:"Ifyoudothusandsoataparticulartime,youwillbemorelikelytohaveawell-adjustedchildthanifvoudoitatanearlierorlatertime."Meanwhile,wecangetsomeideaoftheneedfulscientificinformationfromourstudiesonthedog.
BOUNDARIESOFTHECRITICALPERIOD
Aswehaveseenintheprecedingchapter,itiseasytoestablishabeginningpointforthecriticalperiodofprimarysocializationinthepuppy.Between^and3weeksofageaverylargenumberofchangestakeplaceinrapidsuccession,andallofthesemodifythecapacity
THECRITICALPERIOD119
forformingaclosesocialrelationship.Theperiodofchangeortransitionbeginswiththeopeningoftheeyesandincludestheopeningoftheearsandthestartleresponsetosound.Atitsendthepuppyiscapableofwalking,sothatitcaneitherapproachoravoidanotherindividual.Itbeginstoeatsolidfoodandhencestartstobeindependentofthemother.Itdevelopstheabilitytomakerapidassociationsbetweenoutsideeventsandunpleasantfeelings.Thislastchangeisprobablythemostimportantonewithregardtoestablishingaboundaryforthecriticalperiodforformingprimarysocialrelationships,becausethepuppyisnowcapableofdiscriminatingbetweenindividuals.Thiscapacityisdifficulttodeterminebyobservationandcanbemeasuredaccuratelyonlybyaseriesofelaborateexperiments.Fortunatelythereisachangeinbehaviorwhichseemstobecloselycorrelatedwithit,andwhichiseasytodetermine—theappearanceofthestartleresponsetosound.Wecanarbitrarilyusethisasamarkertoindicatethebeginningofthecriticalperiod.
Howisthisdevelopmentalchangerelatedtoage?Wecanrecordthedateon
Howisthisdevelopmentalchangerelatedtoage?Wecanrecordthedateonwhichthestartleresponseoccursandcalculatetheageofeachanimal.Therewillobviouslybesomevariationinage,reflectingdifferencesinthestateofdevelopment,andoneimportantpracticalproblemisthatofdeterminingtheextentofthisvariationinnormaldogpopulations.
Normalvariationindevelopment.—Inthefirstplacethereisvariationintherateofprenataldevelopment.Theaveragegestationperiodofthedogisusuallyreckonedat9weeks,or63daysaftertheonsetofreceptivity.Thisitselfisonlyanestimate,becauseovulationtakesplaceapproximately72hoursbeforetheendofreceptivity,andthetotallengthoftheperiodofreceptivityvariesagreatdealindifferentanimals.Embryonicdevelopmentinthedogisunusualinmanyrespectswhicharecorrelatedwithitslifeasahuntinganimal.Thefertilizedeggdevelopsveryslowlyanddoesnotbecomeimplantedintheuterusfor3weeks.Evenafterthis,itbeginsrapiddevelopmentonlywhentheplacentahasbeenestablished.Thismeansthattheembryogrowsveryslowlyatfirstandveryrapidlyinthelast4or5weeksofpregnancy,sothatthebitchhasarelativelyshortperiodwhensheisheavyandincapacitatedforactivelife.Boththetimeinwhichtheeggsbecomeimplantedandtheirpositionintheuteruscouldproducevariationinthestateofdevelopment.Wehavenoevidenceonthedog,butstudiesontheembryologyoftheguineapigshowthatembryosofthesamechronologicalagefromconceptioncanvaryatleastadayortwoinstateofdevelopmentwithoutanyobvioussignofabnormality(Scott,1937).Morethanthis,
thereissomevariationinthetimesatwhichpuppiesareborn,somelittersbeingobviouslymorematureatbirththanothers.Thisprobablyaddsatleastanotherdayortwoofdevelopmentalvariation.Finallv,thereistheaccuraevofthemeasurementofa°;eitself.Whenwerecordedtwolittersasbornonthesamedate,theyactuallycouldhavebeenborn24hoursapart,sincenoobservationsweremadeatnight.Allthiswouldadduptoarangeof5or6days'variationindevelopmentforanimalsrecordedashavingbeenbornonthesamedaytodifferentmothers.
Letusnowlookattheactualfigures.Weexaminedandtestedthedogsonceperweekinordertoavoidexcessivehandlingintheearlystagesofdevelopment.Hencewemustestimatevariationonthebasisoftheseweeklyfiguresratherthanondailyones.Thefirstchangeistheopeningoftheeves(Table5.1).Outof195purebred
TABLE5.1
EstimatedVariationinDevil:?v:i:-"iaxEventsAssociatedwiththeBeg::-ofthePeriodsofTransitionandSocializationinPurebredPuppies
EyescompletelyopenITransitionperiod15.0
startletosound\Socializationperiod19.51:
FirstteetheruptedSocializationperiod-v2.9
puppies,onlyonecockerspanielhaditsevescompletelvopenatoneweekofage.Therearelars;edifferencesindevelopmentbetweenthedifferentbreeds,butweightingthebreedsequallywefindthat59percenthavetheeyescompletelvopenat2weeksand100percentat3weeks.Assumingthatthetimeofopeningtheevesisdistributedinanormalcurve,wecanestimatethattheaveragetimeforthiseventis13dayswithastandarddeviationof2.3days.Thestandarddeviationmeasuresthepointofinflexionofthenormalcurve,andthismeansthattwo-thirdsofthepuppieswouldopentheireyesbetween10.7and15.3days.One-sixthofthemmightopentheireyessoonerandone-sixthlater.Thisresultfitsvervwellwithourtheoreticalexpectationthatwhiletheaveragemightfallonaparticularwemightexpectarangeofvariationofapproximatedaweekinthesedevelopmentale\\Qts5kott,195s
Amoreimportanteventformarkingthecriticalperiodisthedate
onwhichtheanimalsgivethestartleresponsetosound.Twoani-
>r1pctionat14days,and74percentat
3weeks.Theestimatedaveragewouldbe19.5dawswithastandard
deviationof2.3days.Again,thiswouldmeanthatone-sixthofthe
THECRITICALPERIOD121
animalsshouldshowthisresponsebefore17.2daysandone-sixth(theslowdevelopers)after21.8days.
Thesefiguresareimportanttorememberininterpretinganyexperimentalresults.Ofanimalsgivenexperimentaltreatmentbetween14and21daysofage,three-quartersofthemwouldhavepassedintothecriticalperiodsometimeduringtheweek,andonlyaboutoneinahundredmighthavespenttheentireweekinthisperiod.Wewouldthereforeexpecttheexperimentalresultsfromthisperiodtobequitevariable.
60-
k-I->(-lL-k-HI,SOCIALIZATION>k—XZ,JUVENILE^
*>EYESOPEN^ADULTEEG
/z-CONDITIONINGV^MOTHEROUT
/BEGINS/
8ea*--"J..
Fig.5.1.—Developmentoftheheartrate.Notethatallbreedsshowadepressionoftheheartrateduringtheearlypartoftheperiodofsocialization.
oftheheartrateduringtheearlypartoftheperiodofsocialization.
Wecannowattempttodefinetheendofthecriticalperiod.Thisisnotaseasytodo,andourmeasurementsaremuchlessexact.Thedataonthedevelopmentofthebrainwaves(basedonasampleofonly10puppies)indicatesthatthematureconditionisreachedsometimebetween7and8weeks(CharlesandFuller,1956).Mothersbegintocompletelyweantheirpuppiesfromthebreastatabout7weeksofage.Theymayormaynotbeinfluencedbythedevelopmentofthepups,butweaningdoesindicateachangeinsocialrelationships.Ourmeasurementsoffearfulreactionstohumanhandlingindicatethatthemaximumreductionofthisbehavioroccursbefore7weeksofage(Fig.5.7).However,ourbestobjectiveevi-
22BEHAVIORPATTERNS
denceofchangeatthistimecomesfromthemeasurementofheartrates.AscanbeseeninFigure5.1,allbreedsshowareductionintheheartratebetween1and3weeksofage,andintwoofthebreedsthischangebeginsbetween1and2weeks.Alowpointoccursat3and4weeks,thisbeingextendedto5weeksinthebasenji.Ahighpointisreachedagainat6weeksinthreeofthebreeds,7weeksinanother,and8weeksinanother.Thischangeinheartratemayreflecteitherachangeintheabilityofthisresponsetobeconditioned,thusbringingitundertheadulttypeofemotionalcontrol,oritmaysimplyreflectachangeintheemotionalresponsestothehandlers.Atanyrate,itisthemostobjectivemeasureofdevelopmentalchangewhichwehaveavailable,anditledustoestimatethattheendofthecriticalperiodoccurredatapproximately7weeks.
Wehaveonemorepieceofconfirmingevidence:thevocalreactionofagroupof32beaglepuppiestoisolationinastrangeroomatdifferentages.Themaximumvocalizationwaselicitedbetween6and7weeks,witharapiddecreasethereafter.Allthesedataindicatethatimportantdevelopmentalchangestakeplaceat7weeksofageorshortlythereafter,andwetentativelysettheendofthecriticalperiodatthisage.Thisdatecanbedecreasedorincreasedbyindividualvariabilityofatleastaweek,sinceotherdataindicatesthatindividualvariabilityincreaseswithage.Asfurtherexperimentalworkshows,thisestimatewasactuallytooearlybyseveralweeks.
Developingatechniquefortestingthecriticalperiodhypothesis.—Ahealthylitterof6beaglepuppieswasbeingraisedinthenormaltestingprograminthe"SchoolforDogs"whenDr.EmilFredericsonjoinedourstaff.Heperformedapilotexperimentontheseanimalsbytakingthemawayfromthemotherand
pilotexperimentontheseanimalsbytakingthemawayfromthemotherandlittermatesatdifferentagesandgivingthemclosecontactwithhumanbeings(Scott,Fuller,andFredericson,1951).Thefirstpuppywastakenatbirthandraisedonabottleuntil2weeksofage.Asidefromdifficultiesingettingittonurse,itshowednobehavioraldisturbance,althoughitwasnotaswellnourishedasitslittermates.Thesecondpuppywastakenawaybetween2and4weeksofage.Itreadilyadjustedtothenursingbottleandshowednodisturbanceofbehavioreitherwhentakenawayorwhenreturned.Accordingtoourtheoreticalcalculations,thisexperiencewithpeopleincludedaweekormoreoftheearlypartofthecriticalperiod.Thethirdpuppy,removedfromthemotherat4weeksofage,showedexcessiveemotionaldisturbanceandatonepointyelpedcontinuouslyfor24hours.However,itsoonbecameadjustedtothefamilyandhomeinwhichitwaskeptandbegantoaetlikeapetdog.Thefinalexperimentalpuppywastaken
THECRITICALPERIOD
123
awayfrom6to8weeksofage.Becausethecriesofthepreviouspuppyhadupsetthehumanfamily,thispuppywaskeptatthelaboratoryandgivenextensivecontactwithpeopleonlyduringofficehours.Itshowedthesamesortofemotionaldisturbanceasthepreviouspuppv,butnotsointensely.Theremainingtwoanimalswereleftwiththemotheratalltimesandusedascontrols.
Afterthisexperience,allthepuppieswereputbackwiththemotherandlittermatesandgiventheregulartestingroutine.Withinaveryshorttimethebehaviorofonewasindistinguishablefromanother.Inthissituationanyeffectsoftheirearlyexperiencewerenogreaterthanthenormalvariabilityinthelitter.
Wenowattemptedtofindoutwhethertheearlyexperiencehadsomelessobviouseffect,andwetriedtoduplicatetheoriginalexperiencebytakingeachanimaltoastrangeprivatehomeandkeepingitovernight.Table5.2showsthegeneralresults.Initsover-all
TABLE5.2RelativeAdjustmentofPuppiesat1YearofAge
Test
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score,theanimalwhichhadbeenremovedbetween4and6weeksmadethequickestandbestadjustmenttothesituation,confirmingourexpectationregardingtheextentofthecriticalperiod.Ontheotherhand,oneofthecontrolsdidalmostaswell,andweconcludedthattheexperienceofsocializationintheordinarylaboratoryconditionswassufficienttoproducealmostasgreataneffectonsomeanimalsasdidtheintensivehometreatment.Oneofus(Fuller,1961)hassincefoundthatsemi-isolatedpuppiescanbesuccessfullysocializedwithaslittlehumancontactastwo20-minuteperiodsperweek.Wethereforebegantolookforanothertechniquewhichwouldproducemaximumdifferences.
Inthepreviouschapterwehavedescribedtheresultsofobservingdogslivinginlargefieldsapartfromhumanbeings.Theexperimentincludedraisingpuppiesinthesamefields,andoneobviousresult
124BEHAVIORPATTERNS
wasthatthesepuppiesbecameextremelywild.Wetookonehomeattheageof12weeksandattemptedtomakeapetoutofit.Itwasextremelyfearfulatfirst,butbyconfinementandhandfeedingweeventuallycalmeditdownandgotittoacceptclosecontactswithpeople.However,itwasalwavsdifficulttocontrolandtimidwithstrangers,andwhenevertherewasachoicebetweenhumananddogcontactsitchosethedog.Itlookedasifrearinginlargefieldsproducedthemaximumeffectforwhichwewerelooking.Beaglesandfoxterriersbecameequallywild,theonlydifferencebeingthatthelattercouldnotbetrustednottokilleachother.
Stillanotherexperimentgaveusanideaofthelimitswithinwhichwecouldwork.MissBarbaraArndt,asummerstudent,raisedalitterofsixbeaglesinalargefield,makingdirectcontactwiththemonlyonceaweek,whenthevwere
largefield,makingdirectcontactwiththemonlyonceaweek,whenthevwereweighed,andeverytwoweeks,whenshegavethemahandlingtest.Shelefttheparentsadishoffoodonceeachday,immediatelygoingawaytomakeobservationsfromthegate,whereshestoodabout20or30feetawayfromthepuppieswithonlyherheadandshouldersshowing.Twoofthepuppiesweretakenawayfromtheparentsat3weeks,raisedbyhandfor2weeks,andreturned.Undertheseconditions,noneofthepuppiesbecameexcessivelytimid,althoughallsixeventuallyshowedavoidancescoresabovethemeanofthoseraisedinthelaboratorywithdailycontactwithpeople.Thehand-rearedpuppiesweretheleasttimidwhenreturnedtothepen,buteventuallygrewmoretimidandmuchliketheothers.Fiveofthesixpuppiesweremuchmoreresponsivetotheobserverthantoanvoneelse,andnoneofthemactedlikethewilddogsofearliertests.Itbegantolookasifaprimarysocialrelationshipwithahumanbeingcouldbeformedwithaverysmallamountofcontactduringthecriticalperiodand,infact,thatitmightbeformedmerelybyhavingthepersoninsightatfrequentintervals.However,thepuppiescouldstillhaveassociatedtheobserverwithbeingfed,andbecomesocializedinthatway.
The"wilddog"experiment.—Withtheseresultsinmind,Freed-man,King,andElliot(1961)designedanexperimentbasedonlargenumbersofpuppies.Thevusedthelargeoutdoorfields,introducingfoodandwaterthroughaholeinthefencesothattherewasalmostnocontactwiththeexperimenters.Thevbroughtineachexperimentalpuppyforonlyoneweekandgaveitstandardizedcontactwiththeexperimenterseachdaw
Fromtheevidencecitedabove,theexperimenterssupposedthatthecriticalperiodextendedroughlyfrom3to7weeksofage,andtheyattemptedtosocializepuppiesat2,3,5,7,and9weeks,leaving
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125
certainpuppiescontinuouslyaloneuntil14weeks.Atthistimeallthepuppieswerebroughtintothelaboratoryandretested.
Theresultscanfirstbeanalyzedintermsofinitialeffects.Thepuppiesweregiventhehandlingtestimmediatelyafterbeingbroughtinandagainafteraweekofhumancontact.Figure5.2
23456AGEINWEEKS
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769
Fig.5.2.—Effectofsocializationatdifferentagesuponavoidanceofanactivehandler.Noteconsistentriseofavoidancescoresafter5weeksofage.Alargenumberoftheresponsesat2and3weeksofageareofthe"noresponse"category;hencescoresattheseagesarenotcompletelycomparabletothoseatlaterages.Lengthoflinesdenotesthechangeresultingfromcontact;topoflineindicatesinitialscore.
showsthatthepuppiesbroughtinat5weeksofageshowedtheleastinitialavoidanceofhumanhandlers,whilethosebroughtinearlierorlatershowedlargernumbersoffearresponses.Nevertheless,afteraweekofcontactwiththeexperimenters,thepuppiestakenat3weeksofageshowedtheleastfear,andthosetakenat5weekswererelativelytimid.Thus,themaximumreductionoffearwasproducedat3weeks,andtheminimumat5.
Inanothertest(the"PassiveHandlerTest"),theexperimentersatquietlyintheroomwiththepuppyeachdayfor10minutesandrecordedhowlongittookthepuppytoapproachandremainincontact.At2weeks,thepuppiesweresoimmaturethatitwas4daysbeforetheybegantospendthefulltimewiththeexperimenters.At
3and5weeksthisoccurredonthefirstday,butitwastwodaysbeforethe7-week-oldpuppiespassedthetest,andthreedaysbeforethisoccurredwiththe9-week-oldpuppies.
Thuswehavemeasuresofseveraldifferentkindsofbehavior.Thefirstisthepositiveresponseofmakingcontactwithapassiveandhencenon-frighteningnewindividualintheenvironment.Thisbe-
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Fig.5.3.—Timingmechanismslimitingtheprocessofsocializationinpuppies.Initially,thepuppiesareunabletorespondtoanactivepersonbutshowlittlefear.Later,thedevelopingfearresponselimitsthecapacitytobeattracted.
haviorismostobviousfrom3to5weeksofageanddeclinesthereafter.Second,thereisthenegative,orfearresponse,tonewandactiveindividuals,whichcontinuouslyrisesafter5weeksofageandprobablycausesthedeclineoftheearlierapproachbehavior.Third,thereistheresponseofrecoveryfrominitialfears,whichisalmostinstantaneousat3to5weeksofageandbecomesprogressivelyslowerthereafter.Allthesebehavioralprocessesaffecttheformationo!theyoungpuppy'sfirstsocialrelationshipsduringthecriticalperiod.TheirnetresultisthatthepuppymakesrapidcontactwithacompletelystrangeindividualonlywithintherelativelyshortperiodFrom3to5weeksofage.
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127
Wemaynowconsiderthelatereffectsoftheseexperiences.Thepuppieswereallremovedfromthelargefieldsat14weeksofage,broughtintothelaboratoryrearingrooms,andsubjectedtoaseriesoftests,includingnewonesaswellasthosepreviouslygiven.Onetestwhoseresultsshowedthelargestdifferenceswasthatofleash-control.Apuppywhichhasneverbeenonaleashbecomesalarmedandfearful,bothinreactiontorestraintandtobeingledintostrangeplaces.Thetestconsistedofleadingthepuppythroughthelaboratorybuildingandupthestairs(themostfrighteningpartofthetrip)andisdescribedindetailinchapter9.TheresultsareshowninFigure5.4.Thoseanimalstakenat5,7,and9weeksmadethebest
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Fig.5.4.—Performanceintheleash-controltest.Animalssocializedat5,7,and9weeksofagebalkedfewertimeswhenledintostrangesituations.
scoresontheover-alltest.Animalsbroughtinforthefirsttimeat14weeksandthosetakenat2and3weeksdidmuchworse.One14-weekanimalwasgivenintensivehumancontactandtrainingforoveramonthandshowedonlyslightimprovement.
Partofthetestincludedofferingafoodrewardattheendoftheroute.Severelyfrightenedanimalsrefusedtoeat,andthebestresponsewasmadebythoseanimalstakenat5and7weeksofage(Fig.5.5).Whenwetakeallagestogetherandrankthemaccordingtoperformanceoneachtest(Table5.3),weseeadefinitetrend.The
BEHAVIORPATTERNS
45
0246810
AGEWHENSOCIALIZED
Fig.5.5.—Eatingduringtheleash-controltest.Animalssocializedat5and7weeksofageatemoreoftenthantherest.
controls(14-weekgroup)gavethepoorestperformancein4outof6tests,whiletheanimalstakenat7weekswerebestin5outof6.Nextbestwerethosetakenat5weeks,confirmingourassumptionsregardingthelengthofthecriticalperiod.However,therelativelygoodperformanceofanimalstakenat9weeksshowsthatthereisno
TABLE5.3
RankOrderofPuppiesoxTestsGivenAfter14WeeksofAge(AfterFreeuman,King,andElliot,1961)
ranks.
THECRITICALPERIOD129
sharpcut-offpointafter7weeks.Rather,thisseemstobethepeakfromwhichadeclineinthecapacityforsocializationbegins.Theendoftheperiodofsocializationmustbeplacedintheneighborhoodof12to14weeks.
Theresultsofthis"wilddog"experimentalsoleadtotheconclusionthatthe
Theresultsofthis"wilddog"experimentalsoleadtotheconclusionthattheprocessofsocializationisacomplexone,involvingseveralbehavioralmechanisms.Similarexperienceatdifferentageswillproducedifferentresults,butthefinaleffectsalsodifferwiththekindofbehaviortested.
BEHAVIORALMECHANISMSINEARLYSOCIALIZATION
Theeffectsoftransferringthecareofayounganimalofonespeciestothatofanotherduringorbeforethenormalperiodofsocializationaresostrikingthatoneislikelytobehighlyimpressedwiththeeffectofwhatseemstobeasimplebehavioralfactor.Thisis,however,acomplexphenomenoninvolvingmanydifferentbehavioralmechanisms.Weobtainedsomecluesastowhatthesemightbefromthefollowingexperiments.
Manyyearsagowetookafemalelambawayfromthemotheratbirthandraiseditonabottlefor10days(Scott,1945).Wethenreturnedhertothefieldinwhichtheparentflocklived.Sheapproachedtheothersheepcuriously,butthefemalesbuttedher,andshemadenofurtherapproaches.Threeyearslaterthisanimalwasstillfollowinganindependentcoursearoundthefield,notjoiningtheflock,eventhoughshehadbeenmatedandhadbornelambsofherown.Wethentriedthesameexperimentwithayoungmalewhichhadbeenrejectedbyitsmotherandraisedonthebottle.Duringthefirsttwoorthreedayshehadsomecontactwithothersheep,sothattheexperimentswerenotexactlycomparable.Themaleactedinthesamewayasthefemalewhenhewasyoung,butashegrewolderandbecamesexuallymaturehebecameinterestedinthefemalesandbegantoassociatewiththeflockmoreandmore.Thisshowedthatoneofthepositivemechanismsproducingsocialrelationshipsintheflockisthesexualbehaviorofmales,althoughthisfactorisunimportantinfemales.
Later,Collias(1956)performedaseriesofexperimentsattheCornellUniversityBehaviorFarmwhichclearlybroughtoutsomeofthebehavioralmechanismsofprimarysocializationinthesheep.Ifalambistakenfromitsmotheratbirthandreturnedatanytimewithinfourhours,shewillacceptitandallowittonurse.Afterthis
timesherejectsit.alons;withanvotherstrangeIambs.Thusthecriticalperiodforsocializationinsheepisshortandsharplylimited,butlimitedbythebehaviorofthemothersratherthanthatofthelambs.
Meanwhile,wedidanexperimentwithavoungfemalepuppy,similartotheonewehadlonewiththenewbornlambs,andexpectedtogetasomewhatsimilar
wehadlonewiththenewbornlambs,andexpectedtogetasomewhatsimilarresult.WetookahybridpuphichsoonbecameknownasChristy)andraisedherfrombirthcompletelyawayfromotherdoss,withtheenthusiastichelpoftheentiresummerstudentcolonyattheJacksonLaboratory.Asmiz-'havebeenexpected,shebecameavervfriendlypuppy,normalinhealthandappeara:.dcA:sofas;eweintroducedhertoother
dogsforthefirsttime.Shewassomewhatfearfulatthestart,butnotforlong.Althoughadultanimalsdidsomegrowlingather.theymadenorealattacks.WhenshewasplacedwithherownUttermatestheyreactedwithplavfulas;ness,towhichsherapidlyre-
sponded.Within4days,shecouldnotbetoldapartfromtheotherseptthatsheomewhatmoreresponsivetohumanbeings.
Thisindicatedthatoneofthepositiveresponseswhichleadstosocializationistheplavfulaggressivenessofvounsjpuppies.Italsoindicatedthatrejectionofstrangeyounganimalsbyadultsisnotasimportantinlimitingsocializationinthedo^asitisinthesheep.
cannowbegintoclassifysomeofthebehavioralmechanisms:ehenterintotheprocessofsocialization.Therearepositivemechanismswhichtendtoproduceclosecontactduringtheinitiationofalastingrelationship.Ontheotherhand,therearenega:mechanismswhichpreventsucharelationshipfrombeingsetupwithallanimals.Undernaturalconditionsthesenegativemechanismspreventtheformationofrelationshipswithanyotherspecandusuallylimitcontactstoafewanimalsofthesamespecies.Asshowninthesheep,positiveandnegativemechanismsofbehaviorarefoundbothintheyoungindividualandinothermembersofthesocialgroup.
Individualmechc.—Thepositiveresponseofanyvoungpuppytoanewanimalorobjectinitspenistoapproachitandin-gtteitwithitsnose,perhapsalsobitingandchewingitifthisispossible.Whenthenewanimalisanotherpuppythismaydevelopintoplavfulfighting,withthepuppiespawingandchewingoneachother.Astheygrowolderwealsoobserveplavfulsexualbehaviorwithc.gandmounting.Fairlvearlvinthecriticalperiodwe
seethetendencytowardafielomimeticbehavior,withpuppiesfollowingeachotherandreactingasagroup.Socialinvestigation,
THECRITICALPERIOD131
THECRITICALPERIOD131
allelomimeticbehavior,playfulfighting,andplayfulsexualbehaviorallbringthepuppiesintocontactandkeepthemtogether.
Ingestivebehaviorisprobablynotasimportantastheaboveindrawingthepuppiestogether,sincethepuppiestendtogrowloverthepossessionoffoodevenataveryearlyage,butfooddoesenterintotherelationshipwiththemother.Theappearanceofthemotherisasignalforthepuppiestocrowdaroundher,eitherattemptingtonurseorwaitingforhertovomitfood.Thismaybeavestigeofthewolf"greetingceremony,"whichinvolvestailwagging,licking,andmuzzlebitinginastereotypedfashion(Ginsburg,1963).
Themostimportantnegativemechanismisagonisticbehavior.Theimmediateresponseofapuppytoanythingnewinitsenvironmentistorunawayorshowsomesortofstartleorfreezingbehavior.Inafreesituation,likethatinthewilddogexperiment,thecapacityforescapedevelopsrapidly,sothatbythetimeapuppyis4monthsofageitispracticallyuncatchable.Thisfearresponsecouldprobablybepartiallyovercome,butitwouldtakeweeksofpatienteffort,justasitdoeswhenoneattemptstomakecontactwithawildanimal.Alongwithescape,thepuppydevelopsthecapacityformoreseriousfighting.Ourexperimentsindicatedthatmostofthepuppieshaddevelopeddominancerelationshipsby11weeksofage,andthatthesewerewellstabilizedby15weeks.Thusthebehaviorofanolderpuptowardastrangerislikelytobeaseriousattackratherthanplayfulfighting.Thiseffectivelypreventstheformationofasocialbond.Figures5.7to5.9showthatthedevelopmentofthesebehaviorsisgradualratherthaninstantaneous.
Socialmechanisms.—Aswellasreactingtoitssocialenvironment,thepuppyisacteduponbyotheranimals.Thefirstimpactofthesecomesfromthecare-givingbehaviorofthemother.Thisismostintenseduringtheneonatalperiodwhenthepuppieslackthecapacitytoformacomplexrelationship.Duringtheperiodofearlysocializationthemotherstillapproachesthepuppies,allowsthemtonurse,cleansthemiftheyaredirty,andvomitsfoodforthem.However,herbehaviorduringthisperiodismuchlessintenseandlessensasthepuppiesgrowolder.Themotheractsasifherattachmenttothepuppieswasstrongestduringtheneonatalperiod,growingweakerthereafter.
Anotherpositivemechanismactingonthepuppyistheplayfulbehaviorofsiblings.Duringtheperiodofsocializationapuppyisconstantlyapproachedbyhislittermatesandstimulatedtothiskindofbehavioraswellasinitiatingit
hislittermatesandstimulatedtothiskindofbehavioraswellasinitiatingithimself.
Undernormalcircumstancesthereisverylittleopportunityfor
negativemechanismstoactduringearlylife.Theneonatalpuppylackstheabilitytomakecontactwithstrangemothers,andevenifitisplacedwithastrangefemale,thelatterdoesnotshowthestrongpatternofrejectionseeninsheep.Manymotherswillacceptstrangepuppieswithoutdifficulty,althoughothershavebeenknowntokillstrangepupsofferedforadoption.Whenolder,thepuppiescanapproachstrangersontheirownpower.Adultdogsusuallygrowlatstrangepuppies,althoughtheyseldomifeveractuallyhurtthem.Suchcontactsusuallyhappenlongaftertheprimarysocialrelationshipshavebeenestablishedandresultintheestablishmentofdominanceratherthanseparation.
Asecondnegativefactoristhedevelopingaggressivebehaviorofpuppies.ThiswasbroughtoutclearlyinanexperimentbyFisher(1955).Hetooklittersoffourfromfoxterriermothersandraisedtheminboxeswhichisolatedthemfromthesightofotherdogsandpeople.Twofromeachlitterwereraisedtogethersothateachhadtheconstantcompanyofanotherdog.Anotherwastakenoutatregularperiodsforcontactwithpeople.Thefourthanimalwasgivennoanimalorhumancontactsuntilitwasremovedfromthepenat16weeksofage.AtthistimeFisherattemptedtoputthelitterbacktogether.Thepuppywhichhadbeencompletelyisolatedwasstrikinglydifferentfromtheothers,standingaroundinwhatappearedtobestupefiedastonishment.Thereactionoftheotherpupswastoattackit.Whiletheisolatedpupfoughtback,itwasineffectual,anditalwayscameoutonthebottomofadominanceorder.Thismeantthatthefirstcontactoftheisolatedpuppywithotherdogswasassociatedwithbeingattackedandthreatened,effectivelypreventingthedevelopmentofapositiverelationship.Theexperienceofsuchpuppieswaslikethatofabottlelambattemptingtorejointheflock.
Fisherfinallyputfouroftheseisolatedanimalstogetherinthesamepenandfoundthattheylivedpeaceablytogether.However,theyneverformedaclosepositiverelationshipandplayedindependentlyofeachother.Iftheyhadbeenplacedinalargefield,itislikelythattheywouldhavebehavedagooddealliketheorphanlambwhichstayedawayfromtheflock.
Stillfurtherobservationsontheseisolatedpuppiesthrowmorelightontheirbehavior.Inconnectionwithanotherprojectweraisedalargenumberofbeagles
behavior.Inconnectionwithanotherprojectweraisedalargenumberofbeaglesinisolationuntil16weeksofage(Fuller,1CX)1).Whenfirstplacedwithotherpuppies,theygavenoreactionandtheotherseitherignoredthemorgrowledatthem.However,whenwetookthesesamepuppiesandbegantohandleandplaywith
THECRITICALPERIOD133
them,weelicitedthesamesortofplayfulfightingbehaviorwhichistypicalofpupsatayoungerage.Withinafewdaystheywerereactingnormallytopeople.
By16weekstheseisolatedpuppieshadlostthecapacitytoexhibitplayfulbehaviorspontaneously,althoughitcouldbeelicitedbyexternalstimulation.Bythisage,normalpuppieshaveconcentratedthisbehaviorinspecialrelationshipsandnolongerofferittostrangers.Thusanotherfactorenteringintothelimitationofthecapacityforsocializationisthelossofthecapacityforinitiatingplayfulbehaviortowardstrangers.
GENETICDIFFERENCESAFFECTINGTHESOCIALIZATIONPROCESS
Oneofourbestobjectivemeasuresofsocializationinpuppiesisthehandlingtest.Inthistestwedoallthethingswhichpeopleordinarilydotopuppies.Firstwetakethemoutsidetheirhomeroomandallowthemafewminutestobecomeaccustomedtotheholdingcage.Thenthehandlertakesthembackintothehomeroom,oneatatime.Firstheplacesthepuppyafootortwoaway,standsperfectlystill,andnotesanyreactionswhichoccurinthenext15seconds.Thenhemovesslowlyaway,turns,andsuddenlywalkstowardthepuppyfromadistanceof5or6feet.Thisisthemostfrighteningpartofthetest.Thehandlerthensquatsdownandholdsoutahandtowardthepuppy.Ifitcomesupandtouchesthehand,theexperimenterliftshishandintotheairsothatthepuppycanjumpupandtouchitifitlikes.Thenthehandlerrepeatsthesamebehaviorbutcallsthepuppyatthesametime.Hethenstrokesthepuppygentlyfiveorsixtimesandfollowsthisbypatting.Atthispoint,thehandlerpicksthepuppyupandobservesitsreactions.Thenheputsitdownagainandrepeatsthestrokingandpattingtechnique.Thefinalpartofthetestisanother30-secondperiodinwhichthehandlerstandsperfectlystillandallowsthepuppyfreeactivity.
Inrecordingdatawemarkonachecklistwhateverthepuppydoesasanimmediateresponsetoeachtypeofstimulation.Noattemptismadetoestimatetheintensityordurationoftheresponse;onlyitsoccurrenceisrecorded.Thustheresultsgiveusthenumberoftimesinwhichaparticularkindofbehaviorhas
theresultsgiveusthenumberoftimesinwhichaparticularkindofbehaviorhasbeenstimulatedor,inotherwords,thenumberoftimesthethresholdofresponsehasbeenreached.
Thedifferentpartsofthetestcanbethoughtofasstimuliofdifferentintensity.Walkingtowardtheanimalismostlikelytostimulate
BEHAVIORPATTERNS
fearfulreactions.Squattingandcallingthepuppystimulatesanapproach,whereaspattingandstrokingarelikelytobringoutplayfulrighting,atleastinolderpuppies.
Escapeandavoidancebehavior.—Averytimidpuppywillrunawaytothecorneroftheroom,crouch,andgiveahigh-pitchedvelpwhichisunmistakablyfearfulintone.Whenwemeasurethisbe-
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havior,wefindthatthebasenjisasabreedaremuchmorefearfulthantheothers
havior,wefindthatthebasenjisasabreedaremuchmorefearfulthantheothersat5weeksofagebutshowagreatchangeby7weeksinresponsetothefrequenthandlingreceivedindailytestingbetweenthosetimes.Thereaftertheamountofescapebehaviorstaysquitelevel(Figs.5.6and5.7).Theotherbreedsshowmuchlessfearat5weeksandrelativelylittlechangeatsubsequenttestingperiods.Underthestandardconditionsofrearingupto5weeksofage,thepuppiesgetlittlecontactwithpeopleexceptwhenfoodisbroughtin
THECRITICALPERIOD
135
onceeachday.Thisamountofcontactisenoughtopreventthedevelopmentoffearfulbehaviorinmostofthebreeds,butitisnotenoughforthebasenjis.
Puppiesraisedunderotherconditionsmaynotshowthesebreeddifferences.Forexample,apuppyraisedinahomefrombirthwillshowalmostnofearfulbehaviortowardpeopleat5weeks,nomatterwhatthebreed;andour3home-rearedanimalsshowedaminimumamountofescapebehaviorinthehandlingtest,theirscoresbeinglocatedverynearthelowerendofthescaleintheirrespective
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Fig.5.7.—Avoidanceandfearfulbehaviorinresponsetohandling.Basenjishavemuchhigherscoresattheoutset,andthescoresofallbreedsfallduringthenext2weeks.Atoneyearofagedogsrespondtothistestastheywouldtocatching,andthescoresofallbreedsaremarkedlyhigherexceptforcock-
ers.
breeds.Undertheseconditions,breeddifferencestendtodisappear.Breeddifferencesalsodisappearwhenpuppiesaregiventhemaximumopportunityto
differencesalsodisappearwhenpuppiesaregiventhemaximumopportunitytodevelopfearresponsesinthelargefields.Fromourexperiencesinthelaboratorywehadexpectedthatcockerspanielsandbeagleswouldbecomenaturallyfriendlydespitetheirlackofcontactwithhumanbeings.Suchwasnotthecase.Evencockersbecameaswildandfearfulasotherbreeds,theonlydifferencebeingthatwhencaughttheydidnotbitequiteashard,probablybecauseofselectioninthecockersfora"softmouth,"usefulinretrieving.
BEHAVIORPATTERNS
Ourresultsindicatedthatthebasenjishadagreatercapacityfordevelopingescapebehavior,probablybecause,asAfricanvillagedogs,suchbehaviorhadsurvivalvalue,whereasinotherbreedsthistraitisconsideredundesirablebymostdogowners.Wecanalsoconcludethatsuchfearresponsescanbegreatlymodifiedineitherdirectionbytrainingandexperience,andthatgeneticdifferencesarelessimportantateitherextreme.
Aggressivebehavior.—Breeddifferencesinaggressivebehaviorcanbemeasuredinthehandlingtest,butweneveractuallyobservedanyseriousattacksoreventhreats.Allreactionswerestrictlyplayful,andthemostextremeonesconsistedofpawingandgentlybitingtheexperimenter'shandsorclothing.AsseeninFigure5.8,
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Fig.5.8.—Agonisticbehavior(playfulfighting)inresponsetohandling.Thisscoreconsistschieflyofplayfulbitingandpawing.Notethatcockersareconsistentlylowerthanotherbreedsandchangetheleastat1yearofage.
thisbehaviorreachesitsheightabout13to15weeksofage.Weshouldremember,however,thatmostofitisnotspontaneousbutstimulatedbytheactiveapproachofthehumanhandler.Thereappeartobedefinitebreeddifferences,withwire-hairedterriersatthetopandcockerspanielsatthebottomofthescale.Theresultsgenerallyagreewiththereputationofthebreedsforfightingability,exceptthatthebeaglesshowasurprisinglyhighrank,andthisisabreedwhichshowsalmostnotendencytowardrealfighting.Itap-
THECRITICALPERIOD137
pearsthatplayfulaggressivenessandseriousaggressivenessarenotnecessarilycorrelated.
Wealsohaveconfirmingevidencefromdominancetests.Thebestindicationofaggressivenessistheexistenceof"completedominance,"inwhichonepuppyalwaystakescommandoverabonepresentedtoapair.Thewire-hairedterriersdevelopalargenumberoftheserelationshipsbefore15weeks,otherbreedsbeingslower(Fig.6.1).Byoneyearofagesheltiesandbasenjishavenearlycaughtup,butbeaglesandcockerspanielsneverdevelopalargenumberoftheserelationships.Wecanconcludethattheterriersarethemostaggressive,thebasenjisandsheltiesnext,andtheothertwobreedsmuchtheleast.Wecanalsosupposethatthesocializationofastrangepuppvtoagroupoffoxterrierswouldbepreventedbyaggressivenessbefore11weeksofage(whichcorrespondstoourobservationsoftheseverefightingthatbreaksoutinthisbreedasearlyas7weeks),andthatthesocializationofastrangertoabasenjigroupwouldbeinhibitedsomewhatlater,perhapsby15weeks.Inthemorepeacefulbreeds,thisfactormightbequiteunimportant.
Socialinvestigationandattraction.—Oneoftheprimaryreactionsinvolvedinsocializationisthepuppy'stendencytocometowardahandlerandinvestigatehim,usuallywaggingitstailatthesametime.Thiskindofbehavioroftenappearsinthehandlingtestandreachesitsheightabout7weeksofage,stayingatafairlyconstantlevelthereafter(Fig.5.9).Suchactivitymaybedividedintoinitialattractionandsubsequentinvestigatorybehavior.Consideringat-trationalone,thebasenjisappeartobelessattractedtopeopleatallages(Fig.5.10).Sheltiesarelowatcertainages,andcockersareconsistentlyhigh.
Asomewhatdifferentpictureispresentedbythesocialinvestigativebehaviorshownafterthepuppiesreachtheexperimenterandbeginnosinghishandsandclothes(Fig.5.9).Thebeaglesexhibitedmoreinvestigativebehaviorthanother
clothes(Fig.5.9).Thebeaglesexhibitedmoreinvestigativebehaviorthanotherbreeds,althoughcockerspanielswereslightlyhigherat5weeks,justastheywereintheattractionscore.
Thedevelopmentoftailwagging.—Thepatternofrapid,horizontaltailwaggingisoneofthemostcommonlynoticedbehaviorsindomesticdogs.Itbeginsataveryearlyageandcontinuesaslongasthedoglives,appearingmostofteninsituationsinwhichthedogisfriendlyandsubmissive.Ithasnofunctionotherthanasocialone,andinalltheserespectsismuchlikethehumansmile.
Itsdevelopmentcanbechartedfromtherecordsofourdailyob-
BEHAVIORPATTERNS
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FlG.5.10.—Attractionandfollowinginresponsetohandling.Basenjisareconsistentlylowinthisscorecomparedtootherbreeds,butsheltiesshowthegreatestdecreaseat1year.
THECRITICALPERIOD
139
servations.Aresearchassistantwatchedeachlitterfor10minutesadayandrecordedeverythingthatthepuppiesdid,latercheckingeachitemonastandardlist.Inthiswaywehavearecordofthefirstdayonwhicheachpuppvwasseentowagitstail.
Tailwaggingfirstappearedat17daysofage(Table5.4a).By30daysone-halfofalldiepurebredpuppieshadbeenseenwaggingtheirtails.Thisbehaviorthusbeginsearlyintheperiodofsocializationandrapidlyincreasesinfrequency.
TABLE5.4aDevelopmentofTailWagging
Whenwecomparethedifferentbreedsweseecertainobviousdifferences.By18daysofageone-fourthofthecockerspanielswereseenwaggingtheirtails,whereasitwasnotuntil30daysofagethatbasenjiswereobserveddoingthis.Atthislatterage83percentofthecockershadbeenseentailwagging.Therestofthebreedswereverysimilartoeachother,withabout50percenttailwaggingby30daysofage(Table5Ab).
TABLE5.46DevelopmentofTailWagging:Occurrenceat30DaysorEarlier
Thedifferencesbetweencockersandbasenjisarehighlysignificant,andbothbreedsalsodepartwidelyfromtheaverageofallbreeds.Wethereforehaveanimportantbreeddifferenceinthede-
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velopmentofaformofsocialbehaviorcloselyconnectedwiththeprocessofsocialization.However,thedifferencebetweenbasenjisandco:orobablyoneofthresholdsofstimulationratherthan
rateofdevelopment,sincethereisalmostnodifferenceintailwag-_I.enbothbreedsarestronglystimulated,astheyarewhentheyarebeing_entheirweeklyweighings.Cockersapparendywagtheirtailsinresponsetoaslightstimulus,whilebasenjisrequirestrrr.ge:stu.^izizz
Theseresultsshowthatgeneticfactorshaveimportanteffectsontheprocessofsocialization.Heredityaffectsboththeindividualreactionswhichlimitsocializationfromwithin,suchasfearre-srrzjri::~er^Srn-'ii.ir.£-:;e~:::■:::::;lir/_i::r.-sziilizi::::fromwithout,suchastheaggressivenessofthefoxterriers.Inaddition,geneticfactorscanaffectthepositivebehaviorofapproach:.~i5;::il:r.Ti:;::.:::::
Oi-.e-::55:":"r::::'::i:iif:':.:■.-{z.esei:E^:z:.:~?ire:ie:e.;i:::asingletraitoffearfulnesswhichcould,ofcourse,affectalltheothers.This,hwillnotexplaintheresults.Thebasenjisare
themostfearfulatfirstandshowtheleastattraction.HowetheyarenotthelowestinsocialinvestigationandareactuallysecondhighestinplayfulaggressrveETireobviouslydealingherewithanumberofseparatetraitswithdifferentgeneticbases.
Thisseparationoftraitsalsogivesusaduetowardunderstandingtheorganizationofbehavior.Ourusualassumptionisthatfearfulnessandaggressivenessaretheoppositeendsofasinglebeh.ioralscale.Thisisnotthecasewithdogs.Abreedmayhavethecapacitytobecomebothhighlyfearfulandhighlyaggrein
thebasenji;orhighlyaggrebatnotfearful,asinthefoxterr
orshowingneitherextreme,asinourotherthreebreedlso
seethatevenaggressivenessisnotaunitarytrait,forabreedlikethebeaglescanshowbothahighdegreeofplayfulaggressivenessandaverylowamountofseriousaggressiven-
Ing:hebehaviorofdomesticdogsshowstheresultofselec-
tionagainstthedevelopmentoftheescapeandavoidancebehaviornormallyfoundinwolves.Thismeansthatthedevelopmentofoneofthefactorslimitingtheperiodofsocializationhasbeendelayed,sothatsuccessfulsocializationcanbeachievedatamuchlaterij>.achievedgoodsocializationwithawolfpuppybdbeforetheeyesopened.Crisler(1958)apparendywassomewhatlesssuccessfulwithpuppiestakenataslightlylaterage,althoughthesituationwasnotstrictlycomparable,inthatsheraisedapairratherthanasingleindividual
THECRITICALPERIOD
Ginsburg(1963)hasrecentlvdemonstratedthatwolvescapturedasadultscanbesuccessfullysocialized.Theprocesstakesmanydaysandthewolvesmustbekeptinapensotheycannotescape.Theexperimenterentersthecageandmaintainsapassiveroleuntilthewolfmakesitsfirstpositiveadvance.Atthispointhemustneitherthreatennorwithdrawfromthewolf,butmustrespondappropriatelyandpositively.Ifthereissuccessfulmutualadjustment,thewolfwillthereafteracceptnotonlytheexperimenterbutotherhumanbeingsaswell.Suchresultsindicatethatthecapacityforformingnewsocialrelationshipsisnotlostinanadultbutisordinarilypreventedfromfunctioningbyescapeandfearreactions.
Therehasbeenselectionfordecreasedaggressivenesswithinmanydogbreedsinordertomakethemeasiertohandle.Inthecaseoftheterriers,however,selectionforaggressivenesshasproceededintheoppositedirection.Thisdoesnotseemtohavelimitedthecapacityforsocialization,sinceoneofthepositivemechanismsofsocializationisplayfulfighting,butrathertohavelimitedthecapacityforgroupliving.Thereisnoindicationthatthetendencytowardsocialinvestigationhasbeenprolongedinanybreed,exceptbytheeliminationoffearfulbehaviorwhichinterfereswithit.Aslongastheyarenotafraid,membersofallbreedsactliketypicalfriendlypuppiesuntilatleast15weeksofage.Somebreedsshowmoreplayfulbehaviorthanothers,butthereisnotrueprolongationofanimmaturesocialstate.
THECRITICALPERIODINOTHERSPECIES
THECRITICALPERIODINOTHERSPECIES
Thefundamentaltechniquefortestingtheexistenceoftheprocessofsocializationistofosteravounganimalonanotherspecies.Withhigheranimalsitisofteneasiesttodothisbyhandrearing,butthelivingrequirementsofotherssuchasthesocialinsectsmaybesodifficulttoduplicatethattheycanonlybefosteredonsimilaranimals.Ifthefosteredanimaltransfersitssocialrelationshipstothenewspecies,wecanconcludethatsocializationhastakenplace.Thenextstepistoattemptthisatvaryingagesinordertotestfortheexistenceofacriticalperiodfortheprocess.Suchexperimentshavesofarbeendonewithonlyalimitednumberofspecies,butresultsaregenerallyconsistent.
Insects.—Antcoloniesusuallyattackstrangespeciesandoftengivethesamereactiontostrangemembersofthesamespecies.Ifyoungantsareexperimentallyplacedinastrangecolonytheybecomeapermanentpartofit,beingcaredforbytheresidentworkers.
Thisregularlytakesplaceintheslave-makingants,whichraidcoloniesofotherspeciesandbringbackyoung.Thesecapturedindividualsthengrowupandtakecareoftheyoungoftheirmasters.Noattempthasbeenmadetofindacriticalperiod,butitmustendsoonaftertheadultsemergefromtheirpupalcases,ifnotbefore.
Honeybeesalsorecognizemembersoftheirowncolony.Aswithants,recognitionisbasedonscentandhasbeenshowntobeanacquiredratherthananinheritedreaction.Furthermore,beesoftwocoloniescanbebroughttogetherwithoutfightingprovidedtheyhavebeenfedonidenticaldietsforasufficientlengthoftime(Ribbands,1953).Thereisnodirectevidenceastowhenthescentofthewholehomecolonyislearned,butitmustbeearlyinlifebecausetheworkerstendtotakeupguarddutiesbeforetheybecomeforagers.Beforebecomingguards,theyoungbeesworkaroundthehive,cleaningthecells,sothatthereisampleopportunitytolearnthescentofthehive.Thus,socializationdoestakeplaceamongsocialinsects,andprobablyduringashortperiodearlyinlife.
Birds.—Thegreatimportanceoftheprocessofprimarysocializationwasfirstrecognizedinbirds(Lorenz,1935).ThenaturalistHeinrothhadattempted,withcharacteristicGermanthoroughness,tohandrearallofthecommonEuropeanspeciesofbirdsinordertolearnmoreabouttheirdevelopmentandbehavior.Someoftheresultswerespectacularexamplesoftransferenceofsocialrelationshipsfromonespeciestoanother.Inonecase,althoughtheadultbird
relationshipsfromonespeciestoanother.Inonecase,althoughtheadultbirdmatedwithamemberofitsownkind,itwasattractedawaybyitsfosterparentwheneverheappeared.KonradLorenzextendedtheseobservationsandmademorespecificstudiesoftwospecies,thegraylaggooseandthejackdaw.Geeseareprecocious,beingabletowalkandswimafewhoursafterhatching,whereasjackdaws,whicharerelatedtothecrowfamily,arehatchedinanimmaturestate.Lorenzfoundthatnewlyhatchedgeeseformedtheirsocialrelationshipswithinthefirstfewhours,whereasjackdawsdidthismoregraduallyatalaterstageofdevelopment.Oncetheserelationshipswereformed,itwasdifficultifnotimpossibletorestorethenaturalrelationships.LorenzcalledtheprocessofformingthisprimarysocialrelationshipPriigung,whichhasbeentranslatedas"imprinting."Thewordalsomeansimpress,andthismighthavebeenabettertranslation.Atanyrate,theyoungbirdsseemtobedeeply"impressed"or"imprinted"byalimitedexperienceearlyinlife.
TheFundamentalimportanceoftheseresultsinrelationtotheoriesoipsychiatryregardingearlyexperiencewassoonrecognized.Fa-
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bricius(1951),Collias(1952),Hess(1959),andothersfollowedupLorenz'workwithdetailedanalyticalstudies.Inprecociousbirdslikeducksorchickens,thereisindeedacriticalperiod.Itiseasiesttodemonstrateimprintinginthechickatabout13to14hoursafterhatching,anddifficultifnotimpossiblebv30hours.Theprimarybehavioralmechanismswhichlimittheperiodare,atthebeginning,thedevelopmentoftheabilitytomovetowardastrangeobjectorpersonand,attheend,thedevelopmentofafearresponsewhichkeepsthebirdsfromapproachingstrangeobjects.Stillothermechanismsareinvolved;asHess(1957)hasshown,aducklingbecomesmorefirmlvimprintedifithastomakeanefforttofollowamodel.
Comparablestudieshavenotbeenmadewiththemoreslowlydevelopingbirds,exceptfortheveryexcellentdescriptivestudiesofMargaretNiceonsongsparrows(1943).Itisevidentthatsuchbirdsaremuchmoreliketheslowlvdevelopingmammalsthanarechicksandducks,andthatcomparableperiodsofdevelopmentexist(Scott,1962b).
Mammals.—Manyspeciesofmammalsotherthandogsandwolveshavebeenexperimentallyhandreared,andmostoftheseshowaspectacularattachmenttotheirhumanfosterparents.Chimpanzees,forexample,readilybecomemembersofhumanfamilieswhenraisedinhomes(Kellogg&Kellogg,1933;Hayes,
ofhumanfamilieswhenraisedinhomes(Kellogg&Kellogg,1933;Hayes,1951).Therehave,however,beenalmostnodetailedanalyticalstudiesofthecriticalperiodforsocializationexceptindogs,sheep,andguineapigs(Gray,1958).Theselasttwospeciesarehighlyprecociousandshowashortcriticalperiodveryearlyindevelopment.Thereareindicationsofacriticalperiodinrhesusmonkeysduringwhichcontactwithotheryounganimalsofthesamespeciesisnecessaryforthedevelopmentofbothsexualandmaternalbehavior(Harlowetah,1963).
Mammalsingeneraldifferagreatdealintheirspeedofdevelopment,somebeingborninarelativelymaturestate,andothersbeinghighlyimmature.Theremaybeagreatdealofvariationevenincloselyrelatedanimals.Forexample,rhesusmonkeysshowrapidandprecociousdevelopment,chimpanzeesandothergreatapesaremuchslower,andhumaninfantsareslowestofall.
Insummary,wecanstatethatallhighlysocialanimalswhichhavebeensofarstudiedshowacriticalperiodforsocializationearlyindevelopment.Themoreprecocioustheanimal,theshorterandearliertheperiodislikelytobe.Thebehavioralmechanismswhichlimittheperioddifferfromspeciestospeciesandcannotbepredictedinadvance.However,adevelopingfearreactionisacommonmechanism.
Itwouldbesurprisingifhumanbeingsdidnotshowatleastthevestigesofasimilarcriticalperiod.Thisconclusionwillreceivegreatersupportifthegeneralityofthephenomenonofcriticalperiodscanbeextendedbystudiesonawidervarietyofvertebrateandinvertebratespecies.
BASICNATUREOFTHEPRIMARYSOCIALIZATIONPROCESS
Wehavesofartalkedaboutthebehavioralmechanismswhichfacilitateorlimitsocializationbutlittleabouttheprocessitself.WhenLorenz(1935)firstwroteabouttheimportanceofimprinting,hestatedthattheprocesswasquitedifferentfromthatofconditioning,inthatitoccurredveryrapidlyandtheresultsseemedtobepermanent.Psychologistswerequicktopointoutthatconditioningcanalsooccurvervrapidlv,"one-triallearning"beingcommonplaceinhigheranimals.Furthermore,Pavlovhademphasizedthelongpersistenceofconditionedreflexes.Evenwhenareflexhadbeenextinguishedbynon-reinforcement,italwaysreturnedspontaneouslyafteranextendedperiodofrest.
Anattractiveandsimplealternatetheorvwasthattheemotionalbondbetweenmotherandoffspringwasproducedbyfeeding.Achildassociateditsmother
motherandoffspringwasproducedbyfeeding.Achildassociateditsmotherwiththepleasureofeating,andthisformedthebasisoftheattachmentwhichwaslatermoregeneralized.ThisideawasimplicitinFreud'sdescriptionoftheoralstageinhumandevelopmentandhassincebeenelaboratedasthetheoryofacquireddrives(MillerandDollard,1941).
Brodbeck(19.54)wasthefirsttotesttheseideasonthedog.Heraisedalitterofcockerspanielsandalitterofbeagles,takingthemawayfromthemothersat3weeksofage.Hefedhalfofthembyhand,andfedtheotherhalfbyasvstemofropesandpulleyssothatthepuppiesneversawwhofedthem.Hethengavebothgroupsthesameopportunitvtohavedirectcontactwithhimandlatertestedtheirreactionsashesatquietlyinthesameroom.Bothsetsofpuppieswerehighlyreactivetowardhim,andthoseofonegroupstayedwithhimjustascloselyasthosefromtheother.Wecancon-eludethatfeedingisnotanecessarypartofthedevelopmentofthesocialbond.Stanley|1962")andFeiderlaterdidasimilarexperimentwithtwolittersofbeagle-terrierhybridpuppies.Thehand-fedpuppieswouldvocalizemoreatthesightoftheexperimenter,butthiswastheonlyimportantdifferencebetweenthetwo.
ElliotandKing(1960)didtheoppositesortofexperimentin
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thattheyhandfedagroupofpuppiesbutdidverylittleelsewiththem.Halfofthepuppiesweregivenalltheycouldeatandtheotherhalfwereunderfed.Whenthesepuppiesweregivenahandlingtest,theunderfedgroupshowedmorepositiveresponsestothehandlers,butbothgroupsshowedmoretimiditythanotherpuppieswhichhadbeenraisedintheregular"schoolfordogs"programinwhichtheyreceivedregularhandling.Fromthisexperimentwecanconcludethatfeedingbyitselfdoesnotproduceahighlysocializedanimal.
StanleyandElliot(1962)conductedaseriesofexperimentsinwhichtheypainstakinglyattemptedtodiscoverthefactorswhichmakeahumanbeingattractivetoyoungpuppies.Thebasicexperimentisamodificationofthepassive-handlertest.Beginningatabout6weeksofagethepuppiesareweaned,neverbeingfedbytheexperimenters.Theyarethentakenoneatatimetoadifferentroom,placedinasmallbox,andallowedtoruntowardanexperimenter.Thisisrepeateddailyforseveralweeks.Thepuppiesbecomehighlysocializedtohumanbeings,evenifthepersontowardwhomtheyrundoesnothingmorethansitpassively.Basenjipuppiesappeartobemoreattractedbyapersonwhoiscompletelypassivethanonewhoattemptstopet
attractedbyapersonwhoiscompletelypassivethanonewhoattemptstopetthem.Allpuppiesbecomecloselyattachedtohumanbeingswithnomorethanthedailycontactinvolvedintheexperiment.
Fisher(1955),inhisexperimentwithisolatedfoxterrierpuppies,treatedonegroupbypunishingthemwhenevertheymadeanypositiveapproach.Thesepuppieswererearedinspecialboxesfrom3weeksofageandwereneverfedbyhand.Aslongashecontinuedtopunishthem,thefoxterriersstayedaway;butoncehestoppedtheyalmostimmediatelyovercametheirfearandcametowardhim.Infact,theypaidmuchmoreattentiontohimthanacomparablegroupofpuppieswhichhehadtreatedwithuniformkindness.Theexperimentshowsnotonlythatfoodrewardsareunnecessaryingettingpuppiestobecomeattachedtopeople,butthattheywillformanattachmentinspiteofconsiderablepunishment.Wemustrememberthatthesewerefoxterrierpuppieswhichhavebeenselectedtotakeagooddealofpunishmentinfighting,andtheresultsmighthavebeendifferentwithamoresensitivebreed.
Meanwhile,Harlow(1958)hadbeenperforminganinterestingexperimentwithrhesusmonkeys.Thesearequiteprecociousanimalsasprimatesgo,andnormallyclingtotheirmothersimmediatelyafterbirthandcontinuetobecarriedbytheirmothersforseveralmonths.Harlowtookthebabymonkeysawayfromtheirmothers
146BEHAVIORPATTERNS
atbirthandofferedthemachoiceoftwoimitationmothers.Onewasdeliberatelyintendedtobeuncomfortable,beingmadeofwiremeshhardwarecloth,andtheotherwascoveredwithsoftterrycloth.Anursingbottlewasinsertedinthehardwareclothmother,andtheinfantgotallitsfoodinthisway.Harlowfoundthatthebabymonkeysspentalltheirtimewiththecomfortablemother,onlygoingbrieflytotheotherinordertonurse.Thebabymonkeysgaveeveryevidenceofbeingprofoundlyattachedtotheterry-clothmother,andHarlowconcludedthatthetheorythattheattachmentoftheinfanttothemotherwasanacquireddrivebasedonfoodrewardscouldbeabandoned.Hewasinclinedtoconsider"contact-comfort"astheessentialelementintheprocess.
IgelandCalvin(1960)wonderedwhatwouldhavehappenedifthemonkeyscouldhavechosenbetweentwocomfortablemothers,oneofwhichproducedmilkandonewhichdidnot.Nothavingmonkeysavailable,theydidacorrespondingexperimentwithyoungpuppiesandfoundthat,ifthepuppies
correspondingexperimentwithyoungpuppiesandfoundthat,ifthepuppieswereequallycomfortable,theyspentmoretimewiththemotherthatproducedmilk.Inshort,foodrewardswillstillaffectthebehaviorofayounganimal,evenifthesearenottheprimaryelementintheprocessofsocialization.
Meanwhile,otherpsychologistshadbeenexperimentingwiththeimprintingofbabychicksonvarioussortsofmodels.Atfirstitwasthoughtthatthemodelmustmovetobeeffective,butlaterJames(1959)showedthatchicksbecameimprintedonamodelwhichwasmerelyexposedtoflickeringlight.Finally,Gray(1960)didanexperimentinwhichbabychickswereexposedtoamotionlessmodelwhichtheycouldseebutnottouch,andtheirsubsequentbehaviorindicatedthattheyhadbecomeimprinted.Thebabychicksthereforebecameattachedtoanobjectwhichneitherrewardednoractivelystimulatedtheminanyway.
Takentogether,theevidencefromdiesedifferentspeciesofmammalsandbirdsleadstotheconclusionthattheprocessofforminganemotionalattachmenttomembersoftheparentspeciesislargelyindependentofoutsidecircumstances.Whetherrewarded,punished,ortreatedindifferently,theyounganimaloftheproperageproceedstoformanemotionalattachmenttowhateverispresentintheenvironmentatthattime.Theessentialmechanismappearstobeaninternalprocessactingontheexternalenvironment.Inthiswayitisindeedquitedifferentfromconditioning,whichisdirectlydependentonoutsidecircumstances.
Thishypothesisfitsmuchoftheexperimentalandobservational
THECRITICALPERIOD147
evidence.Tostateitmoreclearly:ayounganimalautomaticallybecomesattachedtoindividualsandobjectswithwhichitcomesintocontactduringthecriticalperiod.Thecapacitytodothisneednotbelostatlaterages,buttheprocesscanbesloweddownorpreventedbythedevelopmentofinterferingbehavior,particularlyfearresponses.Likewise,theprocesscanbepreventedatlateragesbythedeclineofpositivebehaviorwhichnormallybringstheyounganimalintocontactwithothers.
HUMANAPPLICATIONS
Wehavereasonedthatthereisahighprobabilitythatacriticalperiodforprimarysocializationexistsinhumandevelopment.However,thisconclusioncanbeverifiedonlybydirectobservationandexperimentonhumaninfants.One
canbeverifiedonlybydirectobservationandexperimentonhumaninfants.Oneresultisthefindingthat,aswepointedoutinthelastchaper,thesequenceofdevelopmentalprocessesinmanandthedogoccurinasomewhatdifferentorder(Table4.6).Theperiodofprimarysocializationinhumaninfantsextendsfromapproximately6weeksto6months,thusprecedingtheperiodoftransitiontotheadultmethodsoffeedingandlocomotionratherthanfollowingit.Thismeansthatthebabycanformitsprimaryrelationshipsonlywiththosepersonswhotakecareofit,asitisunabletomakecontactsonitsown;anditalsomeansthatthefirstandprobablythedeepestrelationshipwillbeformedwiththemotherratherthanwiththefatherorsiblings.Alltheseconclusionsarebasedondescriptiveevidence.Experimentalworkofthekinddonewithloweranimalsisdifficultifnotimpossiblewithbabies,andallwehavetogobyaretheresultsofvariousaccidentsandvariationsinhumanbehavior(Gray,1958).
Therehavebeenafewisolatedcasesofchildrenwhohavebeenconfinedbyparentsorcaretakersinsocialisolationcomparabletothatofapuppyraisedinasmallbox.ThebestknownofthesecasesisthatofKasparHauser,ayouthwhoturnedupinNuremberg,Germanyintheyear1828(SinghandZingg,1939).Noonewasabletoverifywhathisactualpreviousexperiencehadbeen,butheapparentlyhadbeengivenanelementaryeducationwhilekeptincloseconfinementfrombabyhooduntilnearlyanadult.Sincethiswasbeforethedevelopmentofthescienceofpsychology,thereportsconcerninghimweremadebyajudgeratherthanatrainedscientist.Hedescribedtheboyasgoodnaturedandsociallyresponsivebutcompletelynaiveabouttheoutsideworld.Therewasnoevidence
148BEHAVIORPATTERNS
ofunusualfearfulness.Forwhatitisworth,thedescriptionofKasparHauser'sbehaviorsoundssomewhatmorenormalthanthatofpuppiesrearedinisolation.
Wolfchildren.—Deliberatelyfosteringahumanbabyonanotherspeciesiscompletelyimpossiblefromahumanitarianviewpoint,butthereareoccasionalnewsreportsofthisoccurringbyaccident.Thesesomewhatlegendaryaccountsusuallyconcern"wolfchildren"inIndia,andhavebeenfictionalizedbvKiplinginhisjunglebooks,butonesuchreporthasamorescientificbasis.Inthe1920'saReverendSinghwassaidtohavefoundtwo"wolfchildren"inIndiaandbroughtthemtoanorphanage,whereheattemptedtoeducatethem(SinghandZingg,1939).Accordingtohisaccount,hefoundthetwochildrenlivinginawolfdenfromwhichwolvesalsoemerged.This,ofcourse,wouldnotprovethat
wolfdenfromwhichwolvesalsoemerged.This,ofcourse,wouldnotprovethatthechildrenhadbeenrearedbywolvesbutsimplythatwolvesandchildrenwerefoundtogether.OgburnandBose(1959)latermadeanintensiveefforttocheckuponthisstorybutwereabletoverifyverylittleexceptthattherehadactuallybeenaReverendSinghandthattherewerenewspaperstoriesaboutwolfchildrenatthattime.Theaccountsoflivingpersonswhorememberedtheincidentwerehighlycontradictory.
Apartfromthedubiousnatureoftheevidence,thechancesthatahumanbabycouldactuallyberearedbvwolvesaresosmallthatwecandiscountsuchreportsasfantasvunlesssometrainedobserveractuallyseesababybeingmotheredbyawolf.Wolves,likedogs,nursetheiroffspringforapproximately7weeks,afterwhichmilkisnolongeravailable.Asearlyas3weeks,thevbeginfeedingtheiroffspringonvomitedfoodandmeatwhichisoftenpartiallyspoiled,particularlyinwarmclimates.Eveninaprimitivehumansociety,ababyhastobenursedfortwoyearsorsoinordertosurvive,andthereisusuallyahighinfantmortalityratefromintestinalinfections.Itisconceivablethatawolfmightadoptahumanbabybutnotthatthebabycouldsurvivewithonlvwolfcare.
Itissignificantthatthesereportsofwolfchildrencomefromareasofgreatpovertywherechildneglectanddesertionarecommon.Itisquitepossiblethatchildreninsuchareashavebeenabandonedbytheirparentsconsiderablylaterthanearlyinfancyandhavebeenabletosurviveand"runwild."JudgingfromGinsburg'ssuccessinsocializingadultwolves,itwouldevenbepossibleforsuchachildtobeacceptedandtoleratedbywolves.\sscientificevidence,however,thereportsconcerning"wolfchildren"havelittlevaluebecauseitisimpossibletocheekwhatactuallyhappenedtotheml>eforetheywerelouncl.Forwhatitisworth,suchchildrenarereportedtobe
THECRITICALPERIOD149
wildandfearful,likethepuppiesraisedentirelyapartfromhumanbeings.
Adoption.—Alessdrastictvpeoffosteringfrequentlytakesplaceinthehumanpracticeofadoption.Foronereasonoranotherbabiesmaybetakenfromtheirnaturalparentsandeitherraisedinorphanagesoradoptedbyotherindividuals.Fromourknowledgeofhumandevelopment,wewouldexpectthatababycouldbetransferredfromoneparenttoanotherduringthefirsttwomonthswithoutthebaby'snoticingwhathadbeendoneaslongasmaternalcarewassufficient.From2to5monthsofage,wewouldexpectthatthebabywouldbeemotionallydisturbedbythechangebutwouldmakearelativelyeasyadjustmenttothenew
disturbedbythechangebutwouldmakearelativelyeasyadjustmenttothenewparent,justaspuppiesseemtododuringtheperiodofprimarysocialization.Beyondthisagethebabywouldhaveformeddefiniterelationshipswhichwouldbebrokenoffwithconsiderableemotionaldisturbance,makingadoptionmoredifficult,bothbecausethebabywouldnotreadilyformnewrelationshipswithstrangersandbecausethefosterparentswouldbeupsetbytheemotionalbehayiorofthechild.
Theactualstudiesofadoptedchildrenarenotimpressiyeasscientificexperiments,butpeoplewhoworkwithchildrenagreeontwothings.Oneisthatchildrenadoptedbefore6monthsofagegetalongbetterthanothers,andtheotheristhatprolongedexperienceinanorphanageproducesbadresultsonmanychildren.Anotherconclusionisthattheresultsarenotalwaysbad,sincemanychildrenturnoutwellinspiteoftheseearlycircumstances.Thisyariation,ofcourse,couldbecausedbydifferencesingeneticconstitutionoftheindiyidualsinvolved.Somechildrenmaybemoreresistanttoemotionaldistress.
Anotherkindof"accidentalexperiment"isproducedbyhospitalizationofveryyoungchildren.Herethebabymaybetakenawayfromitsparentssuddenlyandputwithstrangersfordaysorweeks.Inaddition,itmaybesufferingfromillnessandphysicalpaininthesestrangesurroundings.Bowlby(1951)andothershavefoundthatsuchchildrenshowevervevidenceofsevereemotionaldisturbanceatthetime,despiteeffortsbvnursestokeepthemreasonablycomfortableandhappv.Bowlbvalsofound,workingintheotherdirection,thatmaladjustedchildrenfrequentlyhadsufferedsuchdrasticearlvexperiences.Heconcludedthatsuchchildrenweresometimesunabletodevelopdeepemotionalrelationshipsinlaterlife.Iftrue,thiswouldmeanthattheprocessofsocializationhadbeendefinitelydisturbed.
Lookingattheseexperiencesinanotherway,wecanseethatfor
ayoungsocialmammallivingundernaturalconditions,asituationinwhichitisseparatedfromitsparentsinstrangesurroundingsisacutelydangerous.Suchananimalwouldbeunlikelytosurviveunlessitgaveastrongemotionalreactionwhichmightattracttheattentionofitsparents.Youngpuppiescertainlyreactinthisway,anditmayalsobetrueofbabies.Whyaprolongedseparationandtheresultingemotionaldisturbancewoulddisturbtherelationshipbetweenmotherandchildisamatterofconjecture,butwecansupposethatababymightconcludeinaprimitivewaythattheparentsthemselveswerethecauseofhisemotionaldiscomfortandanticipatethattheymightabandonhimagainandproducethesamepainfulfeeling.
producethesamepainfulfeeling.
Theseare,ofcourse,humanphenomenaintowhichsubjectivereactionsalwaysenter.Ouranimalexperimentsdogivesupporttocurrentideasregardingthedesirabilityofearlyadoptionandthekeepingofchildreninfamiliesratherthaninorphanages.Lateadoptionis,ofcourse,stilltheonlypracticalcourseofactioninmanycases,butitmustbedonewithagreatdealofcareandpatience,includingtherealizationthattheformationofanemotionalattachmentbytheolderchildwillbeamuchslowerandlessautomaticresponsethaninayounginfant.Byaddingtoourunderstandingofthebehavioralmechanisminvolvedinprimarysocializationandadoption,theanimalexperimentsalsosuggestwaysinwhichpsychologicaldamagemaybeavoidedwhenchildrenareplacedinsuchdifficultsituationsbyaccidentornecessity.
THEDEVELOPMENTOFSOCIALRELATIONSHIPS
INTRODUCTION
Asocialrelationshipmaybedefinedasregularandpredictablebehavioroccurringbetweentwoormoreindividuals.Thisdefinitionappliesnotonlytorelationshipsinanimalsocietiesbuttothoseinhumansocietiesaswell,whererelationshipsystemsformafundamentaltypeofsocialorganization.Inhumansocietiesarelationshipbetweentworelativessuchasfatherandsonconsistsofboththeobservedbehaviorbetweenthemandasystemofverbalruleswhichmayormaynotcorrespondtotheactualbehavior.Inananimalsocietytheverbalelementis,ofcourse,missing.
Psychologicaloriginofarelationship.—Whentwopuppiesmeetforthefirsttime,eachrepresentsaproblemtotheother.Ifonepuppyinitiatesplayfulfighting,willtheotherrespondinkind,orbypassivesubmission,orbyrunningaway?Atthefirstmeetingthepuppiesmaytryoutavarietyofsolutionstotheproblem.Withsubsequentexperience,theyworkoutsomesortofsolution,oftenonabasisoftrialanderror,andbegintoreduceittoahabit,omittingmuchoftheoriginalbehavior.Thusasocialrelationshipbeginsasaproblemandendsasasimplehabit.
Fromwhatweknowaboutlearningandhabitformation,wecanpredictthathabitsarenotinvariable;infact,thereisanormaltendencyforananimaltovaryitsbehavioreveninwhatappeartobeidenticalsituations.Thisis,ofcourse,anessentialpartoftheprocessoflearning,forwithoutitnoimprovementofadaptationwouldbepossible.Theamountofvariationisreducedinfrequently
adaptationwouldbepossible.Theamountofvariationisreducedinfrequentlyrepeatedbehaviorbutneverentirelyeliminated.Wealsoknowthathabits
151
152BEHAVIORPATTERNS
arenotunbreakable.Ahabitwhichonceledtosuccessfuladjustment,butnolongerdoesso,mayberepeatedforashortwhilebutsoondiesout.Thereforeasocialrelationshipisneitherinvariable,norincapableofchange.However,socialrelationshipsundertheproperconditionscanbecomeextremelystableandinvariable.
Thedifferentiationofbehavior.—Whenweapplytheideaofdevelopmenttosocialrelationships,wecanseethattherearetwokindsofdevelopment.Oneistherapidpsychologicaldevelopmentofarelationshipwhichmayoccurwithinafewdaysorevenhours,andtheotheristhelong-termbiologicaldevelopmentofarelationshipbasedontheslowerprocessesofgrowthandbiologicalchange.Thesetwokindsofdevelopmentmaybothbedescribedintermsofdifferentiationofbehavior.Inarelationshipbasedonplayfulfighting,twopuppiesatfirstshowmuchthesamekindofbehavior.Attheendoftherelationship,onemayalwaysattackandtheotheronealwayssubmit;theirbehaviorisnowdifferentiatedonapsychologicalbasis,andtheprocessoflearningmayresultinaveryslightoraveryhighdegreeofdifferentiation.
Thispsychologicalprocessisalsoaffectedbytheothertypeofdifferentiationofbehavior.Anewbornpuppyhasrelativelyfewalternatebehaviorpatterns.Asitgrowsolder,thecapacitiesforawidervarietyofbehaviorpatternsappear.Whereasatfirstthepuppycouldonlyyelpinresponsetodiscomfort,itcannowrunawayorattackthesourceofdiscomfortaswellasvocalizing.Thusthepuppydevelopsthroughbiologicalprocessesthecapabilitytodifferentiateitsbehaviorindifferentsituations.
Morethanthis,geneticfactorsdifferentiatethebehaviorofoneindividualfromanother.Insocialmammalstherearebasicdifferencesinbehavioralcapacitiesbetweenmalesandfemalesandbetweenadultsandyoung.Withineachofthesemaintypes,individualsmaybeaffectedbydifferentialheredityandsoshowdifferentkindsofbehavior.Itistheimportanceofthelatterphenomenonwithwhichthischapterismainlyconcerned.
Fundamentalclassificationofsocialrelationships,—Inhisfieldstudiesof
Fundamentalclassificationofsocialrelationships,—Inhisfieldstudiesofprimates,Carpenter(1934)developedaclassificationofobservedrelationships.Withthreetypesofindividuals—males,females,andyoung—itispossibletohavethreerelationshipsbetweendifferentkindsofindividuals(male-female,male-young,andfemale-young)andthreemorebetweenthesamekindsofindividuals(male-male,female-female,andyoung-young).Inthecaseofthedog,whichregularlyFormsrelationshipswithhumanbeings,sixbasickindsofindividualsarcinvolved.Thismeansthattherearefifteenrelation-
SOCIALRELATIONSHIPS
153
shipspossiblebetweendifferentkindsofindividualsandsixbetweenliketypes,makingatotaloftwenty-one(seeTable6.1).
TABLE6.1
SocialRelationships*ofDogandMan
•Thereare21possiblerelationships,usingallcombinationsofageandsex:9dog-humanrelationships(loweJleftcorneroftable)and6eachofdog-dogandhuman-humancombinations(upperleftandlowerrightcorners).
Inourexperiment,therelationshipsformedwerelimitedbythesystemofrearing.Amongdogs,onlytworelationshipswerestudiedseriously,thosebetweenmotherandyoungandthosebetweenyoungbelongingtothesamelitter.Thedog-humanrelationshipswerelikewiselimited.Sinceourexperimenterswerealladults,thechiefrelationshipsstudiedwerethehumanmaleversusyoungdogandhumanfemaleversusyoungdog.
Analysisofsocialrelationships.—Sinceitisdefinedasthebehaviorexhibitedbytwoindividuals,asocialrelationshipsuchasthatbetweenmotherandoffspringmustconsistofbehaviorpatternsbelongingtooneormoreofthenineimportantsystemsofbehaviordescribedinchapter3.Thismakesitpossibletoanalyzeintovarioussortsofbehavioraladjustmentstherelationshipexistingbetweenanytwoindividuals.Sincethereareninesystemsofbehavior,therearelikewiseninepossiblerelationshipsinwhichbothindividualsexhibitthesamepatternsofbehavior.Iftwoindividualsrespondtoeachotherwithunliketypesofbehavior,atotalofthirty-sixmorerelationshipsarepossible.Inactualpracticeonlyafewofthesetheoreticalrelationshipsappeartobeimportantin
practiceonlyafewofthesetheoreticalrelationshipsappeartobeimportantinanyonespecies(Scott,19536).
Inthemother-offspringrelationshipsofdogs,thepredominantbehaviorofthemotherisepimeletic.Thepuppiesexhibitet-epi-meleticbehavior(whiningandyelpingwhenindistress),ingestivebehavior,andeliminativebehavior.Wecancallthistypeofrelationshipcare-dependency.Otherkindsofrelationshipsmaybedevelopedasthepuppiesgrowolder.Intheprocessofweaning,the
motherkeepsthepuppiesfromnursingbygrowlingandthreateningthem,thusestablishingadominance-subordinationrelationship.Othersystemsofbehaviorareexhibitedbythemotherbuthaverelativelylittleimportance.Sincethemothercomestofeedthepuppieswhiletheyremaininoneplace,thereislittleopportunityforaleader-followerrelationshiptodevelopbetweenthem,andthemotherusuallydiscouragesanyattemptsatsexualplayonthepartofthepuppies.
Themostimportantrelationshipbetweenlittermatesisbasedonagonisticbehavior.Thepuppiesgraduallydevelopdominance-subordinationrelationshipswhicharemainlyconcernedwiththedistributionoffoodbutwhichmayalsoaffectthedistancebetweenindividualsastheyoccupytheirlivingspace.Thepuppiesinalittershowagreatdealofallelomimeticbehaviorwithmutualfollowing,butthereislittleornoindicationofimportantleader-followerrelationships.Usually,thefirstpuppytonoticeastrangeobjectwillruntowarditandtherestwillfollow,andwhichpuppyinitiatessuchamovementisamatterofchance.Asforsexualbehavior,whilepuppiesexhibitmuchplayfulbehaviorofthissort,thedevelopmentofadultsexualrelationshipswasnotpermittedbythedesignofourexperiment.Puppiesdoverylittlegroomingeitherofthemselvesoreachothersothatthemutualcarerelationshipseeninprimateshaslittleimportance.Thepuppieshavethecapacityfordevelopingmutualdefenseandcoordinated-attackrelationshipsbutagaintheconditionsofrearingpreventedthisfromdeveloping,sincecontactswithstrangerswerenotpermitted.
Asmightbeexpectedinaschoolfordogs,thedog-humanrelationshipismorecomplex.Thehumanhandlersandcaretakerstakeoverthecare-dependencyrelationshipfromthemotherdogandmaintainitthroughoutthelivesofthepuppies,sothatinthisrelationshipthedomesticdogneverbecomesanadult.Likewise,thehumanhandlersdevelopadominance-subordinationrelationshipwiththepuppiesinwhichthehandlerisalwaysdominant.Bymeansofvarious
withthepuppiesinwhichthehandlerisalwaysdominant.Bymeansofvariouscontrolmethodsthehandlersalsodevelopsomethingofaleader-followerrelationshipwiththepuppies.
Socialcontrol.—Anysocialrelationshipcanbeanalyzedintermsofcontrol.Inmostrelationships,theanimalsobviouslycontroleachotherandtheconceptbecomesimportantonlvwhencontrolisunequal,asitisinadominance-subordinationrelationshiporaleader-followerrelationship.Thedog-humanrelationshipiscomplicatedbydeliberateattemptstoextendandincreasetheamountofsocialcontrol.Twodevicesareimportant:oneisanextensionofthecare-
dependencyrelationshipinwhichthedog'sfoodismadeconditionalonhisperformingcertainactions,andtheotherisanextensionofthedominance-subordinationrelationshipinwhichthedogisforcedtoperformcertainactssuchasfollowingonaleashorsitting.Asmanyobservantwritershavepointedout,thesemethodsareverysimilartothoseonceemployedinhumanslavery.Fromapsychologicalviewpointtheycanbecalledrewardtrainingandforcedtraining.Ineithercasethebalanceofcontrolisshiftedstronglytowardthehumanmemberoftherelationship.
Oneoftheobviousfeaturesofthedog-humanrelationshipisitsmanyresemblancestothehumanparent-childrelationship.Itsdevelopmentthereforebringstheelementalproblemsofchildpsychologyintosharpfocus.Thesuccessesandmistakesofparentswiththeirchildrenareclearlymirroredinthereactionsofyoungpuppiestotheirhandlers.
THEDEVELOPMENTOFDOMINANCERELATIONSHIPSBETWEENLITTERMATES
Thedominancetest.—Wedeliberatelysetupourconditionsofrearingsoastominimizecompetition.Ourpuppieswerefedondryfoodandmilk.Dogsneverfightoverthepossessionofliquidsandseldomattempttodefendafeedingdishinwhichdrydogfoodisalwayspresent.Inordertostudythedevelopmentofdominance,wethereforehadtointroduceacompetitivesituationwhichwecouldcontrolandobserve.From2until10weeksofageeachlitterwasgivenaweeklydominancetrainingperiod.Themotherwasremovedandasingleboneplacedinthepenfor10minutes,duringwhichtimethereactionsofthepuppieswererecorded.
Unlikeliquidanddrydogfood,afreshboneisastrongstimulustoagonistic
Unlikeliquidanddrydogfood,afreshboneisastrongstimulustoagonisticbehavior.Evenpuppiesof2weeksofagewillaccasion-allygrowlandbarkwhengivenameat-coveredbone.Thisisoneofthefewcasesindogsofaspecificprimarystimulusproducingabehaviorpatternandissimilartothemanycasesof"releasers"inbirds.
Asthepuppiesgrewolder,therewasmoreandmorecompetitionoverthebone,andoccasionalfightsbrokeout.At5weeksofagewegaveadetaileddominancetestinsteadoftheusualtrainingperiodandrepeatedthisat11and15weeksofage.
Inthedominancetestallthepuppiesweretakenoutofthepenandbroughtback,onepairatatime.Whentheyhadquieteddown,asinglebonewasbroughtin,showntobothpuppies,andlaidbe-
tweenthem.Anobserverthenrecordedthebehaviorofbothpuppiesfor10minutes,timingthepossessionofthebonebyeachpuppyandnotingtheoccurrenceofgrowls,barks,attacks,andotheritemsofagonisticbehavior.
Alldegreesofdominanceappearedintheinteractionsbetweenthepuppies.Veryrarely,twopuppieswouldsharethebone.Othersappearedtotaketurns;i.e.,aslongasapuppyheldthebonehewasdominant.Stillothersstruggledwitheachothercontinually,andinsomepairsonepuppywouldimmediatelyseizetheboneandholditfortheentire10-minuteperiod.Wedecidedtodefinedominancearbitrarilyasaconditioninwhichonepuppykepttheboneforatleast8outof10minutes.Inordertoprovethatthiswasrealdominanceandnotasituationinwhichthepuppywasallowedtokeepthebonesimplvbecausehegotitfirst,wemadeachecktestattheendoftheperiodbytakingtheboneawayandgivingittotheapparentlysubordinatememberofthepair.Ifthesubordinateanimalcouldkeepit,wesaidthatthefirstanimalwasincompletelvdominant.Ifthebonewastakenaway,wesaidthatthefirstpuppywascompletelydominant.Inshort,wedefinedacompletelydominantanimalasonethatkeptpossessionofthebonethemajorityofthetimeandwasabletorepossessitatwill.
Theresultsshowedthatlittledominancehadbeendevelopedat5weeks.Notmorethan25percentofthetestsshowedcompletedominanceinanybreedatthisage.Bv11weeks,allbreedsshowedalargeincreaseinthenumberofcompletelydominantrelationships.Beyondthispointonlvthewire-hairedterriersshowedacontinuingincrease,althoughthebasenjisandsheltiesshowedanincreasebetween15weeksandoneyear(seeFig.6-1).
Itwasobviousthatthedominanceteststhemselvesservedastrainingperiodsforthedevelopmentofdominancesinceactualfightsoccurredinmany.Thewinningpuppvafterwardsbecamedominantovertheloser.Wealsosawoccasionalfightsamongpuppiesatothertimes,arisingfromundeterminedcauses.Again,thewinnerofthefighttendedtobecomedominantinthefuture.Itshouldbeaddedthatthesefightsbetweenvoungpuppiesweremostlyamatterofnoiseandstruggle,withverylittleactualdamageinflicted.Thusdominancewassettledearlyindevelopmentbeforeadultcapacitiesformoreseriousfightinghadappeared.
Effectofdominanceontheamountoffighting.—Itisoftenstatedthatthedevelopmentofadominanceorderhastheeffectofdecreasingthetotalamountoffighting,sinceonceadefiniterelationshipissetupthereisnolongeranyneedforfights.Inmostofthebreeds
SOCIALRELATIONSHIPS
157
therewasnotenoughobservedfightingsothatrelativepercentagesatdifferentagescouldbeaccuratelycalculated.However,inthebasenjibreed,fightingwasfairlyfrequentandsomeconclusionscanbedrawn(Fig.6.2).Thetotalamountoffightingincreaseswithage,butthisdoesnotholdforallrelationships.Althoughitistruethatfightsbetweenmalesaremuchmorefrequentatoneyearofage,presumablyasaresultofsexualmaturity,thepercentageoftestsinwhichactualfightsoccurbetweenfemales,orbetweenmalesandfemales,remainsconstantbetween10and20percentatany
5II15
AGEINWEEKS
Fig.6.1.—Percentageofoccurrenceofcompletedominanceinlittersofpurebreddogs.
age.Thus,inthisparticularbreed,thedevelopmentofdominanceorganizationseemstokeepfightingataconstantlevel,ratherthandecreasingit,andisunabletosuppressfightingbetweenmalesatsexualmaturity.Ofcourse,wehavenofiguresontheamountoffightingwhichmighttakeplacebetweenstrangepuppiesnotaffectedbyadominanceorder,andthiswouldprobablyshowamuchhigherfigure.
Inaddition,inbothmale-femaleandfemale-femalerelationships,thenumberofattacks(inwhichoneanimalassaultsanotherthatdoesnotfightback)tendstoriseafter11weeksofage.Thenumberofattacksofonemalebasenjionanotherishigherat11and15weeks
BEHAVIORPATTERNS
ofagebutdecreasesatoneyear,probablybecausetheseattacksarenowresultinginactualfightsandareenteredassuchontherecords.Thismeansthatfightingbythedominantanimalisnotsuppressedandmayincreasesomewhat.Nevertheless,thetotalamountoffightingisprobablymuchlessthanitwouldbeifthesubordinateanimalsfoughtback.
20
5■
UJ
(j
LUQ.
^
15--FIGHT
10-■
BASENJI
ATTACKS
20
15
^i-
52
15-•
10
ATTACKS
SHELTIE
FIGHTSN
fc*
II1552
WEEKS
Fig.6.2.—Occurrenceoffightsorone-sidedattacksduringdominancetests.
InShetlandsheepdogsdieresultsaremuchclosertowhatwewouldexpect(Fig.6.2).Therearcmorefightsandattacksat5weeksofagethanatanyothertime.Also,at5weeksofage,there
aremoreattacksinmale-femalepairsthananyothercombination,thisnumberbeingdecreasedtozeroat11weeksofage.
Inthefoxterrierbreedthereweresofewfightsorattacksatanyagethatnopercentagescouldbecalculated.Thisisthebreedinwhichthemostcompletedominanceisseen.Whenseriousfightingbrokeoutinthisbreed,itwasalmostneverbetweenpairsbutinvolvedgroupattacksononeindividual,andthese,ofcourse,couldnottakeplaceinthepaireddominancetests.Intheothertwobreeds,beaglesandcockerspaniels,therewerelikewisealmostnoobservedfights,notbecauseofarigiddominanceorder,butbecausethesebreedshaveaverylowdegreeofaggressiveness.
Thus,thetheoryofthedominanceorderasacontrollingagentinfightingisupheldintwobreeds,foxterriersandshelties,butnotinanother,thebasenjis.Thisfindingmaybepartiallyexplainedbythefactthatthebasenjishaveseasonalbreedingandconsequentlymoresuddenchangesinthelevelofthemalehormoneastheyapproachmaturity.However,thereisalsomorefightinginthisbreedatyoungerages,anditispossiblethatallthisistheresultofforminglessrigidhabitsofdominanceandsubordination.Atanyrate,thereseemtobedefinitebreeddifferencesinthecapacitytodevelopaneffectivecontrolsystemoverfightsbetweenindividuals.
Theeffectofbreedondominanceorganization.—Knowingthatthebreedshavebeenselectedfordifferencesinaggressiveness,wewouldexpectthatthedevelopmentofdominancerelationshipsmightshowlargedifferencesbetweenbreeds,andthisisindeedthecase.
Inwire-hairedfoxterriers,thenumberofdominancerelationshipswasgreatlyreducedafter5weeksofagebythegroupattackswhichledtotheseparationofanimalsfromtheirlitters.However,thepercentageoftestswhichresultedincompletedominancecontinuedtorise(Fig.6.1).Whenwe(PawlowskiandScott,1956)analyzedthisrise,wefoundthatitconsistedalmostentirelyofmale-femalerelationshipsandthatmoreandmoremaleswerebecomingcompletelydominantovertheirsisters(Fig.6.3).
completelydominantovertheirsisters(Fig.6.3).
Thebasenjisshowedadifferentpicture.Thetotalnumberofcompletedominancerelationshipsrosebetween5and11weeksbutstayedatalmostthesamelevelat15,thenrosesharplyagainatoneyear.Thefightingbehaviorofthebasenjithustendstoappearinlaterdevelopment,ratherthaninearlypuppyhoodasitdoesinthewire-hairedfoxterriers.Thedominanceofmalesoverfemalesshowedthesamesteadyriseasinthewire-hairedterriers,andatoneyearnofemaleswerecompletelydominantovermales.
II15
WEEKS
5II1552
WEEKS
WEEKS
Fig.6.3.—Occurrenceofcompletedominanceinmale-femalepairs.
WEEKS
WEEKS
Fig.6.3.—Continued.
BEHAVIORPATTERNS
100
II15
WEEKS
Fig.6.3.—Continued.
Beaglesandcockerspanielswerequitesimilarintheirdevelopmentofdominancerelationships.Therewasarisebetween5and11weeksandaslightdeclineafterthattime,continuinguntiloneyear.Asadults,bothcockersandbeagleswerelikelytobeindifferenttopossessionoftheboneandtopayattentionsolelytotheobserver,sothatnodominancestatuscouldbedetermined.Furthermore,thesetwobreedswereverydifferentfromtheotherswithrespecttomale-femaledominance.Thereislittleindicationthatmoremalesaredominantthanfemales,andifanything,thereisaslightdifferenceinfavorofthefemalesbyoneyearofage.
Shetlandsheepdogs,likebeaglesandcockers,showedalargenumberofcasesofincompletedominanceandparticularlyofcaseswherenodominancecouldbedetermined.Themajorityofthelattercasesturnedouttobebetweenmalesandfemales.Inasmallsampleof11male-femalepairs,thereweretwocasesinwhichthefemalewasdominant,threecasesinwhichamalewasdominant,andsixinwhichtherewasnodominance.Thisisquitedifferentfromtheotherbreeds.Incockersandbeaglestherearemorecasesofcompletedominancebetweenmalesandfemalesthanbetweenlikesexes,andinbasenjisandfoxterriersthereisastrongtendencyformalestodominatefemales.Thesheltiestendnottodominatefemalesinconflictsoverfood.
Thisbreeddifferencemayreflectacharacteristicoftheshelties,
Thisbreeddifferencemayreflectacharacteristicoftheshelties,
SOCIALRELATIONSHIPS163
whoarerelatedtotheScottishcollies.InthestoriesofAlfredPaysonTerhunetherearemanyreferencestothe"chivalry"ofthemalecollietowardthefemale.Certainlyweobservednothingofthekindinthepuppiesoffourofourfivebreeds,butthesheltiesmaybeanexception.However,theseresultswithcompetitionoverabonedonottellthewholestoryofthedominancerelationshipsinthisbreed.Asobservedintheirlargeoutsidepens,thesheltiesdevelopedastrongdominanceorderbasedonspace.Wheneveranobservercamenear,theentirelitterwouldrushoutandstarttobark,butalmostimmediatelytwoorthreeoftheanimalswouldturnontheirlittermatesanddrivethembacktowardtheirhouse,wherethefoodandwaterwerekept.Inonelitter,onefemalecouldneveremergefromthehousewithoutgettingchasedandbarkedat.Asmallmalewasallowedtositoutsidethehouse,whiletwolargemalescouldrunupanddownthepen,barkingfreely.Inshort,thereappearedtobeastrongdominanceorderbasedonspaceratherthanfood,withnodeferencepaidtotheweakersex.Basenjis,ontheotherhand,seemedtobecompletelytolerantofoneanotherwithrespecttospace.Agroupwouldsitpeaceablyorrunsidebysidewithoutinterference,butcompetefiercelyassoonasfoodwasbroughtintothepen.Inaseparateexperiment,inwhichbasenjisweregivenspecialfoodinadish,thedominantmemberimmediatelytookchargeofthedishandwouldallownoneoftheotherstoeat.Oneofthesubordinateanimalsdevelopedthetechniqueofrushinginwhenthedominantanimal'sbackwasturnedandtippingoverthedish.Hewasthenallowedtoeatthefoodspilledontheground,butnotoutofthedishitself.
Suchdifferencesinbehaviorindicatethatdominancehierarchiesarenotuniversalbutaredevelopedinspecifickindsofsituations.Whetheritwouldbepossibleforadogtooccupyadifferentpositioninahierarchyundertwodifferentsituationsisaquestiononwhichwehavenoevidence.
Thebreeddifferencesarealsocomplex.Thefourhuntingbreedsareallstronglymotivatedbyfoodbutdiffergreatlyinaggressiveness,thebeaglesandcockerspanielsbeingmuchmorepeacefulanimals.Theshelties,ontheotherhand,appeartohavearatherhighdegreeofaggressivenessbutarerelativelylittlemotivatedbyfood,sothattheysimplydonotcompetestronglyforitspossession.Therehasundoubtedlybeenselectioninthisbreedforthelackoffoodmotivationwhichwouldbelikelytointerferewiththeirtrainingasworkingdogs.
dogs.
Geneticeffectsonthedominanceorganizationoftheentiregroup.—Thekindoftestdescribedabovedoesnotreflecttheeffectof
BEHAVIORPATTERNS
severalmembersofagroupuponeachother.However,wecanexpressthetotalorganizationintermsofrelationshipsbetweenindividualpairs.Whenwedothis,wefindthatthereisagreatertendencyintheaggressivebreedstodevelopastraight-linedominancehierarchywitheachanimaldominantoverthoseinthelowrerranks.Inthelessaggressivebreeds,adominancediagramhasasprawlingappearancewithseveralindividualsinthesamerank,althoughwegetfew,ifany,casesofthecirculardiagramswhichsometimesoccurinflocksofchickens.
Theeffectsofsexandsize.—Withrespecttosex,wehadthreekindsofrelationshipsinourexperiment:male-male,female-female,andmale-female.Whenmalesandfemalesmeteachotherthemalestendedtodominate,particularlyincasesofcompletedominance.Also,thereweremorecasesofcompletedominancebetweenmalesandfemalesthantherewerebetweenlikesexes,eithermalesorfemales.Thisreflectsthefactthatmalesareontheaveragelargerandmoreaggressivethanfemales.
Table6.2summarizestheresultsofathoroughanalysisoftheeffectofsizeondominanceat15weeksofage.Thereisnoindicationthatsizehasanyeffectonthedominanceexistingbetweenfemalepairs,eveninpairswhichshowedlargedifferencesinweight.Inthemalepairs,heavieranimalstendedtobedominant,providedtherewasadifferenceofatleast1kilogram.Thiseffectismorestrikinginthehybridsthaninthepurebreds,butifallhybridsandpurebreds
TABLE6.2
EffectofSizeon-Dominance-SubordinationRelationships(HybridsandPureBreedsCombined)
9P<.05••P<.01
SOCIALRELATIONSHIPS165
areaddedtogether,thedifferencebetweentheactualfiguresandthosewhich
areaddedtogether,thedifferencebetweentheactualfiguresandthosewhichwouldbeexpectediftherewerenoeffectofsizeisstatisticallysignificantatthe.03level.Withregardtothemale-femalecontests,thereisauniformtendencyforheavieranimalstobedominantinaratioofatleast2to1,butthis,ofcourse,reflectsboththeheavierweightandgreateraggressivenessofmales.
Thisdifferenceindominancerelationsdevelopedbythetwosexesiseasilyexplainablebytheobserveddifferencesinbehavior.Femalesrarelygetintoactualfightswitheachotherandseemtoestablishdominancelargelyonthebasisofvocalizationandthreats.Ontheotherhand,malesoftengetintorealfights,inwhichsuperiorsizeis,ofcourse,importantindeterminingtheoutcome.Similarly,malesarelikelytomakeactualattacksonfemalesratherthanbeingintimidatedbybluff,andtheresultisusuallydominancebythemale,particularlyinthemoreaggressivebasenjiandfoxterrierbreeds.Incontestsbetweenmalesandfemales,thesuperiorsizeofthemalesaswellastheirgreateraggressivenessundoubtedlyplaysapartintheoutcome.
Geneticsandthedifferentiationofbehavior.—Themostimportantconclusionfromtheaboveresultsisthatwegetextremedifferentiationbetweenthebehavioroftwoindividualsinvolvedinarelationshiponlywheretherearelargedifferencesinthecapacitiesofthetwoindividuals,astherearebetweenmaleandfemalepuppies.Morethanthis,bothindividualsmusthavethebasiccapacitytodevelopinadifferentialway.Forexample,beaglesdonotseemtopossessthecapacitytobecomehighlyaggressiveinanyofthecircumstanceswhichwestudied.Iftheabovegeneralizationiscorrect,wewouldexpecttogetgreaterdifferentiationbetweenlike-sexedpairsinsegregatinghybrids(F2'sandbackcrosses)thanwewouldinnon-segregatinghybrids(Fi's)orinpurebreeds,andourexperimentongeneticsandbehaviorprovidesagoodtestofthehypothesis.
AsTable6.3shows,thisexpectationiswellborneoutbythedata.Notonlyarethelike-sexedpairsmoregreatlydifferentiatedinthesegregatinghybrids,butalsothemale-femalepairs.ThebestcomparisonisbetweentheFihybridsandthesegregatinghybrids,andthereisalargerproportionofpairsshowingcompletedominanceineverysegregatinghybridpopulation.Thesameistruewhenthesegregatinghybridsarecomparedwiththepureparentbreeds,exceptforthefemalebasenjis,whichshowslightlygreaterdifferentiationthandothecockerbackcrossesortheF2's.Wemayconcludethatthedifferentiationofasocialrelationshipisproportionaltothedifferenceinbasiccapacitiesofthetwoindividualsconcerned.
BEHAVIORPATTERNS
TABLE6.3
PercentageofCompleteDominanceinBasenjis,Cockers,andTheirHybridsat15Weeks
*P<.05**P<-01
Oneofthebasicreasonsforstudyinggeneticsandbehavioristofindoutjusthowimportantgeneticdifferencesinbehavioralcapacitiesmaybe.Inmanyinstancestheseseemtohavelittleimportanceincomparisontotheeffectsofenvironmentalfactors.Here,inthedevelopmentofsocialrelationships,wehaveacaseinwhichgeneticfactorsarehighlyimportantdeterminantsofbehavior.Thisdoesnotexcludeotherdeterminants,ofwhichwehavemanyexamplesevenindogsraisedinauniformenvironment.Inthemother'srelationshiptothepuppy,relativeageisextremelyimportantinthedevelopmentofadominancerelationship,asmothersarealmostinvariablydominantovertheirpuppies,althoughtheydonotalwaysenforcethisincompetitionoverfood.
Inhighlydevelopedrelationshipsthebehavioroftwoindividualsbecomesdifferentiatedwithrespecttoeachother,i.e.,onebecomesdominantandtheothersubordinate.Atthesametime,eachindividualretainsthecapacitytofurtherdifferentiatehisownbehaviorinrelationtootherindividuals.Thesamepuppymayoccasionallythreatenanotherinarelationshipinwhichheisdominantandincompletecontrol,frequentlyattackinarelationshipinwhichdominanceisunsettled,orbeextremelysubmissiveinarelationshipinwhichheissubordinate.Thesameanimalcanthusbecorrectlydescribedasmoderatelyaggressive,extremelyaggressive,orunaggressive.
Whatthenbecomesoftheideaofa"personality"composedofsimplebehaviortraits?Wearelikelytothinkofananimalorpersonasbeinggenerallyaggressiveorgenerallysubmissive.Thisobviouslydoesnotfitthefacts.Ifwewanttocharacterizethebehaviorofanindividual,weshallhavetodoitintermsofhisrelationships,andinanypracticalsituationthismeansselectingandanalyzingthemostimportantandgeneralrelationshipsoutofmanyspecialandminor
ones.
Isitthenpossibletomakeanygeneralizationsaboutanindividual?Wecansay
Isitthenpossibletomakeanygeneralizationsaboutanindividual?Wecansaythatanindividualhasabasiccapacity,butthiscapacitycanonlybedevelopedintermsofrelationships.Oneanswertotheproblemisthatwhiletherearecertainkindsofrelationshipswhicharespecialandcompletelyunique,thereareotherswhichapplytoseveralindividualsandcanbecalledgeneralrelationships.Examplesofthesetwokindsareeasytofindinhumansituations.Achildhasonlyonemother(aspecialrelationship),butseveralaunts,allofwhomaretreatedmoreorlessalike(ageneralrelationship).Ourpuppyexperiment,ontheotherhand,wassetuptodevelopsocialrelationshipswithasmallgroupofexperimenters,allofwhomattemptedtoactalike.Aswillbeseenfromtheresultsoftheobediencetestdescribedinchapter9,thepuppiesevidentlydevelopedageneralrelationshipwithallexperimenters.
Oneanswertothequestionofthegeneralityofbehaviortraitscamefromthefactthatwhenwetookapuppyoutofthepenandthenputhimbackinwiththelittermates,theyfrequentlythreatenedhim,exhibitingconsiderableaggressivebehavior.Thislookedlikeanopportunitytostudythephenomenonofjealousy,astheotherpuppiesappearedtobe"jealous"oftheonewhohadbeenremoved.Dr.TheodoreZahn,avisitinginvestigatoratHamiltonStation,systematicallystudiedthisphenomenoninseverallitters,takingeachpuppyout,returningit,andobservingtheresults.Hesoonfoundthatrightingwasconfinedtocertainindividualsineachlitter,observingonly10casesofdominancein61relationships.Whenhecomparedhisresultswiththoseofthedominancetestoverbones,hefoundthatmostoftheanimalswhichthreatenedeachotherhadnotpreviouslyshownconsistentdominance.Inotherwords,themanifestationof"jealousy"reflectedthefactthatcertainanimalshadnotestablishedadefinitedominancerelationshipbetweenthemselves.
InanothersortofexperimentKing(1954)placedlittersofadultbasenjisandcockersinlargefieldsandobservedtheirreactiontotheintroductionofstrangeanimals,uptothepointwhenseriousfightingbegantotakeplace.Whenheanalyzedhisdata,hefoundthatthedogswereexhibitingmostaggressivenesstowardanimalslikethemselves.Femalecockersattackedstrangefemalesmoreoftenthantheydidstrangemalesandattackedstrangecockersmorethantheydidstrangebasenjis.Thisinterestingfindingindicatesthatindogs,atleast,thereisnobasichostilitytowardunlikeindividuals.Iftheyarebasicallyhostile,itistowardstrangersresemblingthemselves.Onepossibleexplanationisthattheyattempttoextendthe
dominancebehaviorwhichtheynormallyexhibitintheirowngrouptoinclude
dominancebehaviorwhichtheynormallyexhibitintheirowngrouptoincludeanimalsoffamiliarappearance,butthatthisgeneralizationislesslikelytowardanimalsshowinganunfamiliarsizeandshape.Thereisalsoatendencytoreacttoanimalsoftheoppositesexthroughsexualratherthanagonisticbehavior.
Mostofourstudiesofsocialrelationshipshavebeendonebetweenthetwomembersofapair,partlybecausethisisprobablythemostimportantkindofrelationship,andpartlybecausethetechniqueisrelativelysimple.Whenonebeginstoexaminerelationshipsintermsofgroupsofthreeindividualsinsteadoftwo,theproblemofanalysisbecomesextremelycomplex.Itis,however,animportanttheoreticalandpracticalquestionwhethertherelationshipbetweentwoindividualsisthesamewhentheyarebothpartofagroup.Instudiesofchickensandgoats,thereiseveryevidencethatindividualpaircompetitionsgivethesameresultasgroupcontests.Intheseanimalsfightingalwaysoccursbetweentwoindividualsandtherearenogroupattacks.Butdogsarecapableofgroupattacksonanindividual,andthesituationheremaybequitedifferent.
Wehavesomeobservationalevidencethatthepresenceofagroupmodifiesthebehaviorofoneindividualtowardanother,inthiscasetowardahumanhandler.Weoftenfoundwhenweenteredadogpenthatsomeanimalscameboldlyforwardandothershungback.Yetwhenwetestedallanimalsinanindividualhandlingtest,wefoundthatsomeoftheapparentlyshyanimalswerestronglyattractedtopeople.Theystoodatthebottomofthedominanceorderamongdogsandwerebeingkeptawayfromthehumanhandlersbythemoredominantmembersofthegroup.Dogbuyersfrequentlyselectpuppiesonthebasisofwhichpuppyinagroupcomesmostboldlyforward.Insodoingtheymaybeselectingforaggressivenessagainstotherdogsaswellasagainstshynessofpeople.
Moreobjectivedataonthispointwereobtainedbymeasuringthecatchingtimeofindividualsinagroupduringtheweeklyinspection.Whenwecomparedthesetimeswithattractionscoresinthehandlingtest,wefoundarelativelylowcorrelation.Outof22littersanalyzed(2eachfromallbreedsandhybrids),16showedapositiverank-ordercorrelation,withanaverageRof.30.
Inconclusion,theexpressionofbehaviorinasocialrelationshipisahighlycomplexexpressionofgeneticdifferenceswhoseactionisdependentuponthedevelopmentofbehaviorbetweentwoindividualswhomutuallyaffecteachother.Neverthelesswecanexpresstheresultsasagenerallaw:arelationshiptendstobedifferentiatedinproportiontothedifferentialbiologicalcapacitiesofthetwoindi-
thetwoindi-
SOCIALRELATIONSHIPS169
victualsinvolved.Themostimportantofthesebiologicalcapacitiesaredeterminedbysex(whichis,ofcourse,hereditary),byindividualheredity,andbyage(whichreflectsbiologicaldevelopment).Allofthesedeterminetheprocessofpsychologicaldifferentiationofbehaviorwhicheventuallyfreezesarelationshipintoarelativelystableform.
Thisgeneralizationneedstobewidelytestedinordertobefirmlyestablished.Assumingthatitiscorrect,allsortsofpracticalapplicationsimmediatelysuggestthemselves.Ifwedesireahighlydifferentiatedrelationship,asinaleader-followerrelationship,thisshouldberelativelyeasytoestablishbetweenquiteunlikeindividuals,asbetweenolderandyoungerpersons.Itwouldbemostdifficulttoestablishleadershipwithinagroupoflikeageandsex,wheretheonlybasicdifferentiationwouldbethatbetweenindividualshavingmarkedlydifferentheredity.Itisnowonderthatpeoplelookingataboys'grouparelikelytoconcludethatoneofthemisa"natural"leader,sinceheredityisalmosttheonlywayinwhichoneboy'sbehaviorcouldbedifferentiatedfromtherest.Ontheotherhand,itisalsopossiblethathisbehaviorcouldhavebeendifferentiatedbyunusualprevioustraining.Thislastquestionhasnotbeenansweredbyourdogexperiment,inwhichearlyenvironmentwaskeptuniform.Experimentswithinbredmiceinwhichhereditywaskeptconstantbutcertainindividualsweregivenpre-traininginfightingshowthatarelationshipcanalsobedeterminedbydifferentialtraining(Scott,1944).Ifwewanttomakeourgeneralizationmoreuniversal,wemustaddthefactorofdifferentialdevelopmentofcapacitiesbytrainingandpreviousexperience.
THEMOTHER-OFFSPRINGRELATIONSHIP
Fromthedescriptionofdevelopmentinthepreviouschapterweconcludedthatthepuppywasincapableofforminganytruesocialrelationshipuntilapproximately3weeksofage.Thisconclusiondoesnotapplytothemother,whocanbegintoformrelationshipsassoonasthepuppiesareborn.Thusthemother-offspringrelationshipisextremelyone-sidedinthefirstfewweeksafterbirth.Furthermore,sincethemotherpaysthegreatestamountofattentiontothepuppiesinthesefirstfewweeksandbeginstoleavethemmoreandmoreastheygrowolder,theeventualrelationshipofpuppiestotheirmotherisweakerthanthatformedwiththeirlittermates.
Thegeneralbehaviorofthemothertowardherpuppiesatfirstincludesagreatdealofnursing,combinedwithmuchlickingand
BEHAVIORPATTERNS
cleaning.Ifdisturbedbyexperimentersorcaretakersshecomesoutofthenestboxandinvestigatesorbarksattheintruders.Shemakesnoattempttodefendthepuppiesagainsthandlingbyfamiliarpersons,butoftenseemsnervousanddiscontinueshercarewhiletheyareabout.Consequently,itisessentialtokeepthemotherandherlitterinundisturbedsurroundingsforthefirstfewweeks.
Individualdifferencesintheattentivenessofmotherstowardtheiroffspringarecommon,andwewishedtofindoutwhethertherewereconsistentdifferencesbetweenthedifferentbreedsinrespecttomaternalcarewhichmightaffectthebehavioroftheiroffspring.Wethereforecollectedobjectivedataonthemother-offspringrelationshipandselectedtheagesof1weekand7weeksforparticularstudy,theformerbecausematernalattentionwasclosetoitsheightatthispoint,andthelatterbecauseitisatimewhenallmothersareintheprocessofweaningtheirpuppiesandmightexhibitdifferentialbehaviorifiteveroccurred.
Nursingbehavior.—Whilewemadetheweeklyobservationsandweighings,wealsorecordedwhatthemotherwasdoingaseachpuppywastakenawayfromherandplacedonthescales.AsseeninFigure6.4,themotherscontinuedtonursetheirpuppiesverynearly
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SOCIALRELATIONSHIPS
171
100percentofthetimeimmediatelyafterbirth,butthisfiguresteadilywentdownwardinsubsequentweeks,beingapproximately30percentwhenthepupswere4weeksold.Therewasalmostnodifferencebetweencockerandbasenjimothers,buttheFimothersapparentlylefttheiroffspringinagreaternumberofcases.Thesehybridmothers(Fi)hadaverymuchbettermilksupplythanthepurebredonesandonthewholetookexcellentcareoftheiroffspring.Itlooksas
purebredonesandonthewholetookexcellentcareoftheiroffspring.Itlooksasiftheamountoftimespentnursingmightnotbedirectlydependentuponthemilksupplybutratherupontheresponsesofthepuppies.Thatisythestimuluswhichkeepsmotherwiththepuppiesmaybetheirsuckingbehavior.However,thenumbersofanimalsconcernedaretoosmalltodrawanydefiniteconclusionsexceptthatthedownwardcurvesobviouslyconfirmtheimpressionthatthemothersaremuchmoreattentivetothepuppiesintheearlypartoftheirlives.Asimilarconclusioncanbedrawnfromobservationsonundisturbedmothers(Table6.4),exceptthatundertheseconditionsthereareindicationsofbreeddifferencesbetweencockersandbasenjis.SimilarresultshavebeenobtainedbyRheingold(1963)withthisandnumerousothermeasuresofmaternalcare.
TABLE6.4
OccurrenceofMothersNursingPuppiesunder2WeeksofAgeduring10-mlnutedailyobservations
Retrievingtest.—Whenthepuppieswere1weekoldwetookthemotheroutoftheroomforafewminutes,tookthepuppiesfromthenestbox,anddistributedthematequalintervalsaroundtheedgesofthenurseryroom.Thenweputthemotherbackandobservedherfor15minutes,recordingwhichpuppieswerevisited,thenumberofvisitstoeach,andthetimewheneachpuppywascarriedbacktothenest.Themotherusuallywentfrompuppytopuppy,touchingeachonewithhernose.Thepuppiesmeanwhileusuallymadecontinuouswhiningnoises.Finally,themotherwouldpickeachoneupandtakeitbacktothenest,carefullycarryingitinherjawswiththepuppy'sfeetdanglingdown.
BEHAVIORPATTERNS
TABLE6.5
OccurrenceofRetrieving1-week-oldPuppiesbyPurebredandHybridMothers
Figuresbasedonverysmallsample.
AsTable6.5shows,thebasenjimotherscarriedtheiryoungbacktothenestmoreoftenthandidthecockers.However,therewerebigindividualdifferences,usuallyconsistentfromlittertolitter.Somemothersalmostalwaysretrievedtheirpuppiesandothermothersneverdidso.Tenofthe13cockermothersdidnoretrievingatall,whereas6outof8ofthebasenjimothersretrievedatleastsomeoftheirpuppies.Thisissomewhatcuriousbecausethecockerspaniel
someoftheirpuppies.Thisissomewhatcuriousbecausethecockerspanielbreedhasbeenselectedfortheabilitytolearntoretrieveandcarrygame.Apparentlythesetwotypesofretrievingarenotcloselyrelated,andwecanconcludethatthebasenjimothershavebeenselectedforbettermaternalcare,probablybecauseoflesshumanassistanceintheirnativeAfricanvillages.
Therewasconsiderablevariationintemperaturebetweendifferenttests,andonemightsupposethatthemotherswouldretrievethepuppiesmorepromptlyifthepuppieswerecoldandmakingmorenoise.Analysisofthedatashowedthatthetemperaturehadnoconsistenteffect,butratherthatthecharacteristicbehaviorofthemotherwastheimportantfactor.
Anotherinterestingobservationwasthatthemothersseemedtoplaynofavorites.Theyvisitedeachpuppyaboutthesamenumberoftimes,andwhentheybegantobringthembacktheydidsoinwhatappearedtobearandomorder.Sometimesthemotherwouldbringbacksomeofthepuppiesandliewiththeminthenestbox,leavingtheothersoutside.Atothertimesthemothermightstopandallowapuppytonurseoutsidethenest.Wedidnot,however,makethecriticaltestofrepeatingtheobservationtoseewhetherthepup-picswerecollectedinthesameorder.
Thesedataconfirmtheimpressionthatdogmothersmakelittleifanydistinctionbetweenmembersofthelitter.Tinsisquitedifferent
fromtheconditionsofhumanmotherhood,inwhichthenecessarilydifferentagesofchildrenmakedifferentialtreatmentnecessary.Thedogmotherisinthesamesituationasahumanmotheroftwins,orperhapsquintuplets,allbeingthesameageandverymuchalike.Theonlytimeadogmotherwillshowobviousdifferentialtreatmentisinthecaseofasickordvingpuppy.Oncethepuppybeginstogetcoldandinactive,themotherpaysverylittleattentiontoit.
Weaningtest.—Whenthepuppieswere7weeksofage,wetookthemotheroutofherpenforanhour,sothatmotherandpuppieswereseparatedforaconsiderableperiod.Wethenputherbackwiththepuppiesandrecordedtheensuingactivitiesonachecklist.Usuallythepuppieswouldallrushtowardthemother,attemptingtonurseasshemovedaroundtheroom.Theirbehaviorwasquitesimilartotheresponsegiventoahumanhandlerwhenheholdsoutahandtotheyoungpuppies.Ifthemotherallowedthemtonurse,sheusuallystoodstillforafewminuteswhiletheyleapedaround,pawed,andsucked.Whiletheyweredoingthisshemightvomit,whereupontheyatethenewfood.Iftheysubsequentlytriedtonurse,shewouldturnontheoffendingpuppieswithaloud
subsequentlytriedtonurse,shewouldturnontheoffendingpuppieswithaloudgrowl,openinghermouthasiftobiteandrushingtowardthem.Thepuppiesatonceretreated,sometimesrollingontheirbacksandyelping,butthemotherwasneverseentoactuallybiteoneofthem.Atthisagesuchbehaviorwastypicalofalmostallmothersandtheiroffspring.
Anothertestwastoplaceaboneinthepenwiththemotherandpuppies.Inalmosteverycasethemotherdidnotcompetewiththem,althoughshewasalwaysdominantoverthemwhentheyattemptedtonurse.Inothersituationswherethemotherandpuppieswerefeddishesofsemi-solidfood,wehaveobservedmotherswhichwouldtakepossession,drivethepuppiesaway,andburythefoodwithshavingsfromthefloor.Thenormalbehaviorofmotherstowardpuppiesofthisage,however,seemstobetolimitthepuppies'nursingbehaviorbuttoallowthemtoeatotherfoodatwillwithoutcompetition.
Followingtest.—Themothersweretakenawayfromthepuppiesat10weeksofage.Neitherappearedtobedisturbedbythechange.Themothershadonlyonecontactwiththepuppiesthereafter,at18weeksofage.Atthistimewebegantotrainthepuppiestowalkonaleash.Wesoonfoundthatifwebeganleashtrainingwithoutsomepreparation,thepuppiesbecamefrightenedanddidverypoorlyonthetest.Therefore,asanintroductiontotheleash,wefirsttrainedthepuppiestofollowwithoutit.
Onthefirstdayofthetestthepuppieswerefedaspecialdishoffishbytheexperimenter,andthesamethingwasrepeatedthenextday.Onthethirddaytheexperimenterwentintothepenwiththefooddishesbutinsteadofgivingthemtothepuppies,shewalkedoutofthepenandtowardthelaboratorythroughanexperimentalfield.Thepuppieswerefedaftertheyhadfollowedherintothelaboratory.Onthefourthdaythepuppiesweretestedoneatatime.Theexperimenterdidnotcarrythefoodbutsimplywalkedalong,andinsteadofgoingdirectlythroughthefield,shewentaroundtheedgeofthefence.Thus,ifthepuppywasinterestedonlyinthefoodreward,itcouldrunaheadoftheexperimenter.Theamountoftimewhichthepuppyspentwithinadog'slengthoftheexperimenterwasrecordedtogetherwiththetotaltimespentwalkingfrompentolaboratory.Theexperimenteralsoratedthepuppyaccordingtohowcloselyitfollowed,providingasecondmeasureofthetendencyofapuppytofollow.Onthefinaldayoftheexperimentthesameprocedurewasrepeated,exceptthattheexperimenterledthemotherofthepupsonaleash,allowingthepuppytofollowatwill.
Thisisnotaperfectexperimentfordeterminingwhetherthepuppyismore
Thisisnotaperfectexperimentfordeterminingwhetherthepuppyismoreattractedbythehumanhandleroritsmother.Itshouldhavebeendoneinreverseorderaswell,tocancelthepossibleeffectoftraining.Astheexperimentwasactuallyrun,almosteverypuppyspentmoretimeclosetothehandlerwhenthemotherwasalsopresent,andoftenthreetimesasmuch.Wecanatleastconcludethatthepuppieswerestillstronglyattractedbytheirmother(Fig.6.5).Ontheotherhand,thereactionofthemothertothepuppieswaseitheroneofindifferenceorrejection.Ifthemotherhappenedtobeinheat,aswassometimesthecase,shemightbeapproachedbyamalepuppybutwouldwarnhimoffwithagrowl.Whenevertinssortofbehavioroccurred,themotherwasstronglydominantoverthepup.
Inconclusion,themothersdevelopthreetypesofrelationshipswiththeiroffspring.Inthecare-dependencyrelationship,developmentproceedstowardadecreasingamountofmaternalcareandincreasingindependenceofthepuppies.Thischangeisbroughtaboutintwoways.Themotherbeginstoleavethepuppiesmoreoftenandatthetimeofweaningactivelyrejectsthem.Thereislittleornodifferentia]treatmentbythemother,whohasthesamegeneralrelationshipwithallthepuppiesinthelitter.Thephenomenonofsiblingrivalrysimplydoesnotoccurinordinarydogdevelopment.
Thereis,however,competitionoverfood,andthepuppies,whoneverseemtocompetewitheachotherformaternalcare,develop
SOCIALRELATIONSHIPS
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Fig.6.5.—Averagetimespentwithhandlerduringthe"followingtest."Notethatthesameorderismaintainedbetweenbreedsineverytest,withoneexception.Allbreedsspentmoretimewiththehandleronthesecondday,whenthemotherwasalsopresent.
strongdominancerelationshipswitheachotherinconnectionwithfood.Thedominancerelationshipbetweenmotherandpuppiesisquitedifferent.Themotherdoesnotordinarilyexertdominanceinthepresenceofabone,althoughsheisdefinitelydominantinothersituations,particularlywhenweanedpuppiesattempttonurse.Eventhistypeofdominanceisdifferentfromthatbetweenpuppies,asitneverseemstoinvolveactualfighting,butisdevelopedandenforcedsolelybymeansofthreats.
The"followingtest"indicatesthatundertheproperconditionsaleader-followerrelationshipcouldbedevelopedbetweenmotherandoffspring,anditispossiblethatthismayoccuroccasionallyinthewildCanidae.However,inmostcaseswolfpuppiesdonotstaywiththeirparentsbutformnewpacksoftheirown.Awell-developedleader-followerrelationshipisnotacharacteristicpartofeither
well-developedleader-followerrelationshipisnotacharacteristicpartofeitherdogorwolfsocieties.
THEDOG-HUMANRELATIONSHIP
Aswesawinthepreviouschapter,therelationshipsbetweendogsandhumanbeingsmaydevelopinmanydirections.Atoneextreme,
apuppyraisedentirelyapartfromhumanbeingsmaylaterreacttowardthemwithextremefearandhostility.Attheother,apuppytakenawayfromdogsatanearlyagetransfersallitssocialrelationshipstothehumanspeciesandbecomesan"almosthuman"dog.Whateverthisrelationshipmaybe,itisnormallywellformedby7weeksofage,althoughitgoesondevelopingandchanginglongafterthat.Weshallnowdiscussthefurtherdevelopmentofthedog-humanrelationshipandtheeffectofgeneticdifferencesuponit.
Anyrelationshipis,ofcourse,determinedbythebehaviorofbothparties.Sincewewereinterestedprimarilyinthebehaviorofthedogsandnotoftheirhumanhandlers,wetriedtostandardizethehumanhalfoftherelationship.Weinstructedallexperimentersandhandlerstotreatthepuppieswithuniformkindnessandnottomakespecialpets.Intestsituationswemadeitaruletogiveeverydoganequalopportunity,withoutplayingfavorites.Ifanyspecialtreatmenthadtobegiventooneanimalinalitter,theinstructionsweretodothesamethingtoallmembersofthegroup.Whiletesting,allexperimenterswereinstructedtowearwhitelaboratorycoatssothattheirgeneralappearancewassimilar,althoughtheydifferedindetailsofclothing.
Becauseofthegoodscientifictrainingandco-operationoftheexperimenters,theefforttostandardizehumanbehaviorwaslargelysuccessful.Fromtheviewpointofanalyzingtheeffectsofheredity,theresultswereexcellent.Anunexpectedresultwasthatthequalityofthesocialrelationshipwhichdevelopedwassomewhatshallow.
Thedevelopmentofthecare-dependencyrelationship.—Ourchiefexperimentalmeasureherewasthehandlingtest,describedinthepreviouschapter.Thisisessentiallyatestofsocialrelationships,anditsresultsaredividedintoseveralparts.Thefirstincludesinitialresponsesbythepuppytothreateningbehaviorbytheexperimenter,andthesearescoredasreactionsofescapeandavoidance.Second,asthepuppiesgrowoldertheybegintoreacttowardthehandlerinmuchthesamewayastheyacttowardthemother,runningtowardhimand
muchthesamewayastheyacttowardthemother,runningtowardhimandwaggingtheirtailsandlickinghishands.Stilllater,thepuppiesbegintoreactastheywouldtowardtheirownlittermates,withagreatdealofplayfulfightingandoccasionalplayfulsexualbehavior.Thepositivepatternsofbehaviortendtooccurincombinationwitheachotheratthisage,andtheirseparationisperhapssomewhatartificial.Inscoringthetest,however,wedividedtheresponsesintofearfulbehavior,playfulfighting,socialinvestigationandet-epimeleticbehavior,andattraction.Theet-epimeleticbehaviorandattractionscoresareperhapsmostcloselyrelatedtothecare-depend-
Thefivepurebreeds.Lefttoright,wire-hairedfoxterrier,Americancockerspaniel,Africanbasenji,Shetlandsheepdog,andbeagle.
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Outsiderunswherethepuppieslivedfrom16to52weeksofage.InthebackgroundisthenurserywinsoftheBehaviorLaboratory.
Nurseryroominterior.Shetlandsheepdogfemalecarriesapuppyinaretrievii..Puppieslivedinroomssuchasthisonefrombirthuntil16weeksofage.
BehaviorLaboratoryandStaff
BehaviorLaboratoryandStaff
Backrow:DanielReynolds,PearlMcFarland,DanielG.Freedman,DonaldDickerson,JohnA.King,DouglasG.Anger,DuaneBlume,EdnaDuBuis,FrankClark,SheldonIngalls,HoweSmith.
Middlerow:MaxineE.Schnitzer,MarianBurns,FlorenceSmith,MargaretCharlesHiggins.
Frontrow:ClarenceC.Little,JohnPaulScott.(JohnL.Fullerwasawayonleavewhenthispicturewastaken.)
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Someoffspringoftheancestralcockespanielsusedinthecross.
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Backcrosstothecockerspaniel,litter2249-57.Notecocker-likeearsandsegregation
oflongandshorthair.Theseandfollowingpicturesofhybridswerealltakenat16weeksofage.
Backcrosstothebasenji,litter3301-06.Noteuniformshorthair,theresultofadominantgene,andbasenji-likeappearanceofsomeanimals.
PilOTUI
CSBF2litter3394-3400.Noneofthe72puppiesinthetotalF2populationshowedanexactresemblancetoeitherparentbreed.
Pygmiesreturningfromahuntingtripwithabasenji.Thenetsareusedtotrapgamesuchasthesmallantelopescarriedbvthehunters.Thebasenjirunswiththemastheybeatthebrush,andthebellarounditsneckhelpstofrightenthegame(bypermissionoftheAmericanMuseumofNaturalHistory).
HuntingpartyatNinevah,Iraq,1952.TheirthreedogsbelongtothebreedfromwhichtheEuropean,greyhoundswereprobablydeihed,beingbroughtbackbyCrusaders(photobyR.T.Hatt).Thesalukiisabreedde-velopedfromthesamesourceinmoderntimes.
Left:MalepurebreddingoinAustralia(photobyDr.X.W.G.Mcintosh).Xotegeneralsimilaritytothebasenji.Right:Kurdishguarddog.Iraq,1952.Notestronglycurledtail.Animalssuchasthiswereusedinancienttimesaswardogs,aswellasforguardingflocksandproperty(photobyR.T.Hatt).
Forcedtraining
Above,apuppyistaughttoremainonthescaleswhileweighed,startingatbirth.Thepuppyinthepictureisonlytwoweeksofage.
Left,theleashcontroltest.Abalkatthestairs.
Basicrewardtraining
Goal-orientationtest.Uponreleasefromthestartbox,thepuppylearnstoruntothedishoffoodinitsownpen.
Advancedrewardtraining
Motor-skilltest.Inthis,themostdifficultpartofthetest,thedogmustclimbthe
Motor-skilltest.Inthis,themostdifficultpartofthetest,thedogmustclimbtheramptoadishoffoodontopofboxes5feethigh.
Detourtest(firstbarriertest).Inthisfirstproblem-solvingexperience,thepuppymustgoawayfromthegoalonthefarsideofthebarrierinordertoreachit.
Manipulationtest.Thepuppymustgetthedishoutofthebo:withhisDawsorteethinordertoeat.
Mazetest.Apuppyapproachestheexitthefoodreward.
T-Mazeanddelayed-responsetest.Onlydoorleadstoanexit.Inthedelayed-respitest,thepuppymustrememberaprevsignal.
Trailingtest.Puppylearnstofollowanartificialtrail.Asingledropoffishjuiceisplacedoneachmetalplate;thetrailendswithasmalldishoffish.
Spatial-orientationtest.Onlytherighthandrampleadstothegoal.Arrangementofthegoalboxandrampsisalteredineachpartofthetest.
encyrelationship.AsseeninFigures5.9and5.10,thesescoresrisequiterapidlyandthenleveloff.Byoneyearofagetheyhavedecreasedconsiderably,indicatingthattheanimalsarenowmoreindependent.
Anothermeasureofdependencyisthe"followingtest,"alreadydescribedin
Anothermeasureofdependencyisthe"followingtest,"alreadydescribedinconnectionwiththemother-offspringrelationship.Thetimespentclosetoahumanhandlervariedagreatdealamongindividualpuppies,butthereareaveragebreeddifferences.Cockers,forexample,spendmoretimeclosetothehandlerthandobasenjisontheaverage,althoughsomeoftheindividualdogsspendingthemosttimewiththehandlerwerebasenjis(Fig.6.5).
Formostofthedogs,beingremovedfromthepensandtestedwasarewardingexperience.Wheneverahandlerappearedatthegate,thepuppieswouldswarmtowardhim,attemptingtogetout.Inmostoftheteststheyobtainedbothafoodrewardandtheopportunitytomoveintoanewenvironment,andtheypresumablyassociatedtheexperimenterswiththeserewardingexperiences.Wemadecertainspecialexperimentsinanattempttoanalyzethisrelationshipinmoredetail.
Thefirstoftheseexperimentswasastudyoftheeffectoffeeding.Foodrewards,whichcanbeusedsoeffectivelytomotivatelearnedbehavior,mighthaveapowerfuleffectonsocialrelationshipsandtheattractionofananimaltowardthosewhofedit.Thefactsdonotbearthisout.Mostoftheregularfeedingwasdonebyanimalcaretakers.Thepuppieswereintenselyinterestedinthematfeedingtimebutlostallinterestassoonasfeedingwasoverandpaidlittleattentiontothemthereafter.And,aswesawinthelastchapter,puppieswhicharemachinefedbecomejustasattachedtopeopleasthosewhicharehandfed.Inshort,apuppywhichismerelyfedregularlybyhandandgivennootherattentiondevelopslittlemorerelationshipwiththefeederthanhewouldwithafeedingmachine.
Wecanconcludethatfeedingitselfisaminorpartofthecare-dependencyrelationship.Thisdoesnotmeanthatfoodcouldnotbecomeanimportantpart,particularlyiffoodwasmadeconditionaloncertainacts,andsometimesgivenandsometimeswithheld.Butitdoeslookasifthemereactoffeedingdoesnotproduceastrongemotionalreaction.Ineverydaylanguage,apuppydoesnotautomaticallyloveyoubecauseyoufeedit.
However,ElliotandKing(1960)didadifferentsortofexperimentinwhichtheyregularlyhandfedagroupofpuppiesbutmadenoothercontactwiththem.Halfthepuppieswereunderfedandhalfwereoverfed.Thepuppieswerefedtwiceadayafterbeing
weanedat4weeksofage,andsoonbecamestronglyinterestedinfoodastheirregularmealtimesapproached,runningtothegateandwhiningrepeatedly.At5
regularmealtimesapproached,runningtothegateandwhiningrepeatedly.At5weeksofage,theunderfedandoverfeddogsshowednodifferenceswhengiventhehandlingtest.At6and7weeksofage,however,theunderfedpuppiesshowedlessavoidanceandmoreattraction,thedifferencesbeingsignificantatthe.01level.Bothgroupsweremoreafraidofastrangehandlerthanofthepersonwhoregularlyfedthembutexhibitedthesamedifferencesinreactiontoeitherhandler.Astheygrewolderthesameaveragedifferencespersistedbutwerenolongerstatisticallysignificant.Wecaninterprettheseresultsasmeaningthatmakingthepuppieshungryspeedsuptheprocessofprimarysocialization(i.e.,theformationofasocialrelationshipwithhumanhandlers),althoughtheoverfedpuppiestendtoeventuallycatchupwiththeotherswithoutthespecialimpetusofhunger.
Allthepuppiesinthisexperimentexhibitedanotherinterestingaspectofbehavior,inthatneitherexperimentalsnorcontrolsdevelopedasocialrelationshipwithhandlersasrapidlyaspuppiesintheregular"schoolfordogs,"wheretheyweregivenmuchhumancontactinadditiontofeeding.Wemavconcludethathandfeedinghasadefiniteeffectonthedevelopmentofthesocialrelationshipbetweenpuppiesandpeople,particularlvifthepuppiesareunusuallyhungry,butthattherelationshipwillalsodevelopnormallywithoutfeedingbeinginvolved.Thisagreeswithourknowledgethatstrongrelationshipsdevelopbetweenlittermatesinspiteofthefactthatonelittermateneverfeedsanotherbutinsteadoftencompeteswithhimforfood.
Relationshipsofhome-reareddogs.—Morelightisthrownontheoriginofprimarysocialrelationshipsbvourexperimentwithhomereareddogs.Thiscouldbedoneononlvavervsmallnumberofanimals,sothatgeneralconclusionsareimpossible.Eachpuppywastakenfromthelitterat4weeksofageandraisedinthehomeofastaffmember.Eachhomewassomewhatdifferentfromtheothertwo.Silver,theShetlandsheepdog,Livedinahousewithtwosmallboysandatomcat.George,thebeagle,livedwithayoungmarriedcouplewhohadnochildrenbutdidhaveacat.Gyp,thebasenji,wenttoahomewheretherewasalreadyanadultfemaledogandseveralsmallchildren.Allthefamilieswerefondofpetsbutdifferedsomewhatintheirideasofdog-rearinganddiscipline.
Thepuppieslivedtheordinarylivesofhouseholdpets,exceptthattheywncfrequentlytakenbacktothelaboratoryandtested.Whilethere,theywerekeptapartfromotherdogsandmightspendall
SOCIALRELATIONSHIPS179
daybythemselvesbeforetheywerereturnedtotheirhomes.Aswesawfromotherexperiments,isolationisanunpleasantexperienceforapuppy,andoverandoveragaintheyhadtheexperienceofbeingplacedinanunpleasantemotionalsituationandeventuallyrescuedfromit.Wewouldexpectthatthesepuppieswouldhavestrongemotionalreactionsassociatedwithhumanbeings.
Ingeneralthesepuppiesweremorefreeandconfidentwithhumanbeingsthanthekennel-reareddogs.Ontheteststheysometimesdidbetter,particularlywhenwiderexperiencemightbeofsomeassistance,buttheyalsodidworseinsometestswhichwerebasedonthekennelexperience.
Themoststrikingresultwasthedifferenceinadultbehavior.Twoofthepuppiesbecameextremelydependentandhighlyattachedtopeople.Oneoftheusualproblemsofraisingapetbeagleisitstendencytogooffhuntingforhoursatatime,neverreturningtothehouse.George,thebeagle,wouldscarcelyleavehisowners'yard.Silver,theShetlandsheepdog,wasinstantlyresponsivetohumanbehaviorandeasilytrained,eitherpositivelyornegatively.Hedefendedhisyardagainstallstrangedogs,bothmaleandfemale.Hebecamesexuallyresponsivetothecatwithwhichhewasbroughtup,whilethebeaglebecameattachedtotheclothbagofavacuumcleaner.Ontheotherhand,Gyp,thebasenji,becamemoreandmoreindependent,roamingthestreetsandfightingwithotherdogs.Perfectlybehavedinthelaboratory,hebecamealmostacaninedelinquentathomeandeventuallybecameuncontrollable.
Althoughtheenvironmentwasnotuniformforthesethreeanimals,thesamegeneraltreatmentproducedintwoofthedogsaconditionofoverdependencyandalackofmaturity,buthadrelativelylittleeffectontheother.Thebasenjibecame,asadog,anormallyindependentanimal;asapet,hewasoverlyindependentanddifficulttocontrol.Thebeagleandsheltiedevelopedamuchricheranddeeperrelationshipwithhumanbeingsthandidthekenneldogs,whereasthebasenjiwasmuchlessaffected,possiblybecauseofcontactwithanotherdoginthehomeaswellashisdifferentheredity.
Theeffectofhomerearingonthebehaviorofthesethreedogscanbedeterminedbycomparingtheirtestrecordswiththoseofothermembersofthesamebreedasdistributedonthestaninescales.Asmightbeexpected,themostobviouseffectwasontherelationshiptoahumanhandler.Thehome-reareddogswerealllessfearfulandshowedmoreplayfulaggressivebehaviorand
dogswerealllessfearfulandshowedmoreplayfulaggressivebehaviorandmoreevidenceofattractionduringthehandlingtests.Gyp,thebasenji,was
180BEHAVIORPATTERNS
anunusuallyconfidentdogat5weeksofage;andSilver,theShetlandsheepdog,showedanunusualamountofattractiontohumanhandlersat13to15weeksofage.Boththesescoresweremorethantwotimesthestandarddeviationawayfromtheaverageoftheirrespectivebreeds.
Similareffectsshowedupinthereactivitytests.Thepetsweremoreactive,stoodmoreerect,andshowedmoretendencytoinvestigatetheirsurroundings.Alltheseresultsareconsistentwiththeinterpretationofananimalwhichisconfidentinstrangesurroundings.Onepeculiaritywasthatallofthemshowedmoremusculartremorthantheaverageinreactiontorestraintinastrangeplace.Ontheperformancetests,alltheanimalsdidbetteronthefirstbarriertestgivenat3weeksofage,whereconfidenceinastrangesituationundoubtedlyhasastrongeffectontheoutcome.Inover-allperformance,thebasenjiscoredbetterthanaverageonfiveperformancetests,poorerthanaverageinone,andaverageinfourmore.Hedidoutstandinglybetterthanotherbasenjisinthetrailingtest.
Thebeaglewasbetterinthreetests,worseintwo,andaverageinfive,confirmingtheimpressionofhisownersthathewasadogofquiteaverageintelligence.Hedidoutstandinglywellontheleash-controltest,butthisprobablyreflectsprevioushometraining.
TheShetlandsheepdogdidbetteronfourtests,poorerinone,andaverageinfive,turninginoutstandingperformancesonthefirstbarriertestandonthetrailingtest.Thebehaviorofalldogsonthelasttwotestswereapparentlygreatlyaffectedbytheirreactionstostrangesituations.Thesheepdogshowedaslowerthanaverageperformanceonspeedscoresintwoofthetests,reflectingthefactthatthisanimalbecameobeseasitgrewolderandcouldnotrunasfastastheothers.
Thehomeenvironmentchieflyaffectedtherelationshipofthedogswithpeopleandtheirconfidenceinstrangesituations,andthisenabledthemtodobetterthantheaverageincertaintestsinwhichthiswasimportant.Theiradditionaloutsidetrainingandexperiencewithricherenvironmentsbenefitedtheminsomeothertestsbutdidnotmaketheminto"superdogs."
CONCLUSIONS
CONCLUSIONS
The1mostimportantconclusionthatranbedrawnfromtheseexperimentsisthathereditydoeshaveanimportanteffectuponthedevelopmentofsocialrelationships.Involving,asitdoes,aprocess
ofmutualadaptationandlearning,theexpressionofheredityinasocialrelationshipisfarremovedfromtheprimarybiochemicalactionofagene.Nevertheless,theendresultcanbeexpressedinasimplestatementthatthedifferentiationofbehaviorinasocialrelationshipisproportionaltothedifferencesinthecapacitiesofthetwoindividualsinvolved.Inthecaseofthedominance-subordinationrelationshipdevelopedbetweenyoungpuppies,theoutcomeisaffectedbybothsexandbreeddifferencesinthecapacitytodevelopaggressivebehavior.Theseexperimentshavemanyotherimplications,andtheywillbediscussedingreaterdetailinthefinalchapter.
Whilewewereabletoworkwithonlyalimitednumberofmothers,therewereobviousindividualdifferencesintheirbehaviortowardtheiroffspring.Verypossiblyalargersamplewouldshowthattherewereimportantbreeddifferencesinmaternalbehavior.Oneinterestingfactwasthatthehybridmothers,whichgavemoremilkthanpurebredones,spentlesstimenursingtheiroffspring,suggestingthatthemotherstendedtoallowtheiroffspringtonurseaslongasthepuppieskeptsucking.Thereisagreatdeclineintheamountoftimespentinnursingduringtheneonatalperiod;sothatbythetimethepuppiesentertheperiodofsocialization,nursingisaquickandcasualaffair.
Aswellasdifferencesinmaternalcare,therearebreeddifferencesinthereactionsoftheoffspring.Thissuggeststhepossibilitythatpartofthebehaviorwhichweconsidercharacteristicofabreedmaybeareflectionofthesocialenvironment,i.e.,thebehaviorofmothersandlittermates.Inthecaseofsocialbehavior,geneticfactorsmayinpartcreatetheirownenvironmentwhichinturnmodifiestheirdevelopmentandexpression.
Incontrasttothedog-dogrelationships,whichwereallowedtodevelopfreely,thedevelopmentofdog-humanrelationshipswasmorestrictlycontrolled.Asfaraspossible,thehumanhandlerstreatedeachpuppyinthesameway.Theycontrolledandstimulatedthebehaviorofthedogsbutrespondedtotheminonlyalimitedway,sothatthepuppiescouldcontrolhumanbehaviortoonlyaverysmallextent.Theresultwasarelativelyshallowsocialrelationshipcomparedtothedeeperandmorecomplicatedrelationshipwhichhousedogsordinarilydevelopwiththeirmasters.
developwiththeirmasters.
Wewereabletocomparetheeffectsofnormalhomerearinginthecaseofthreedogs.Theprincipaleffectwastomakethemmoreconfidentinthepresenceofpeople,andthisinturnaffectedtheirperformancewhereconfidencewasneeded.Basenjishaveatendencytobeafraidofstrangeobjectsandapparatus,andthemore
confidenthome-rearedbasenjididmuchbetterinthetrailingtest,inwhichsuchfearswerearealhandicaptoperformance.Otherwise,homerearingseemedtohelptheanimalsintestswherewiderexperiencewasofvalueandtohandicapthemwherekennelexperiencewasimportant.Wealsohadtheimpressionthatthethreehome-reareddogshadmorehighlydifferentiatedbehaviorasindividualsthandidthoserearedinakennel.Thisundoubtedlyresultedinpartfromdifferentialamountsoftrainingbutalsosuggeststhepossibilitythatpartofwhatweconsiderthecharacteristicbehaviorofdogbreedsisdevelopedandexaggeratedbydifferentialtreatment.
Thuswereachthegeneralconclusionthatthecourseofdevelopmentofsocialrelationshipsisdeterminedbygeneticdifferencesbetweentheindividualsinvolvedandbythenatureofthesocialenvironment.Socialrelationshipsinturninfluencealmostallotherbehaviorandaretheframeworkwithinwhichalltestsofperformancetakeplace.
Precedingchaptershavedealtwithbasicinformation:theoriginofdogs,theirbasicpatternsofbehavior,andthebroadoutlinesofbehavioraldevelopment.Thenextsectionwillemphasizethedevelopmentandanalysisofbreeddifferencesinperformance,includingthecapacitytoaccepttrainingandtosolveproblems,andthedependenceofeachoftheseuponbasicphysiological,emotional,andanatomicalcharacteristics.
THEDEVELOPMENT
ANDEXPRESSION
OFBREEDDIFFERENCES
ANALYSISOFGENETICDIFFERENCES
Beforepresentingtheresultsofthegeneticstudiesitisnecessarytoexplainscoringsystemsandmethodsofstatisticalanalysis.Forthemostpart,ourprocedureswereconventional,butsomeexplanationofthegeneticsignificanceofourresultsisnecessaryforpersonsmorefamiliarwithbehaviorthanwithbiometricalgenetics.Itwillbecomeclearthat,althoughstatisticalanalysisisessentialforaninterpretationofourfindings,itisnotsufficientinitself.Toagreatextent,theinternalconsistencyofthedatamustbeconsideredinarrivingatconclusions.Inanexperimentinvolvingsomanyvariables,numerousbreeddifferencesthataresignificantattheconventional5percentlevelwouldbeexpectedbychance.The1percentlevelofsignificanceisprobablyasaferboundaryinmultivariatecomparisons.
Furthermore,quantitativeestimatesoftheheritabilityofatraitdependuponclearseparationofgeneticandenvironmentalsourcesofvariance.Purebreedsofdogsareappreciablyheterogeneousinmanyrespects;hence,thewithin-breedcomponentofvarianceisareflectionofgeneticaswellasenvironmentaldifferencesamongmembersofthesamebreed.Frequentlythevariancebetweenbreedswasconsiderablygreaterthanthatwithinbreeds;andonoccasionweusedthebetween-breedvariancecomponentasanestimateofgeneticeffects.Heterogeneityinthebreedscausesthebetween-breedvariancetogiveunderestimatesofthetotaleffectofheredity.
Theuseofbetween-breedvarianceasameasureofgeneticeffectsassumestheessentialsimilarityoftheenvironmentsofthedifferentbreeds.Inpracticethereweresystematicdifferences.Forexample,basenjipupsdevelopedinabasenjiuterus,andfor70daysafterbirthwerenursedandcaredforbyabasenjimother.Fortheirentire
185
186BREEDDIFFERENCES
periodofobservationtheylivedwiththeirbasenjilittermates,notwithcockerspanielsorbeagles.Bycross-fostering,byrearinginmixed-breedgroups,orbyrearinginisolation,itwouldhavebeenpossibletoisolatetheeffectsofdifferentialsocialenvironmentatvariousstagesoflife.Pilotstudiesofeachtypewere,infact,carriedout,butnotonascalelargeenoughtopermitdetailedstatisticalanalysis.Theoutcomesofallsuchexperimentswereconsistent;breedcharacteristicspersistedincross-fosteredpups,inisolation-rearedpups,andinpupstransferredaftersomeweeksormonthstoalitterofadifferentbreed.Becauseoftheseconsistentresults,webelievethatgeneticcontributionstobreeddifferencesovershadowenvironmentalcontributions.
Geneticheterogeneitywithinparentstockswouldtendtolowerestimatesofheritability,whilesystematicenvironmentaleffectswouldraisethem.Becausethetwopotentialsourcesoferrorworkinoppositedirections,wemayhopethataroughbalancewasattained.Beforeproceedingwithamoredetaileddiscussionofourmethodsofanalysis,wewilldescribethestaninesystemofscalingquantitativescores(Guilford,1950).
STANINESCORINGSYSTEM
Thescoresofoursubjectswereexpressedindiverseunitssuchaserrors,runningtimesinseconds,orarbitrarynumericalratingsderivedfromadescriptivescale.Thesescoreshavemeaningonlyinsofarastheyarerelatedtoaparticulartestingprocedure.Inordertomakedifferentsetsofscorescomparable,wehaveconvertedmanyofthetestresultstostanines.Inthissystemallscoresaredividedintoninegroupsbaseduponrankorderingandeachgroupofscoresisrepresentedbyasingledigit.Theconversionischosensothatthemeanofthescoresforthereferencepopulationiscloseto5.0andthestandarddeviationisabout2.0.Thusascoreof5.0indicatesthatthesubjectwasbetweenlimitsof±0.25standarddeviationsfromthemeanofthetransformed
betweenlimitsof±0.25standarddeviationsfromthemeanofthetransformedscores.Themeanofthetransformedscores,ofcourse,correspondstothemedianoftheoriginalscores.
Transformationofscoreshasanumberofadvantages.Intervalsonthestaninescaleare,inasense,uniformthroughouttherangeofscoreswithinaparticularpopulation.ThissatementisnottrueFormanyoitheoriginalscores.Forexample,inonetestinvolvingrunning-timesubjectsrunningatfullspeedcouldcoverthecourse
ANALYSISOFGENETICDIFFERENCES187
in2seconds.Ananimalaveraging4secondswasclearlyrunningmuchbelowmaximumspeed,andthedifferencebetween2-secondand4-secondsubjectswassignificant.Somedogsremainedwithintheapparatuslongafterthegatehadbeenopened,andtheirrecordedrunningtimesaveraged20secondsormore.Undertheseconditions,thedifferencebetween20and22secondswasnotcomparabletothatbetween2and4seconds.Conversionstoreciprocalsortologarithmsmighthavebeensatisfactory,butweselectedatransformationbasedonrankorderingasmoregenerallyapplicabletoalltypesofscores.
Thestanineconversionmakesitpossibletocompareperformancesinquitedifferenttests.Astaninescoreof7,forexample,alwaysmeansthatthesubjectwasbetween0.75and1.25standarddeviationsabovethemeanonthetransformedscale.Theoriginalscoresmayhavebeenrunningtimesorratingsofemotionality,butsuchdifferencesdonotaltertheprocedureofrankingwhichisthebasisofthetransformation.Staninesarealsoadvantageousforcomputations,particularlywhendeskcalculatorsmustbeemployed.Avarietyofanalysescanbeconductedmoreeasilyonscoresexpressedassingledigits.
Therearealsocertaindrawbacks.Thedisadvantageoftransformingdatainthiswayisthatitmayobscureordistortinformationwhichisobviousontheoriginalscale,orwhichcouldbebroughtoutmoreplainlybyusinganothertransformation.AsMather(1949)haspointedout,thereisnoapriorireasonforassumingthatonescalewillappropriatelymeasuretheeffectsofeverygene.Consequentlythestaninescalemayincertaincasesobscureprecisemeasurementsofbehavioraldifferencesandindicationsofgeneticsegregation.Theadvantagesofthemethod,however,outweighitsdrawbacks,particularlyifmanycomputationsmustbemade.
Theuseofstaninescarriestheimplicationthatthetraitsmeasuredbyourscoresareessentiallycontinuousratherthandiscontinuous,andthatthebasesampleusedtocomputethetransformationtableswasarepresentativesampleofthepopulationinwhichwewereinterested.Specifically,thismeansthatweassumethatdogsarenotdividedintobrightanddulloremotionalandnon-emotionalclasses,butthatintelligenceandemotionalityasmeasuredbyourtestsarequantitativecharacterswiththemajorityofthepopulationintermediateandrelativelyfewsubjectsattheextremes.Further,wehaveassumedthatthefivebreedschosenforstudyrepresentafaircross-sectionofdogs.Althoughtheseassumptionswerenotstrictly
BREEDDIFFERENCES
proved,thedistributionsofthetestscoresareingeneralagreementwiththem.Stanineconversionswerenotmadeonscoreswhosedistributionsobviouslycontradictedtheseassumptions.
Theprocedurefortransformingoriginalscoresintostaninesisillustratedbydatafromthemotivationtest.TheoriginalscorewasthetotaltimeinsecondsadogrequiredtoruntentrialsinonedaythroughanL-shapedcourse.Eachdogwastestedonthreeseparatedays,sothatthreescoreswereavailableforeverydog.Wechoseasampleof100dogs,10malesand10femalesfromeachofthefivepurebreeds,selectingatrandomwithineachbreedandsex.Thedistributionofthe300scoresisshowninFigure7.1.Thecurveis
RUNNINGTIME-MOTIVATION
MEDIAN
■—-*■-
300
400
500
SECONDS
Fig.7.1.—Distributionof296runningtimes(4scoresoffscaletoright)from100dogsgiven3trialseach.Thesamplingprocedureisdescribedinthetext.
markedlyskewed,butthereisnoevidenceofbimodalitywhichwouldjustifytheclassificationofsubjectsintofast-runningandslow-runningdogs.
Theoriginalscoreswerearrangedinrankorderandcut-offpointswereselectedatpointscorrespondingtocumulativepercentagesforsegmentsofanormaldistribution,one-halfastandarddeviationwide(Table7.1).Notethatthecumulationofscoreswasstartedfromtheslow-runningend,becausewewishedtoexpressourresultsintermsofspeedandthefastestsubjectshavethelowesttimescores.ThetransformationtostaninesshiftsthedistributionofscorestoanapproximatelynormalformasinFigure7.2.Wecan,there-
ANALYSISOFGENETICDIFFERENCES
TABLE7.1ConversionTable—OriginalScoretoStanine
fore,bytheuseofstanines,essentiallychangethebasisofmeasurementofanindividual'sbehaviorfromascalebasedonabsolutephysicalunitstoonebasedonperformanceofastandardpopulation.
60r
SPEE0MOTIVATION
3456789
STANINE
Fig.7.2.—Distributionof300motivation-speedscoresafterconversiontostanines.
ANALYSISOFVARIANCE
Analysisofvarianceseparatestheeffectsoftwoormorefactorsuponasetofmeasurements.Inourexperiments,themajorinterestlayinestimationofthecontributionofhereditytototalvariance.Totalvarianceisreadilyestimatedbystandardprocedures,andtodetermineheritabilityitisonlynecessarytofindsomemeansofcalcu-
190BREEDDIFFERENCES
latingthegeneticcomponent.Inpractice,thisissomewhatcomplex.Weshalldescribethesituationintheexperimentcomparingfivepurebreeds.
Inthisexperiment,potentiallygeneticcontributionscanappearinthreeforms:
1.Asystematiceffectbetweenbreedsmayappearbecauseofdifferencesingenefrequencybetweentheseveralbreeds.Weshalllabelthisvariance<t2hb.
2.Somegeneticvariationmaybeattributabletodifferencesingenotypesbetweenthevariousmatedpairsineachbreed.Weshalllabelthisvarianceo2hm.
3.Someofthevariationamongmembersofthesamesibshipisattributabletorandomsegregationintheoffspringofheterozygousparents.Wecallthis
randomsegregationintheoffspringofheterozygousparents.Wecallthisvariancecr2h.
Thedesignoftheexperimentdoesnotpermitseparationofcr2hfromenvironmentalvariance,butct2hbando2hmcanbeestimated,providedcertainassumptionsaremadewithrespecttoenvironmentaleffects.
Wecanalsosubdivideenvironmentallyproducedvariance.
1.Asystematicenvironmentaleffectcouldhavebeenproducedbytheassociationofpuppiesalmostexclusivelywiththeirownbreed.Thisvarianceweshalldescribeasct2eb.
2.Asimilarsystematicenvironmentaleffectcouldhavebeenassociatedwithaparticularmotherandwouldcharacterizeallmatingsofthismother.Thisvarianceweshallcallo2em.
3.Eachlitterhadaparticularanduniquelifehistorycharacterizedbyseasonofbirth,exposuretoaccidentalstimuli,testingbyaparticularresearchworker,etc.Thevarianceattributabletothesecommonlittereffectswewillcallct2el.
4.Eachsubjecthadcertainuniqueexperiences.Eventhoughweendeavoredtotreatallalike,absoluteuniformitywasnotpossible,andlittermateswerenot,ofcourse,boundbyanyexperimentaldesignintheirtreatmentofotherindividualsinthelitter.Variancedependentupontheseindividualexperientialdifferenceswedenoteaso2e.
Thecomplexityofsourcesofvariationissomewhatdiscouragingatfirst.Inalargeexperiment,itwouldtheoreticallybepossibletoisolateeachcomponent,althoughbiologicallimitationsonthenumberoflitterswhichasinglefemalecouldproducewouldinterferewitheventhebestpossibledesign.Ourexperimentwastoosmalltopermitdirectestimatesofallcomponents.Hence,wewereForcedtolooklordefensiblesimplifications.
Inthefirstplace,cross-fosteringfailedtodemonstratemajoreffects,andindividualsrearedinmixedlittersdidnotdiffermarkedlyfromtheirownbreed.Weconcludedthatindogs,<t2ebandct2emweretoosmallformeasurementinsmallsamples;hencetheywereneglectedinmostanalyses.Ineffect,suchansimplificationassumesthatculturaldifferencesbetweenbreedsarenotimportantdeterminantsofbehavioralvariation,althoughwelaterfoundevidencethat"breedenvironment"hasaneffectonsomeofthevariables(seechap.14).
"breedenvironment"hasaneffectonsomeofthevariables(seechap.14).
Theimportanceofct2elcanbetestedbydeterminingwhetherlittersofthesamematingdiffersignificantlyfromeachother.Whenthequestionisputtothedatatheanswerisnotstraightforward;theydoonsometestsbutnotonothers.Weconcludethatthecontrolofenvironmentfromlittertolitterwasimperfectinspiteofourbestefforts,andthatinanalysisweshouldtakeintoaccountbe-tween-littervariation.
Theseparationbetweencr2handcr>,bothcontributingtowithin-littervariance,isnotpossiblewiththedatafromthepurebreeds.Anestimateofthedistributionofthewithin-littervariancewas,however,possibleinthehybridizationexperiment.WecanbecertainherethattheF2andbackcrosshybridsweregeneticallymorediversethantheFi's,yetthewithin-littervariancesofbehavioralmeasureswerenotuniformlysmallerintheFi's.ThegeneticdiversityofthepurebredlitterswascertainlylessthanintheF2hybrids,andthegeneticcontributiontothevariancewithinsuchlittersmusthavebeenless.Thus,whenweassumethatthewithin-littervarianceofthepurebreedsisenvironmental,wemayunderestimatetotalgeneticeffectsforcharactersofhighheritability,buttheerrorisprobablytoosmalltobedetectableexceptinverylarge-scalestudies.
Finallywemustconsiderct2hbandAi,althoughourprimaryinterestisinct2hr.Byderivingourpurebredstocksfromafewcloselyrelatedindividuals,weendeavoredtoreducect2hmtoalowvalue.Wecanomitseparatecalculationofbetween-matingvarianceandincludeitwithbetween-littervariance.Insodoing,somegeneticcomponentswillbeincorrectlyclassedasenvironmental,andtheeffectwillbetoreducetheprobabilityoffindingsignificantbreeddifferencesandsoleadtoaconservativeestimate.Inanticipationweshallnotethatthisanalysisprovedsuitableforthebreedcomparisons.Amongthehybrids(seechaps.12and14)ratherlargedifferenceswerefoundamongmatingsofthesametype.
Insummary,asurveyofthesourcesofvariationinourexperi-
BREEDDIFFERENCES
mentleadstothefollowingsimplifiedschemaofanalysisforasampleofbbreeds,eachmadeupof/littersofkindividuals(Table7.2).
TABLE7.2
TABLE7.2
SimplifiedInterpretationofAnalysisofVarianceinBreedComparisonExperiment
Practicalcomputationsmusttakeintoaccountinequalitiesinthevarioussubgroups.
Inthisschema,threehierarchialmeansquaresarecomputedbetweenbreeds,litters,andindividuals.Thevariancebetweenindividualsofthesamelitterisameasureoftheeffectofnon-controlledenvironmentalandgeneticfactors.Themeansquareforlittersalsoincludesacomponentwhichweinterpretaspredominantlytheeffectofspecific-litterlifehistories.Anygeneticdifferencesinmatingsofthesamebreedwillalsobeincluded.Ifbetween-littereffectsarenon-significant,thenthewithin-littermeansquare(estimateof<r2h+o2e)isthepropertermfortheFtestofbreeddifferences.
Ifthebetween-littereffectissignificant,thentheproperdenominatorfortheFtestofbreedeffectsisthemeansquareforlitters(estimateof<r2e+o2h+kcr2EL).Obviously,thistestismorerigorousthanasimplecomparisonofbreeddifferenceswhichneglectspecific-littereffects,anditismoredifficulttoestablishsignificance.Becausetheprocedureisconservative,morefaithcanbeplacedonit.
Theratioofothbtototalvariance(o2h+or2e+o*bl+<r2ns)isknownastheintraclasscorrelationcoefficientandisperhapsthemostgenerallyusefulindexofthemagnitudeoftheeffectsofheredity.Acorrelationof.25,forexample,meansthatone-fourthofthetotalvarianceofapopulationdrawnatrandomfromthetotalsamplewouldbecluetobreeddifferences.Anotherintraclasscorrelationcanbecomputedforthelittereffect{ctel/cTc+cr'2h-fo2el)whichistheproportionofvariancewithinabreedattributabletospecific-litterhistories.Bothmeasureshaveprovedusefulinouranalyses.
Themostgenera]applicationsofthisbasictheoryarepresentedinchapter14inconnectionwithanover-allanalysisofvariationin
ANALYSISOFGENETICDIFFERENCES193
thepurebreedsandhybrids.Chapters8to10areconcernedwiththeanalysisofbreeddifferencesandtherelativeranksofthepurebreedsinvariouscapacities,whereaschapters11,12,and13areconcernedwiththeanalysisoftheresults
whereaschapters11,12,and13areconcernedwiththeanalysisoftheresultswithhybrids.
Moredetailedstatisticaltechniquesaredescribedandtheirapplicationdiscussedinseveralofthesechapters.Theanalysisofvariancemethodcanbeextendedtoincludedetailedanalysisofenvironmentaleffects.Elliotcarriedoutanelaborateanalysisofthissortuponthesecondbarrier(ormaze)test,whichisdescribedinchapter10.
Inchapter11,methodsaredescribedforestimatingthenumbersofgeneticfactorsinvolvedinaparticulartrait.Chapter12includesmethodsforusingoffspring-parentregressionsandfortheanalysisofhalf-sibandfull-sibfamilies.Thedesignofourcrossbreedingexperimentwassuchthatthesamepurebredfemalewasbredtotwodifferentmales,oneoftheotherpurebreed,andonebeingherownson.Thissamesonwasbredtotwogeneticallydifferentfemales,themotherandafullsister.Thismakesitpossibletocompareanimalshavingoneparentincommonandthustoestimatetheeffectsoftheparents.Thismethod,incontrasttothemoregeneralonedescribedabove,makesitpossibletoanalyzetheeffectsofhereditywithoutassuminghomogeneityoftheparentbreeds.
Finally,thewell-knowntechniqueoffactoranalysiswasappliedtotheresultsonthreedifferentoccasions,andthefindingsaredescribedinchapters13and14.Theassumptionsandlimitationsdiscussedaboveapplytoallproceduresemployed.Despitethecomplexityofthefactorsaffectingbehaviorandtheelaboratenatureofthestatisticaltechniquesrequiredfortheiranalysis,onebasicresultclearlyemerged:largeeffectsattributabletoheredityweredemonstratedinalmosteverytestweadministered.
CHAPTER8
EMOTIONALREACTIVITY
TheworkofHall(1941),Searle(1949),andothersonthegeneticsofratbehaviorindicatednotonlythatemotionalbehaviorwasaffectedbyheredity,butthatemotionalityhadanimportanteffectonperformancetests.Inourdogswethereforestudiedtheearlydevelopmentofsuchemotionalreactionsasdistressvocalizationandtailwagging,andparticularlythechangesinemotionalreactionsinresponsetohumanbeingsduringtheprocessofsocialization.Importantbreeddifferenceswerefoundinallthesecharacteristics.
Inadditiontotheirovertexpression,emotionsalsoincludeinternalresponseswhichcanbemeasuredbywell-knownphysiologicaltechniques.Thesetechniquesaremosteasilyappliedtolargeranimalsunderrestraint,andwethereforeplannedamajortestoftheemotionalandphysiologicalreactionsofolderpuppiesandgrowndogsastheystoodonaPavlovstand.Wehopedtodefinetheeffectofheredityuponexternalandinternalemotionalreactivity.
Reactivityisabroadtermwhichmayhaveseveralmeanings.Wedefinedreactivityastheintensityofallresponses,externalandinternal,madetoastimuluschange.Suchabroaddefinitioncreatessomeproblemsofmeasurement,sincethevariouspossibleresponsesdonotnecessarilyvarytogether.Nevertheless,theconceptseemstohavevalidityfromthepointofviewofgenetics.
DEVELOPMENTOFAREACTIVITYTEST
Apparatus.—Inordertoreducethereactivitymeasurementstomanageableproportionsandtofacilitatephysiologicalmeasure-
ments,subjectswererestraineduponaPavlovstand.Heretheywereexposedtoastandardsetofsituationsdesignedtoelicitanemotionalresponse.Sincewewereinterestedinobservingphysiologicalcorrelatesofreactivitv,weconnectedoursubjectstoanoscillograph,usingmodifiedbatteryclipsassurfaceelectrodes.Topreventthemfrompullingtheclipsoffortanglingthewires,dogswerelightlvrestrainedbylegloopswhichweretiedovertheirbacksandconnectedtoasteelbarabout4.5feetabovethefloor.Thesupportingframeforthisbarwasbuiltintoalargecage8X8X7feetwhichwascoveredwithscreenwireforelectricalshielding.Observersandrecordingequipmentwerestationedjustoutsidethecageinthesameroom.
Behaviorinthetestsituation.—Withinthiscageweobservedtheresponsesofthepurebredandhybriddogstoaseriesofsocialandnon-socialepisodes.Theresponseswereobviouslymodifiedbytheconditionsoftesting,andreactivitymeasuredinanothersituationmighthavetakenverydifferentforms.Themajorityofsubjectstoleratedtheattachmentofelectrodesandthefittingoflegloopswithanominaldisplayofexcitement.Goodvisualobservationsandoscillographrecordscouldbeobtainedfromsuchanimals.Afewsubjectsreactedsoviolentlytosimplerestrictionofmovementthattestinghadtobediscontinuedorcarriedoutinamodifiedform.Evenmorecommonweredogswhichslumpeddownintheharnessandweresoinhibitedthroughoutthatlittle
whichslumpeddownintheharnessandweresoinhibitedthroughoutthatlittledifferentiationofreactivitywasdetectablefromepisodetoepisode.ThesetwotypescorrespondedtoPavlov's(1928-41)"excitable"and"inhibited"animals,whichhetestedundersimilarconditions.Betweenthesetwoclasses,therewasanenormousrangeofvariability.Theextremepatternsappearedtobemoreareactiontothetestsituationasawholethantoitsspecificcomponents.
Ageoftesting;observervariation.—Asastandardprocedureeachsubjectwastestedatthreeages:17,34,and51weeks.Atthetimeofthefirsttestthedogshadjustbeenplacedinanoutsideyard;at34weekstheyhadcompletedthemajorbehavioraltestswiththeexceptionofspatialorientation.The51-weektestcameafterapproximately12weeksoflivingintheoutsideyardswithaminimumofhumanhandling.Inthesethreeteststheeffectsofchangesinage,previoustestexperience,andcurrentconditionsofmaintenanceandhandlingarecombined.Itwouldhavebeenpossibletodesignanexperimenttoseparatetheseeffects,butthiswouldhaveinvolvedmoresubjectsthanwereavailableandwouldnotneces-
196BREEDDIFFERENCES
sarilyhavegivenmoreinformationregardingbreeddifferences,sinceallbreedsweretreatedalike.
Overthecourseoftheexperimentchangesinpersonneloccurred,thusintroducingproblemsofvariationbetweentheratingsofindividualobservers.Toreducethissourceoferror,eachnewobserverwastrainedbvtheprincipalinvestigatoruntilratingswerejudgedtobereasonablvuniform.Asampleofcorrelationsbetweenobserverratingsonthesamesubjectvariedbetween.85and.95.
Episodesinthereactivitytest.—Thereactivitytestwasdividedintotenepisodes:(1)Preparation.Duringthisperiodofvariabledurationtheexperimenterattachedelectrodesandadjustedtherestrainingloops.(2)ControlI.Thesubjectwasleftaloneforoneminuteinanelectricallyshieldedcubicle,lightedfromtheinside.Anobserverviewedthesubjectfromthesidethroughascreenwhichblurredbutdidnotobscurethedog'sviewtotheoutside.(3)Quieting.Anexperimenterentered,spokesoftlytothesubjectwhileextendinghishand,walkedtotherearofthecubicle,andleftquietlyafter30seconds.(4)ControlII.ArepetitionofControlI.(5)Bell.Adoorbellattachedtothecubiclewallwassoundedfor30seconds,followedby(6)ControlIII.AnotherrepetitionofControlI.(7)Shock.Foursingleshocksfromaninductioncoilweredelivered
ofControlI.(7)Shock.Foursingleshocksfromaninductioncoilweredeliveredtothedog'sleftforelegat5-secondintervalsandobserva-tionswerecontinuedfor60secondsfollowingthefirstshock.(8)Threatening.Anexperimenterenteredthecubicle,graspedthedog'smuzzlewhilespeakinginaloudharshvoice,andforcedthesubject'sheadfromsidetoside.Inaddition,itwasoftennecessarvtountangleloopsorre-attachelectrodeswhichweredislodgedduringtheshockperiod.Allsuchhandlingwasdoneinabrusquemanner.(9)ControlIV.RepetitionofControlI.(10)Release.Afterreleasingthedogfromthelegloops,theexperimenterremainedstandinginthecubiclefor30seconds,thensteppedoutsideandwaitedbvthedoorforanadditional0.5minute.Latencyofthedog'sleavingthecubiclewasrecordedtothenearestsecond.
Ratingscales.—Ratingsofbehaviorweremadeineachofthe10episodeswithastandardchecklist.Eachspecificbehaviorpatternwasratedona5-pointscale,thehighervaluescorresponding
greaterenergyexpenditure.Exceptionsweremadeforsuchcate-
goriesasaggression(biting)whichwasscorednolowerthan4or
sionappearedonlywhensubjectsweremoreactive
thanav<Someitochaspostureandtailcarriage,were
ratedineachepisode;others,suchastailwaggingorvocalization,
EMOTIONALREACTIVITY
197
onlvinthoseepisodesinwhichsucharesponsewasobserved.Withthisratingsystem,thetotalscoreisameasureoftheaveragevigorofallformsofresponseover10episodes.DetailsofscoringareavailableinScottandFuller(1950).
Inaddition,graphicrecordsofrespiration,electrocardiogram,andelectromvogram(recordedfromthethigh)wereavailableforallexceptthepreparationandreleaseepisodes.Therespiratoryratedatahavenotvetbeenanalyzedcompletely.Heartratechangesfromepisodetoepisodewerenoted,aswellastheheartratesundercontrolconditionsandanindexofsinusarrhythmia.Anarrhythmicheartwouldslowdownandseemtoalmoststop,thenspeedupforafewbeats.Theelectromyogramswereratedona5-pointscalebycomparingthemtoasetofstandardrecordsrankedfromextremerelaxationto
comparingthemtoasetofstandardrecordsrankedfromextremerelaxationtoviolenttremor.
Whenpossible,ratingswereconvertedtostaninestofacilitategroupcomparisons,butsomedistributionsweretooskewedtopermittransformation,sothatcomparisonsweremadeintermsoftheproportionofeachpopulationrespondingatalevelarbitrarilycalledhigh.Eventuallyweused18specific-responseratings(Table8.1).Inaddition,compositescores(sumofscoresonallovertbe-
TABLE8.1SpecificResponseRatings
havior)werecomputedforthecontrolepisodesalone,forreactionstothebell,andfortheshockepisode.Ahandler-effectscorewascalculatedbasedonthenetchangeintotalscorebetweenstimulationperiodsandcontrolperiods.Somedogsweremoreactivewhenalonethanwhenstimulated;inothers,thereversewastrue.Wewerelookingforevidencethatsuchresponsescouldbeaffectedbyheredity.
■I
RESULTS
:tychangesassociatedwithage.—Changesintotalscores
fromoneagetoanotherwerenotspectacular.AsshowninFigure
•eagles,andbasenjisareconsistentlymoreemotionally
-nansheltiesandcockersatallthreeages.Specificratings
7-
z
it
CD
1734
5
5
elI-—.•.:dtthefivepure:..three
^nkdefinitelyhigherthantheo::
showedsimilarresults.Terrierswerehighontremorandpantingatallagesandlowonvocalization.Infact,themeansofeachbreedremarkablvconsistentinviewoftherelativelylowcorrelationsbetweenratingsonsuccessivetests.TetrachoriccorrelationsbetweenratingsatI"34weeksrangedfrom.063to.SISwith
amedianof.333.Correspondingfiguresforscoresat34and52weeks
219I_vithamedianof.532..Althoughmor.
relationswerestatisticallysignificanttheyweretoolowtobeofvalueforprediction.Actuallythemeanofitsbreedisoftenabetterpredictorofanindividualsscorethanitsscoreonapre-vio
:^nificantl}betweenthethreetests.Except-ntingwasmuchmoreprevalentat17and34weeks.
EMOTIONALREACTTVTTY
199
Liplickingdeclinedinallbreedsexceptbasenjis.Furthermore,youngerdogstendedtobemoreactivewhenanexperimenterwaspresentinthecubicle;olderdogsweremoreactivewhentheexperimenterwasoutside.
TABLE8.2
••P<.01
Inallbreedsheartratesdeclinedwithage.fromapproximately220beatsperminuteatoneweekofageto130atoneyear(seeFig.5.1).Therelativepositionsofthebreedsremainedfairlyconstantfrom17weeksthroughouttherestofthefirstvear.Theintraclasscorrelationforcontrolperiodheartratewashighestat34weeks,indicatingasomewhatgreatereffectofgeneticdifferencesatthisagethanwitheitheryoungerorolderanimals(Table8.2.
atthisagethanwitheitheryoungerorolderanimals(Table8.2.
InTable8.3arechangesinheartrateaccompanyingtheentrance
TABLE8.3ChangeenHeartRate(BeatsMinute)DuringQuieting
P<.01
ofanexperimenterforEpisode3,quieting.Inthesedatathebreeddifferencesaregreatestat17weeks,whenthecockerspanielsshowedamaikeddropandthewire-hairedterriersasimilarincrease.Onthelatertestsbasenjisandbeaglesconsistentlvshowedcardioac-celeration,whilespanielscontinuedtoshowdecelerationunderthesameconditions.Incontrast,theheartrateresponsesofthesheepdogsandterriersareinconsistentatdifferentagesandwithinbreeds.Thesmallaveragechangeforterriersdoesnotindicatethatallmembersofthisbreedmaintainedaconstantheartratewhenthestimuluswaschanged.Bothmarkedaccelerationanddecelerationwerefoundinafewindividuals,butthemeanwasclosetozero.
e=ee::z~zmces
TABLE8.4
MeanStanineScoresorFivePureBreedsonTenBehavioralandFourHeartRateMeasuresatThreeAges
Breedcomparisons.—Tables8.4and8.5summarizereactivitytestscoresforthefivepurebreeds.InTable8.4aremeasureswhichwereconvertibleintostanines,togetherwiththeresultsofanalysisofvarianceofthetransformedscores.Readersinterestedincomparingthesignificanceofdifferencesbetweenpairsofbreedscanusetheapproximationthatdifferencesof1.0stanineunitswilloccurinabout5percentofcomparisonsinarandomsample.Forexample,thefirstfourbreedsareseparatedfromeachotherbyadifferenceofoneormoreonthetotalbehaviorscoreat17weeks.Foxterriersareintermediatebetweenbasenjisandsheltiesandthusarenotsignificantlydifferentfromthesetwobreeds.Thismeansthat8outofapossible10interbreedcomparisonsaresignificantlydifferentat5percentorbetter.
Perhapsthemoststrikingfeatureofthistableisthealmostuniversaloccurrenceofhighlysignificantdifferencesbetweenthefivebreeds.Thirty-onedifferencesoutof42aresignificantatthe.001level.Onlyheartratechangeduringbellringingandthehandler-effectscorefailasdiscriminatorsofbreeddifferences.A
ringingandthehandler-effectscorefailasdiscriminatorsofbreeddifferences.Apreponderanceofsignificanteffectsofheredityhasnotbeenachievedbydiscardingmeasureswhichfailedtodiscriminatebetweenbreeds.Allofthemeasuresonwhichreliabledatawerecollectedhavebeenincluded.Itismuchmoredifficulttofindscoreswhicharenotaffectedbybreeddifferencesthantofindthosewhichareaffected.
InTable8.5aresetforththeresultsofmeasurementswhichwerenotsuitableforstanineconversionbecauseofskewnessofdistributions—usuallytheoccurrenceofmanyzeroscores.Evaluationofthesignificanceofdifferencesbetweenbreedswasaccomplishedbythechi-squaremethod,andcontingencycorrelationswerecalculatedinordertocomparedegreesofhereditaryinfluence.Aswiththemorenormallydistributedscores,differencesbetweenbreedswerehighlysignificantonallmeasuresexceptthatofelimination,wheretheincidencewastoolowforasatisfactorystatisticalcomparison.
Itisinstructivetocomparethevaluesoftheintraclasscorrelationsateachage.Overtwo-thirdsofthesecorrelationsfallbetween.15and.45.Themedianvaluesatsuccessiveagesare.23,.27,and.29.Thusweinferredthattheproportionateeffectofheredityonallscoresconsideredtogetherismuchthesamebetween17and51weeks,althoughcorrelationsforindividualmeasuressuchastheheartratemayriseandfall.Thereissomepossibilitythatgeneticdifferencesareexpressedmoredefinitelyintheone-yearphenotype,ashighintraclassandcontingencycorrelationsoccurtwiceasoftenat51weeksasateitheroftheothertwoages.
1-zlZZF-RENCES
TABLE8.5
PercentagesofSubjectsExceedingArbitraryThresholdsonEightMeasuresinReactivityTest
•Thresholdsforgroupingscoresonliplicking,resistancetoforcedmovement,andlatency-ofemergencewerenotthesameatallagesbecauseofdevelopmentalshiftsinaveragefrequencyofoccurrence.
Sinceasubstantialportionoftheobservedvariationinreactivitywasnotcorrelatedwithbreeds,wemayinquireintocausesotherthanheredity.Hadthepurebreedsbeenhighlyinbredsoastobenearlyhomozygousatallloci,wecouldconcludeonthebasisoftheintraclasscorrelationsthat55to85percentof
couldconcludeonthebasisoftheintraclasscorrelationsthat55to85percentofthevariationsinthetestmeasureswasattributabletoenvironmentalfactorsactingtodifferentiateindividuals.Eachbreed,however,wasactuallyfairlydiverseingenotypesothatthecalculatedcorrelationsareminimalestimatesofgeneticinfluences.Environmentalfactorswereprobablvnotasimportantastheabovefigureswouldimply.
Stillanotherapproachistoinvestigatetheeffectsofsexandoflitterinfluencesonthetest.Amongthepurebreeds,totalreactivityscoresofma)lgcd4.9onthestaninescale;femalesaveraged
EMOTIONALREACTIVITY203
5.0.Thetwosexesgavealmostidenticalresults,indicatingthatthisformofhereditaryvariationhaslittleeffectonthescores.Ontheotherhand,therearesignificantdifferencesbetweenlitterswhenallthreetestsaregroupedtogether.Ourexperimentaldesigndoesnotpermitallocationofthesourceofthiseffect,butsomeorallofthefollowingmaybeinvolved:specificgenesfromaparticularsetofparents,maternalcaredifferences,climaticchanges,changesinobservers—infactanyvariablewhichmightbemorealikeformembersoflittersthanfordogsingeneral.Removingthelittereffect,however,doesnotinthisinstancedecreasethebreeddifferences.Theintraclasscorrelationforbreeds(basednowuponlittermeans),is.61,denotingremarkablylargehereditaryeffects.
Interpretation.—Afteremphasizingdifferencesbetweenbreedsintheformandintensityofemotionalexpression,wewishtocautionthereaderagainstacceptingtheideaofabreedstereotype.Typicallytherangeofscoresforabreedextendedover5or6points,andoccasionallyovertheentire9pointsofthestaninescale.Basenjisandcockerspanielshadmeanstaninesof6.00and3.03,respectively,atoneyear;but65percentofthebasenjisand41percentofthespanielsoverlappedinthemiddlerangeof4to6.
Noone-year-oldterrierwasratedbelow6ontremoralthoughallotherbreedshadindividualswithlowscores.Althoughterriersdidnothavescoresinthelowzone,theotherbreedswerenotrestrictedinthisway,andratingof7and8werecommoninfour.Theleastamountofoverlapwasfoundinbitingatoneyear;83percentofbasenjiswerebitersand93percentofcockerspanielswerenon-biters.
Themostgeneralinterpretationofthesedifferencesbetweenbreedsisthatthey
Themostgeneralinterpretationofthesedifferencesbetweenbreedsisthattheyarerelatedtodifferentialresponsestoinhibitorytraining.ThisisparticularlyevidentinFigure8.1,inwhichthecockersandsheltiesrankedconsistentlybelowtheotherbreeds.Boththesebreedsareeasilytrainedtorepressanyactivity,althoughtheresponsestakequitedifferentforms.Anysortofthreat,butparticularlyahandmotion,willmakeacockerceaseallactivity,buttheeffectismomentaryandtheanimalshowsnosignsofemotionaldisturbance.Inhibitionofasheltieislonglastingandappearstobeaccompaniedbyprolongedemotionalarousal.
Thisbringsuptheproblemofwhetherthereactivitytestmeasuresasingleunderlyingtrait,oracompositeofgeneticallyinfluencedcapacities.Manyofthescoresarepartiallycorrelatedwitheachother,andtwoofthemeasures,heartrateandsinusarrhythmia,arehighlyinterdependent.Aslowheartrateisarrhythmicand,con-
204BREEDDIFFERENCES
versely,afasterheartrateisregular.Afactorialanalysis,aswillbeseeninchapter14,resultedinsplittingthevariousreactivitymeasuresamongseveralfactors,heartratebeingone,andageneralfactorforconfidence-timiditybeinganother.
SUMMARY
Theemotionalresponsescharacteristicofthedifferentbreedscontinuetochangeanddevelopthroughoutthefirstyearoflifesothatbreeddifferencesonthereactivitytestwerepresentandhighlysignificantinastatisticalsenseatallages.Thetestsituationsseemtoaccentuateemotionaldifferencesbystimulatingdistinctalternateresponses,suchaspassivityorattemptstoescape.Selectioninthepasthasobviouslybeenhighlysuccessfulinseparatingthefivebreedswithrespecttoalargenumberofemotionalresponses.Somuchvariationstillremains,however,thatitwouldprobablybepossibletoselectcockerspanielsforafewgenerationsandproduceoffspringliketerriersorbeagles—atleastwithrespecttoparticularresponses.Tosynthesizebythismethodatotalpatternofresponsessimilartoanotherbreedwouldbeamoredifficultifnotimpossibletask.
Allthisstronglysupportstheconclusionthathereditygreatlyaffectstheexpressionofemotionalbehaviorandalsothatdifferencesinemotionalbehaviorformaprominentpartofthecharacteristicbehaviorofbreedsandindividuals.
formaprominentpartofthecharacteristicbehaviorofbreedsandindividuals.ComparabledifferenceshavebeenreportedinhumanindividualsbyLaceyandLacey(1958).Whetherornotsuchdifferencesarerelatedinturntotheperformanceofbreedsintrainingandproblem-solvingtestsisaquestionwhichwillrecurinfuturechapters.
EXPERIMENTS
ONTRAINABILITY
Anumberofourproceduresinvolvedmodificationofadog'sbehaviortowardapatternspecifiedbytheexperimenter.Suchlearningdiffersfromproblemsolvingbyrequiringamorestereotypedresponsefromtheanimal,althoughthefundamentalprocessofselectivereinforcementofsuccessfulresponsesoperatesinbothtypesoftests.Itisthereforeconvenienttoseparatesuchtestsasquieting,leashtraining,retrieving,motorskills,andobediencefromproblem-solvingtestsinthemoreusualsense.
Trainingtestscaninturnbedividedintoforcedandrewardedcategories.Inforcedtraining,thetraineeispunishedforadeviantresponseorpreventedfromcarryingitout.Inrewardtrainingheisrewardedwhenhemakesthecorrectresponse.
Trainingtofollowapprovedculturalmodesisanimportantpartofchilddevelopmentandislikewiseimposeduponapuppyadoptedintoahumanfamily.Remainingquiet,walkingonalead,andsittingquietlyoncommandarepartoftheusualregimenofpetdogs.Ourproceduresweresimplystandardizedformsofsuchtraining,coupledwithanobjectiveratingscaleforperformance.Insuchforcedtraining,theexperimentersestablishedinadvanceapatternofbehaviorwhichwastoserveasamodelandsystematicallypunisheddeviations.Analogieswithcertainaspectsofchildrearingarefairlyclear.Trainingwascontinuedforaspecifiedperiod,andcomparisonsbetweengeneticgroupsweremadeatvariousstages.Rewardtrainingismorecloselyrelatedtoordinaryproblemsolvingsincethesubjectisfreertoadoptanyindividualmodeofrespondingwhichissuccessful.Thetasksinretrievingandmotorskills,however,involveaminimumofsensorydiscrimination;instead,theexperimenteren-
205
BREEDDIFFERENCES
BREEDDIFFERENCES
couragesandrewardsthesubjecttoperformrelativelysimpleacts.Parentssimilarlytrainachildtothrowaballorclimbstairs.
Thatthereareindividualdifferencesintrainabilityis,ofcourse,commonknowledge.Ourinterestwasindeterminingtheportionofvariabilityattributabletogenetics,andintherelationshipbetweentrainabilityandothercharacteristicsofthesubjects.Inparticular,wewereinterestedinwhethertrainabilitywascorrelatedmorecloselywithothermeasuresoflearningorwithmeasuresofemotionalresponse.
FORCEDTRAINING
Quieting.—Theearliestforcedtrainingaroseoutofattemptstoweighpuppiesaccurately.Itwasnecessarytokeepthemquietonthescaleswithoutactuallytouchingtheminordertotakeareading.Wedevelopedatechniqueofplacingasubjectonthescaleplatform,holdingourhandsnearbutnottouchinghimunlesshestartedtowriggleorstepoff.Thebestpossibleperformancewasforapuppytoremaininactiveforoneminuteofweighingandobservation.Ratingsweregivenoneachtrialasfollows:3,active;2,partlyactive;and1,quiet.
Figure9.1showstheresultsatdifferentages.Noneofthevery
i.o
.9.6
fc.7
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Fie.9.1.—Proportionofanimalsratedasquietduringweighing.Thecurvesaresmoothedbytaking3-pointmovingaverages.
TRAINABILITY207
younganimalsremainedquietforawholeminute,butbeginningatabout5weeksofage,someindividualsinsomebreedsbegantodothis.Graduallymoreandmorewerecompletelytrained.Atfhesametimethebreedsbegantodifferentiate,sothatby16weeksnearly70percentofthecockerspanielswereremainingquietbutonly10percentofthewire-hairedfoxterriers.Sheltieswerethesecondmosteasilytrained,andbasenjisandbeagleswereclosetothemeanofthefoxterriers.
Leashtraining.—Trainingtowalkonaleadwasbegunat19weeksofage.Thepuppiesweregivenfivetrials(oneperday)overacourseleadingfromtheiroutsidepenstothelaboratory.Beginningonthethirdday,theywereledthroughaportionofthelaboratoryandupaflightofstairs.Thepuppiesworeachoke
aportionofthelaboratoryandupaflightofstairs.Thepuppiesworeachokecollarattachedtoachainleash.Ananimalwhichbalkedthreetimessofirmlythatitcouldnotbeinducedtocontinuewalkingwasliftedandcarriedbytheexperimenteroverthecourse.Thesubjectswereledbackoverthesamepath,butnorecordsweremadeoftheirresponsesonthereturnjourney.Asecondseriesoffivetrialswasgivenduringthetwenty-secondweekwhentheywereledtothelaboratoryfordiscriminationtraining.
Wewantedtotrainthedogstowalkonaslackleadattheleftoftheexperimenterwithoutvocalizationorbodilycontact.Demeritswererecordedforthefollowingfaults,withanarbitraiymaximumscoreononedayofthreedemeritsineachcategory.
Balksontheoutdoorcourse
Balksatdoorsorgates
Fightingorbitingleash
Draggingbehindorrunningahead(positionerrors)
Interferencewiththeexperimenter(bodycontacts)
Vocalization
Aconvenientwayofmeasuringtheeffectivenessofleashtrainingistheprogressivereductionofthetotalnumberofdemerits.Ofequalinterestisthefrequencyofoccurrenceoftheseveraltypesofdemeritsoverthewholecourseoftraining.Suchmeasuresprovedtobeparticularlysuitableforcharacterizingpatternsofresponsesforthefivebreeds.
Intheleashtest,unlikemostofourbattery,therewasnosignificantincreaseinreliabilityastrainingproceeded.ThisiswellshownbythetetrachoriccorrelationsbetweenthethreepairsoftestsrecordedinTable9.1.Thecorrelationswere:rtetlt2=.72;rtet4t5=.76;rtet9,io=.79.Althoughalmostallsubjectswerereceivingveryfew
BREEDDIFFERENCES
demeritsattheendofthetrainingperiod,theywerenomorepredictablefromdaytodaythantheywereatthestartoftraining.Thecorrelationbetweenthesumsofoddandeventrialswas.86,whichishighwhenoneconsidersthat
sumsofoddandeventrialswas.86,whichishighwhenoneconsidersthathandlerswerechangedonalternatetrials.
TheeffectsoftrainingonthenumbersofdemeritsinthefivepurebreedsareshowninTable9.1.Forsimplicity,onlysixofthetendaysaresummarized:thefirsttwo,thefourthandfifth,andthelasttwodays.Thesewerechosentoberepresentativeofthebeginning,middle,andlatestagesoftraining.
InspectionofTable9.1showsthatthemeansofthebreedscome
TABLE9.1MeanNumberofDemeritsinLeashTraining
closertogetherastrainingproceeds.Thus,therangeofbreedmeansonDay1was5.8demerits,andonDay10,2.1demerits.Onemightinferfromthisthattheeffectoftrainingwastodiminishtheimportanceofhereditarydifferencesuponbehavior,buttheconclusionwouldbeincorrect.WhentheproportionoftotalvarianceattributabletobreeddifferencesiscomputedforDay1andforDays6-10combined,therespectivevaluesare53.7and52.4percent,anegligibledifference.Thelastfivedayswerepooledinthiscalculationinordertomakethemeannumberofdemeritsmorenearlyequalforbothsetsofscores.Ingeneral,thedogsmadeaboutasmanyerrorsonthefirstdayastheydidduringthewholesecondweek.
Trainingfortherigidcriteriademandedbythistestdoesnoteliminatenorevendiminishtherelativecontributionofhereditytobehavioralvariation.Ofcourse,iftheprocesscouldbecontinuedtothepointwherenodemeritswereassigned,allindividualandbreedvariationwouldvanish,andhereditaryeffectswoulddisappear.Intin'stest,over50percentofthevariationinthetotalscorecouldbeattributedtobreeddifferences.Theproportionisunusuallyhigh,andthereforeitisInterestingtoanalyzethiscasefurther.
(raeobviouscourseistocomparethebreedsonthedifferenttypes
TRAINABILITY
209
ofdemeritsseparatelyinordertoseewhetherthegroupsdifferinnumberofdemeritsonly,orintheircategoriesaswell.Byconversiontostanines,itispossibletocompareeachtypeofdemeritonthesamescale.
Figure9.2showsthemeanstaninescoresforeachdemeritcategory.Itisclearthatbreeddifferencesinnumbersofbalksandposi-
BALKSINDOORS
VOCALIZATION
BABEACSSHWH
BABEACSSHWH
Fig.9.2.—Typesofdementsgivenduringleash-controltraining(staninescale).
tionerrorsarelessmarkedthaninfightingtheleash,interference,andvocalization.Basenjiswereoutstandingintheirvigorousresistancetotherestraintofacollarandlead;Shetlandsheepdogssimilarlyinterferedexcessivelywiththehandlerbyleapingonhimandwindingbetweenhislegs;beaglesweretheforemostemittersofhowlsandwailsduringinitialstagesoftraining.
Applyingananalysisofvariance,wecancomputefortheseveral
BREEDDIFFERENCES
BREEDDIFFERENCES
demeritcategoriestheproportionofvariationattributabletobreeddifferences.Thesevaluesare:balksintheopen,1.9percent(notsignificant);balksatdoors,28percent;fightingtheleash,72percent;outofposition,39percent;interference,55percent;andvocalization,40percent.Alldifferencesexceptthefirstaresignificantatbetterthanthe.01level.
Thepatternofintercorrelationsbetweenthesixtypesofdemeritsshowssomestrikingrelationships.ThesehavebeenarrangedinTable9.2tobringthelargercoefficientsofcorrelationalongthemain
TABLE9.2IntercorrelationsofTypesofDemeritsDuringLeashTraining
diagonal.Suchanarrangement,accordingtoGuttman(1955),showsthedegreetowhichtheseveralkindsofdemeritscanbeconsideredasexpressionsofcommonfactors.
Intercorrelationsbetweenthetwotypesofbalksandpositionerrorsarethehighestandseemtodefinethecentralcharacteristicsofthemodeltowardwhichtrainingisdirected,thatis,adogwalkingfreelyontheleashbythesideofthetrainer.Thedemeritswhichmoststronglyseparatethebreedsareperipheraltothiscorecharacteristicandmaybeinterpretedasalternativeformsofemotionalresponsetothesituation.Demeritsforinterferencecorrelatenegativelywithallothertypes.Byaddinginterferenceratingstoobtainatotaldemeritscore,wetendedtounderstatebreeddifferences.
Althoughtrainingreducesthenumberofdemeritsinallcategories,itdoesnotdosoequally.Theproportionofbalksandvocalizationfalls,buttheproportionofpositionerrorsandinterferenceincreases.DetailsaregiveninTable9.3.Thusthehereditarydifferencesatthebeginning,middle,andendoftrainingareexpressedindifferentbehaviorpatterns.Ifonlythetotalscoresarecompared,thisinterestingfactisconcealed.
Weconcludethaieachbreedischaracterizedbyapatternofresponseswhicharedifferentiallyaffectedbytraining.Astrainingproceeds,theexpressionofhereditarydifferencesshifts,butthepro-
TRAINABILITY21
TABLE9.3TypesofDemeritsinEarly,Middle,andLatePhasesofLeash-
TABLE9.3TypesofDemeritsinEarly,Middle,andLatePhasesofLeash-ControlTest
portionofvarianceattributabletogeneticschangeslittleornotatall.Withinafewdays,subjectsaretransformedfrompuppieswhopulloffatwildanglesordragtheirfeet,emittingbloodcurdlingyelps,todocilecreatureswalkingfreelybytheirhandlers.Butthehereditarycontributiontoindividualityisdetectableatallstagesoftraining.
Theobediencetest.—Athirdmajorproceduredesignedtotrainsubjectstoachieveaspecifiedcriterionofbehaviorwastheobediencetest.Animalsweretrainedovera3-dayperiodtoremainonastandfor30secondsandthentojumpdownoncommand.Duringtheearlystageseachsubjectworeachokecollartowhichaleadwasattached.Astrainingprogressedrestraintsweregraduallyremoved,andthehandleronsuccessivetrialsmovedawaytodistancesof1.5,3,6,and12feet,andfinallybehindascreen14feetfromthestand.
Ifthesubjectleapedprematurelyduringatest,thehandlermovedclosertothestandforthenexttrial,andstartedanewseriesofincreasing-distancetrials.Ameasureoftheleveloftrainingattainedoneachdaywasobtainedbyarbitrarilyassigningascoretothesubject-trainerdistanceandaddingthescoresofaday'strials.Assignedvalueswere:chokecollar(0);6inches(1);1.5feet(2);3feet(3);6feet(4);12feetandbehindscreen(5).Subjectswhofailedtoleapatcommandwithin10secondsweregentlypushedfromthestandbythetrainer.
Thetrainingprocedurewasdesignedtobringindividualstoacommonstandardasquicklyaspossible.Equalizationwaspromotedbycountingtwochoke-collartrialsasequivalenttoasinglehand-controltrialinscoring.Thusthemorerecalcitrantsubjectsreceivedadditionaltraining.Inaddition,trainingwasdiscontinuedonanydaywhenthesubjectstoodfor30secondswiththehandleratthe12-footmark.Thiswasdonetoavoidovertrainingsubjectsandtherebyincreasingtherangeofindividualvariation.
OnDay4and,formostsubjects,againonDay5,astandardized
212BREEDDIFFERENCES
setoffivetrials,oneeachat0.5,1.5,6,and12feetandbehindthescreen,wasrepeatedtwice.Procedurewasthesameasintraining,exceptthatnopunishmentwasgivenforprematureleaping.Acompositescoreforthetestwasobtainedbyaddingthetimespentonthestand,plus30foreachtrialinwhichthesubject
addingthetimespentonthestand,plus30foreachtrialinwhichthesubjectjumpedoncommand,plus60foreachtrialinwhichthesubjectdelayedfor10secondsfollowingthecommandtojump.Scorescouldrangefromzeroforasubjectwhoalwaysleapedfromthestandimmediatelyuponrelease,to450forasubjectwhofailedtojumponcommandinallfivetrials.Theoptimum"obedience"wouldbeascoreof300.However,theresultsmadelesssensewhenarrangedaccordingtoascaleof"obedience"thanwhenarrangedaccordingtoascaleofinhibitionofmovement.Inoursystem,therefore,highscoresdenoteinhibitedsubjectswhichremainedimmobileonthestand;lowscoresdenotehyperactivesubjectsnotwellcontrolledbythehandler;andmiddle-rangescoreswereobtainedbydogswhichwerereadilycontrolledbythehandler.Resultswereconvertedtothestaninesystem.
Inaddition,twootherratingsweremadeonmostofthesubjectsinthetestsituation.Ameasureof"confidence"wasobtainedbynotingwhetherthedogwouldeatfromadishplacedfirstonthestand,thenbesideit,andfinallyatsomedistance.Somedogswouldnottakefoodatall.Ameasureof"attraction"wasobtainedbyratingthesubjectonhisapproachtothehandlerbetweentrials.Eachdogwascalledbythehandlerafterhehadfinishedrecordingeachtrialonthedatasheet.Resultsofthesetwomeasurescouldnotbeconvertedintostanines,andsubjectsweremerelyclassedaslow,medium,andhighwithrespectto"confidence"and"attraction."Theobjectinrecordingthesemeasuresofemotionalandsocialbehaviorwastoseewhethertheyhadanyconsistentrelationshipwithdegreeoftrainability.
Finally,aspecialprocedurewasadoptedduringtheprogramtotesttheeffectsofchanginghandlers.Eachlitterwasassignedtotwohandlers,onemanandonewoman.Withineachbreedorhybridgroup,maleandfemaledogsweredividedseparatelyatrandombetweenthehandlers.Amongthepurebreeds,theretestonDa\5wasconductedbytheotherhandler;amongthehybrids,theretestwasadministeredbytheoriginalhandler.Thisdesignpermitsevaluationoftheefficacyofmaleandfemaletrainersandtheextenttowhichobediencetrainingisgeneralizedasaresponsetohumanbeingsascontrastedwithspecificindividuals.Onewouldpredictthattherewouldbesonicdeteriorationofperformanceonretestwithanotherhandlerandpossiblythattheeffectwouldbemoreextremeinbreeds
TRAINABILITY
213
withthenameofbeingone-mandogs.Amongoursubjects,thebasenjishavesuchareputation.
Allthebreedsshowedmarkedimprovementoverthethreedaysofpreliminarytraining.Figure9.3demonstratesthattheorderofper-
6-
5-
I23
DAYS
Fig.9.3.—Leveloftraining(stanineunits)onsuccessivedaysofobediencetest.
formancedoesnotshift;infact,thespreadofthemeansincreaseswithtraining.Theproportionofthetotalvarianceattributabletobreeds,ft,alsoincreases,butnotsignificantly.Thesameorderofbreedscoringwasmaintainedonthetestdayandintheretest.ResultsofbothtestsareshowninTable9.4.Differencesbetweenbreedswereagainhighlysignificant,withintraclasscorrelationsinthefirsttestof.149,andonretest,.262.
Thereliabilityoftheindividualscoresontestday(Day4)canbeestimatedbythecorrelationof.939betweenthetwohalvesofthetest.Thecorrelationbetweentestandretestwas.863.Thesefiguresindicatethatafewdaysoftrainingproducehighlyconsistentbehaviorontheobediencetest,evenmoresothanintheleash-trainingtest.
Itisinterestingtonotethattheaverageperformanceofdogstrainedbymenandthosetrainedbywomenwerealmostexactlythe
214BREEDDIFFERENCES
TABLE9.4MeanStanineScoresonObedienceforPureBreeds
Breed
Basenji
Beagle
Beagle
Cockerspaniel
Shetlandsheepdog...Wire-hairedfoxterrier
All
SexofExperimenter
Day4
Day5
F
MFMFMFMFM
MFM
FMFMFMF
FM
M
F
N
115
10
11
13
11
9
10
10
5
8
4845
MeanScore
Day4
4.003.20
4.905.505.806.506.505.056.606.19
5.425.47
Day5
3.403.20
4.254.455.416.045.504.706.205.44
Difference
betweenDay5-Day4
-0.600.00-0.65-1.05-0.39-0.46-1.00-0.35-0.40-0.75
4.824.88
0.600.59
same(5.47and5.42,respectively).Theaveragechangeinscoreonretestwasalsopracticallyidentical(—0.60)whetherthechangewasfrommaletofemaletrainerortheopposite.Thehybrids,whowerere-testedbythesameindividual,felllessthanhalfasmuch(—0.27)onretest.Theseresultswouldhavebeenpredictedontheargumentthatanychangeinthetestingsituationwouldproducedetrimentaleffectsuponperformance.Wefoundnoindication,however,thatanyonebreedwasmoreaffectedthananotherbreedbythechangeinexperimenters.Thenumberpergroupisrathersmall,buttheexperimentdoesnotsupportthenotionthatsomeofthetestedbreedsattachthemselvesonlvto
notsupportthenotionthatsomeofthetestedbreedsattachthemselvesonlvtooneindividual,whileothersshifttheirresponsesreadilytoanotherperson.
Itwassomewhatsurprisingtofindthatperformanceontheobediencetestasmeasuredbythetendency7toinhibitjumpingwascorrelatedneitherwithourmeasureof"attraction"norbv"confidence."Strikingbreeddifferenceswerefoundinthesetworatings.Withinanyonebreed,however,highorlowconfidenceorattractionratingswereunrelatedtoobediencescores.Itisperhapsoddthattrainingwasequallyeffectivewhetherornotthesubjectwasattractedtothetrainer,andwhetherornotthesubjectwaswillingtoapproachthestandtoreceivefood.Theresultssuggestthatthevariouspartsofthedog'sbehavioralrepertoiretendtobeindependent.Hisentirebehaviorisaffectedbygenotvpe,butgeneralfactorsoftrainabilityandemotionalityarenotreadilyfound.
Tosummarizetheresultsofthistest:
1.Breedsdifferwidelyintheeasewithwhichtheycanbetrainedtoremainquietoncommand.
TRAINABILITY215
2.Allsubjectslearnundertraining,butthedifferencesbetweenbreedspersist,atleastoveraone-weekperiod.
3.Thecontributionofhereditytototalvariancedoesnotchangegreatlyovertheperiodoftraining.
4.Changingtheexperimenterforaretestproducesamoderatedecrementinscore,whichisabovethatfoundwhentheretestisperformedbytheoriginalexperimenter.Theeffectisaboutthesameinallbreedsexamined,butgreatindividualvariationisfound.
Comparisonofbreeds.—Alloftheseforced-trainingtestsinvolveteachingtheanimaltobeinactive.Thepuppyistaughttostayquietlyonthescalesbyhandsignalsandrestraint.Whenplacedonaleash,heisbeingtaughttorestrainanyactivityexceptthatoffollowingtheexperimenter.Finally,ontheobediencetest,heistaughttobeinactiveonaplatformatadistancefromthetrainer.
Whenthebreedsarerankedonallthreetests(Table9.5),the
TABLE95RankofFivePureBreedsunderForcedTraining
TABLE95RankofFivePureBreedsunderForcedTraining
Test
ControlledActivity>•Overactive
ScaleactivityCSSHBABEAWH
LeashcontrolCSWHBABEASH
ObedienceCSWHBEASHBA
cockerspanielsemergeastheeasiesttotraininallthreesituations.Basenjisandbeaglesareconsistentlyhardtotrain,butsheltiesandwire-hairedfoxterriersmaydowellinonesituationandpoorlyinanother.
Weareforcedtoconcludethatthereisnosimplegeneralcapacityinvolvingrestraintforacceptingforcedtraining.Thetrainabilityofcockersisrelatedtotheirformerselectionfortheabilitytoaccepttrainingtocrouch.Thisresponseiseasilyelicitedbyhandsignals,andthesewereusedtosomeextentinallthreetests.Thesheltiesareeasilytaughtrestraintbydirectlytouchingtheirbodiesbuttendtobeactivewhenawayfromanexperimenter.Theydo,however,crowdagainsttheexperimenter'slegsduringtheleash-controltest.Wire-hairedterriersrespondtohandcontactwithplayfulfightingbutacceptrestrainttrainingatadistance.Ontheleashtheytendtopullaheadoftheexperimenter.Basenjisrespondtomostkindsofrestraintwithattemptstoescape,whilebeaglesgivetheappearanceofbeingrestlessinanyrestrainingsituation.Theseobservationsareborneoutbythelowcorrelationsbetweenthethreetests(Table
BREEDDIFFERENCES
TABLE9.6
CorrelationsbetweenTestsofForcedTraining(FromC.L.Brace)
•Sig.at.05**Sig.at.01
9.6).Theonlycorrelationofanyimportanceisaslightnegativecorrelationbetweenleashfightingandlearningtostayontheplatform.
Wethereforeconcludedthatthebasictrainabilitycharacteristicsofthedifferentbreedstendtobespecifictoparticulartestsituations,andthattheyarebasedon
breedstendtobespecifictoparticulartestsituations,andthattheyarebasedonalargevarietyofcapacities.Insometestsituations,thepossessionoftwodifferentcapacitieswillproducewidelydifferentresultsbetweenbreeds;inothersitmayproducealmostidenticalperformances.
REWARDTRAINING
Intheseteststheanimalisgivenarewardassoonasheperformsthedesiredact.Theusualtechniqueistobreakthetrainingdownintoaseriesofsteps,firstteachingtheanimaltodoasimplefirststep,thenaddingmoreandmorerequirementsinsequenceuntilacomplexseriesofactshasbeenlearned.ThisstepwisetraininghaslongbeensuccessfullyusedtotraincircusanimalsandhasbeendevelopedintoanartwiththetechniquesofoperantconditioningdevisedbySkinner(Skinner,1938;BrelandandBreland,1961).Foodisthemostcommonreward,butthedogisalsonotableforitsresponsivenesstowordsandattitudesofahumanhandler.
Inthesectionwhichfollows,wehavesummarizedresultsofthehabitformation,retrieving,andmotor-skilltests.Themotivationtestdescribedinchapter10asapreliminarytodiscriminationtrainingalsofallsinthiscategory.
Goalorientation(habitformation)test.—Thistestgivenwhenthepuppieswere9weeksofage,hadtwofunctions.Weintendedit
TRAINABILITY
217
asbasictrainingforrunningtoagoal(asafoundationformorecomplextests),andwealsoattemptedtomeasuretherapiditywithwhichapuppycouldchangeahabitonceitwasformed.Thetestitselfconsistedofshowingthepuppyasmallbitoffishinawoodenboxandthenplacinghiminacagewithawiregateinfrontasinthephotograph(seeplates).Theexperimenterlefttheroom,raisedthegatewithastringrunningthroughapulley,andrecordedthebehaviorofthepuppy.Thepuppywasgivenatotaloffourtrialsontwosuccessivedays,andthenthepositionoftheboxwaschangedtoadifferentcorneroftheroom,adistanceofabout6feet.Thepuppythenransixmoretrialsoveraperiodofthreedays.
AsFigure9.4shows,differencesbetweenbreedsweregreateron
SH\
GOALORIENTATION
56TRIALS
Fig.9.4.—Meantimescoresongoal-orientationtest.
thefirsttwotrialsthanonthethirdandfourth.Weselectedthesecondtrialforanalysis,inthehopesthatthiswouldproveameasureofbasicmotivationforrunningtoagoalafterthepuppieshadachancetolearntheobjectofthetest.Basenjisgavethebestperformance,andsheltieswerethepoorest.Asonmanyothertests,thebehaviorofthebeaglesshowedahighdegreeofvariability.Differencesbetweenbreedsweresignificant,buttheproportionofvarianceattributabletothiscausewasonly7percent(Table14.3).
Whenthepositionofthegoalwaschanged,largedifferencesbe-
tweenthebreedsreappeared,thebasenjisagainperformingbestandfoxterriersmostpoorly.Unlikeotherbreeds,sheltiescontinuedtoimprove,performingaswellasthebasenjis.Allthebreedsperformedverysimilarlyonthesubsequenttrials,andtherewasnoindicationofanvdifferencesintheabilitytoswitchfromonehabittoanother.
Thesuperiorityofthebasenjisonthegoal-orientationtestmayreflectsimplvtheirsuperiorrunningspeedatthis_tmore
probablyitshowsagreatertendencytowardvisualorientation.Therewasno
probablyitshowsagreatertendencytowardvisualorientation.Therewasnoindicationthatdifferencesbetweencockersandbasenjisshowedanyregularformofinheritance7;generalconclusionisthatallbreedsperformedinaverysimilarfashiononthissimplekindofrewardtraining.
7liningtoretrieve.—Mostdogscanbetaughttoretrieveastickandreturnittotheirma:houtanyapparentrewardother
thantheexecutionoftheactitself.Somedogs"beg"theirmasterstothrowobjectsforretrieval.Inaddition,manybirddogbreedsare
;JarlytrainedtoretrievewoundedorkilledbirdsandreturnthemtotheirmastersThecockerspanielhasinthepastbeenselectedforitsabilitytobetrainedinthisfashionandalsofora"softmouth,"meaningthatacockerwillpickupthebirdwithoutbitingorcrushingit
originallydidafewretrievingexperimentswith9-week-oldcockerspanielpuppies,anagewhensuchtrainingusuallysucceeds
Pfaffenberg.Thetrainingschedulebecamecrowd
however,andthetcostponedtoamuchlaterage(32wee*
trainedouranimalsbyusingamodificationoftheplay-retrievingprocedurewhichmostownersemploywiththeirdo^s.Anunfamiliarobjectwhichcouldbeeasilycarriedwasleftinthepenforacoupleofdaysinorderthatthedogsmightfamiliarizethemselveswithit.Onthesucceedingthreedavseachanimaltedforretrievalof
adumbell-likeobject(twothinblocksofwoodconnectedbvaheawwoodendowel'onatotalof9tri^
Theresultsweredisappointing.Only11percentofthepurebreddogsactuallyreturnedthedumbellandreleaseditinatleastonetrial,andnoneofthedifferencesbetweenbreeds.ificant
Moredetailedanalysisgaveasimilarresult.TheactofretrievingcanbebrokendownintosmallerbehaviorpatternsforpurposesofanTedogmustfollowtheobjectthrown,pickit
up,earn-it,returnit,and,finallyreleaseitwhenthetrainerattemptstotakeitavynearly100percentofthedosswouldfollowthe
ynearly100percentofthedosswouldfollowthe
object,andabout25percentwouldpickitupandcamit.butvervfewwouldactuallyreturnittothetrainer.A^ain.thedifferencesare
TRAINABILITY219
TABLE9.7
PercentageofAnimalsSuccessfullyTrainedinRetrievingTest
notgreatenoughtoindicatethatthereareanyimportantbreeddifferences.Occasionallyweobservedpuppiescarryingotherobjectsintheirmouthsaboutthepen—aspontaneousmanifestationofpartofthecompletepattern.However,therarityofsuchobservationspermitsnoconclusionsregardinggeneticorenvironmentalcausation.
Weconcludedthattheabilitytolearnretrievingisratherwidelydistributedthroughoutdogbreedsandthatthespecialabilitiesofthecockerspaniel,ifany,areconfinedtoretrievingbirdsinthefieldratherthantheplayretrievingwhichwastheobjectofthetest.Wewerealsoimpressedwiththerelativedifficultyoftrainingtheolderanimalscomparedtothefewwhichweretrainedat9weeks.Thereispossiblyacriticalperiodforlearningtoretrieve,thatis,atimewhentheprobabilityofexecutingthecompletepatternisrelativelyhigh,sothatrewardtrainingcanbemaximallyeffective.
Themotor-skilltest.—Aboutone-thirdofthewaythroughtheexperimentweobservedbasenjisjumpingtothetopsoftheirhousesandsurveyingtheworldfromthesevantagepoints.Somemembersofthisbreedcouldscramblehalfwayupthefenceoftheirenclosureandclingtoanarrowshelfwhilepeeringthroughthewiremesh.Noneoftheotherpurebreedsdidthis,andwethereforedesignedatesttomeasuredegreesofclimbingandjumpingcapacity.
Themotor-skilltest,asitwasnamed,requiredthedogstoclimbtothetopofapileofboxes,andlatertocrossabridgeleadingfromthepiletoanotherhighpointinordertoobtainafoodreward.Onthefirstdaywestackedtwowoodenboxesinthepenandplacedadishcontainingaspoonfuloffishuponit.Abroadrampledtothetop,andtheheightof2feetwasjustenoughsothatadogcouldnotreachthefoodfromtheground,andmusteitherjumptothetoporclimbtherampinordertoeat.Wefirstplacedeachsubjectinturnonthepileandallowedittoeat,thenplaceditbackonthegroundand
ittoeat,thenplaceditbackonthegroundand
measuredthetimerequiredtoreachthetopagain.ThetestwasrepeatedonDav2,andonDav3wasmodifiedbyincreasingtheheightto3feet.Asthepilegrewhigher,theramp,ofcourse,grewsteeper.OnDay4thestacksofboxeswere4and5feethigh,atwhichpointthetestbecamemostdifficult.OnDay5thestackwasreducedtothe3-footlevel,butthedogsnowhadtowalkacrossaplanktoreachthefood6feetawayonthetopofthehouse.Theplankwasatfirstonefootwide,andonthesecondtrialwasreplacedbyoneonly6incheswide.Manydogsfoundthisdifficult,andsomelosttheirfootingandfelloff.
Ifadogdidnotreachthegoalaftertwominutes,theexperimentertookaleashandledhimuptherampsothathecouldeat.Thus,forcedtrainingwassecondarilycombinedwithrewardtraining.
Thewholetestmayalsobeconsideredthecanineequiyalentofanathletice\entsimilartoahighjump.Theearlypartofthetestonthelowboxesconsistedoftrainingtheanimalsinmotiyationandinthetechniqueofclimbingandjumping,whilethelasttwodayswereequiyalenttoacontestinwhichtheheightoftheobjecttobeclimbedwasgraduallyraisedtooneofconsiderabledifficulty.
rfinedasfailuretoreachthefoodwithintwominutes.
lateverthecause,weresomanythattheresultsofthetestarebestexpressedintermsofpercentagesofsuccessratherthantimeF§9.5.Asexpected,thebasenjisdidbetterthananyotherbreedonthefirsttrialofthetest:butunexpectedly,diecockerspanielsdid
3A5-;-:'.■---;-
'CCr**2BOXES—>*B:>E:->=:>:$3:»iS=L~'»--_-'.•"
ZQ
MM
"60
<->40
a:
Q.
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TRIALS
Fig.9.5.—Proportionofanimalssucceedingoneachtrialofthemotetest.
TRAINABILITY221
equallywellonthetotaltestresults(Table9.S).Thebasenjisobviouslyhadsuperiorclimbingability,butthecockerswereturninginanequallygoodperformance.Whatactuallyhappenedwasthatthebasenjisreactedsuspiciouslytothestrangeobjectsplacedintheirpen,andtendedtoapproachtheboxesslowlyandcautiously,finallyjumpingorclimbingtothetop.Theyalsoshowedverylittleim-provementinpreliminarytraining.Ontheotherhand,thecockersshowednofearofthetestequipmentandusuallybackedoffandranrapidlyattherampsothattheirmomentumwouldcarrythemtothetop.Theresultwasthatthecockersactuallyhadalowerpercentageoffailuresthanthebasenjis,exceptonthefirsttrialandonthehighestsetofboxes.Beaglesandfoxterriersfellintosecondrankwithaboutthesamepercentageoffailures.Bothbreedsshowedupbadlyonthe4-and5-footstacks.TheShetlandsheepdogswereoutstandinglypoorallthewaythroughthetest,apparentlybeingquitefearfulofheightsandbeingrelativelylittleinterestedinthefoodrewardundertheseconditions.Theywereapproximately95percentunsuc-
cessfulonthemostdifficultpartsofthetest.Theoyer-allresultscanbeevaluatedbythechi-squareanalysis.Significantbreeddifferenceswereobtainedonalltrialsat5feet(P—.001).
Themostinterestingpartoftheseresultsisthewayinwhichtheanimalsorganizedtheirabilitiestomeettheactualsituation.Thebasenjiswiththeirsuperiorheightandjumpingabilitywereobviouslysuperiorinclimbingability.Yetthecockers,byorganizingtheirowncapacities,wereabletocompetesuccessfullyexceptunderthemostextremeconditions,andeventhenthedifferenceswerenotgreat.Onthemostextremetest,withtheboxesstackedto5feet,62percentofthebasenjissucceededagainst44percentofthecockers,adifferenceofonly18percent.Thetestisnot,therefore,afavorableoneforgeneticanalysisthroughthecrossbreedingexperiment.Nevertheless,theperformanceofthehybridswasofconsiderableinterest.TheFihybridsdifferedconsiderablyfromeachother
222BREEDDIFFERENCES
andtendedtoresembletheirmothers.Thebasenjibackcrosseswereverysimilartobasenjis,andtheF2'ssomewhatintermediatebetweenthetwobreeds.Thebackcrossestothecockersmadebyfarthebestrecordsinthepreliminarytrainingphaseoftheexperiment,butmadetheworstrecordonthemostdifficulttrial.Wemayconcludethattherearetwogenetictendenciesoperatinghere.Oneisthecapacityofthecockertorespondquicklytothetypeofmotivationaltrainingusedinthisexperiment,andtheotheristheclimbingandjumpingabilityofthebasenji.Thesetwointeractincomplexways.
SUMMARY
Theresultsofalltrainingtestsindicatethattheabilitytorespondsuccessfullytotrainingishighlyspecific,withtheresultthattheexpressionofanyoneabilityishighlydependentuponthetypeoftrainingused.Furthermore,itappearstobeextremelydifficulttodeviseatestwhichmeasuresonlyonesimplecapacity.Evenwhenthepuppieswerebeingtrainedtobequietonthescales,thecockerspanielsrespondedwiththeirtendencytosit,whilethefoxterriersemployedanothercapacity,thatofreactingaggressively.Theleash-controltestbroughtoutboththecharacteristicresistancetorestraintofbasenjisandthesheepdogtendencytocrowdnexttoaperson,ortoasheep.Inshort,inanyparticularsituation,apuppyorganizesthecapacitieswhichithappenstopossess,usuallyselectingthecombinationwhichgivesthebestresults.Thiswasespeciallyevidentinthemotor-skilltest,inwhichcockerspanielswereabletocompensateforalackofjumpingabilitybysuperiormotivationandeffort.
Whereithasbeenpossibletomeasurethecomponentsofbehaviorinvolvedin
Whereithasbeenpossibletomeasurethecomponentsofbehaviorinvolvedintraining,itisobviousthatemotionalreactionshaveahighlyimportanteffect.Suchreactionsappearnotonlyinthespecialsituationsdevisedtotestthem,asdescribedinchapter8,buttheyalsoeitherfacilitateorinhibittrainingofalmostanysort.
Theimportanceofbreeddifferencesvariedfromtesttotest,rangingfromverylargedifferencesintheleash-controlteststononeinretrieving,althoughinthelatteritmighthavebeenpossibletodemonstratedifferencesbyselectingamorefavorableagefortraining.
Traininghasvariouseffectsupontheexpressionofbreeddifferences.Inthequietingtest,trainingactuallyincreasedthemagnitudeofdifferences.Inmosttests,themagnitudeofdifferenceswasdecreased,buttheproportionofvarianceattributabletobreedmight
neverthelessremainconstant,asitdidintheleash-trainingandobediencetests.Demandingahigherdegreeofperformanceafterpreliminarytrainingmayincreasethemagnitudeofdifferences,asitdidinthemotor-skilltest.
Finally,eachtestoftrainingbroughtoutindividualconclusionsofgreatinterest.Theobediencetest,forexample,showedthatdogsofallbreedstendtogeneralizetheirtrainingfromonehandlertoanother,givingnosupporttothe"onemandog''theorv.Whethersuchdogsactuallyexistinotherbreedsindependentofdifferentialtrainingisanopenquestion.Theleash-trainingtestshowedbreeddifferencesthroughouttheperiodoftraining,buttheforminwhichthesedifferenceswereexpressedvariedastrainingprogressed.Inshort,theeffectofhereditvupontrainabilitvishighlycomplex,bothbecauseofthenumberofspecificbasicabilitiesinvolvedandbecauseofthecomplicatedinteractionbetweenthemmadepossiblebybehavioraladaptation.
THEDEVELOPMENTANDDIFFERENTIATIONOFPROBLEM-SOLVINGBEHAVIOR
Anewbornpuppycannotsurvivewithouttheconstantcareofitsmotherorofaconscientioushumancaretakeractingasasubstitutemother.Untilthepuppyemergesfromthenestboxatabout3weeksofage,lifeoffersfewchallengesandweseelittleevidenceofproblemsolving.Thisdoesnotmeanthatthepuppylearnsnothingduringthese3weeks.Thereissomeevidencethatsimplediscriminationsareacquired,andweknowthatmaturationofthesensoryandmotorsystemsisoccurringduringthistime.Thepointisthatunderordinary
motorsystemsisoccurringduringthistime.Thepointisthatunderordinaryconditionsproblem-solvingbehaviorisnotconspicuousandishardtodemonstrateunderexperimentalconditions,perhapsbecausecriticaltestsaredifficultinananimalwithrestrictedresponsecapacities.
At3weeksofagealargenumberofbehavioralchangesoccur.Ofparticularimportanceistheappearanceofthecapacitytoformstableconditionedreflexeswithrapiditycomparabletothatofanadult.However,theretinaisstillundeveloped,andthepuppyisunabletoperceivedifferencesindepthuntil4weeksofage.ChangesinthealpharhythmoftheEEGindicatethatfullvisualcapacityisnotreacheduntil7to8weeks.Moreover,motorabilitiesarestillundeveloped,sothatapuppyisclumsyandtireseasily.Consequently,6weeksofageisveryclosetotheearliestpracticaltimeforadministeringaproblem-solvingtest.Forthenextfewweeksthepuppyisremarkablyadaptableandresponsivetoalmostanysortoflearningexperiencewhichhisdevelopingmotorcapacitiesandshortattentionspanwillpermit.
By4monthsthepuppyliasdevelopedintoanindependentcreaturewhocanfindhisownfood,negotiatecomplicatedpathways,and
224
PROBLEM-SOLVINGBEHAVIOR225
ingeneralcopewithordinaryenvironmentalchallenges.Thepuppyatthisageis,ofcourse,fartooyoungtohaveacquiredthespecializedabilitiesforwhichdogsarefamous,abilitiessuchassheep-herding,guidingtheblind,orperformingincircuses.Hecan,however,beeasilytrainedtoobevsimplecommandsandcansolvecomplicatedproblemsprovidedthatnohighlydevelopedmotorskillsorgreatendurancearerequired.
Eventhesimplesttrainingmaybeconsideredasaformofproblem-solvingbehavior.Fromamultitudeofpossibleresponses,thepuppymustlearntoselectthosebringingthelargestorthequickestrewardandtoavoidthosewhichresultinpainordiscomfort.Severaltrainingprocedureswereconsideredinthepreviouschapter.Hereemphasisisplaceduponmorecomplicatedtestsinvolvingspatialrelationshipsandvisualcues.Attentionwillbegivenalsotothebarriertest,manipulationtest,andthemazetest,whichwerecarriedoutwithyoungersubjectsinanefforttolearnmoreaboutthedevelopmentofproblem-solvingability.
DEVELOPMENTOFPROBLEM-SOLVINGBEHAVIOR
Severaldifficultiesbesettheinvestigatorwhoattemptstostudythedevelopmentoflearningintheyoungpuppy.Thenewbornsubjecthasfewsimpleresponses,andonecandemonstratelearningonlybyanincreaseordecreaseinthefrequencyofoneofthesefewpatterns.Inolderpuppies,thecapacitiesforresponseareenormouslygreateranditiseasiertoshowwhetherornotaparticularresponseoccursasaresultoflearning.
Itisdifficulttonotetheexacttimeoftheappearanceofanyparticularlearningcapacity.Complextaskscannotbemasteredsuddenlyevenbyexperiencedsubjects,andattainingacriterionlevelrequiresmanytrials,oftenspacedoveraconsiderableperiodoftime.Shouldweestablishourcriterionofmaturationasthedayonwhichthepuppyfirstmeetsourstatisticalrequirementforlearning,orasthedayonwhichtrainingisbegun?Ifittakesapuppy2weekstodemonstratethathehaslearnedaparticulartask,wecannotdeterminetheageatwhichtheabilitywasacquiredmorepreciselythansometimewithinthe2-weekperiod.Obviously,greateraccuracyispossiblewhentestingisrestrictedtosimpleproblemspotentiallysolvablewithinafewtrialsconductedinoneday.Undersuchconditions,maturationalchangesoccurringduringtheperiodoflearningcanbeneglected.Suchrestrictions,however,eliminatethemostinterestingmaturationalproblems.
Sinceourexperimentwasdesignedprimarilytodetectdifferencesinproblem-solvingbehaviorattributabletoheredity,wedonothavedatatodemonstraterigorouslytheageatwhichvariouskindsoflearningbecomepossible.StudiesonmonkeysbyMasonandHarlow(1958a)andbyHarlow(1958)withthisobjectiveusedthesameproceduresbeginningatdifferentagesongeneticallysimilarsubjects.Severalstudiesfromourlaboratoryhavebeenconcernedwithlearninginnewbornpuppies(Fuller,Easier,andBanks,1950;Corn-wellandFuller,1960).Inordertoevaluatehereditaryfactors,however,itwasmorepracticaltogiveeachtestataparticularage.Toanextent,ourseriesoftestsrepresentstepsofincreasingdifficultycorrespondingtotheincreasedmaturityofoursubjects.Itwouldhavebeeninteresting,hadourresourcesbeenunlimited,tohaveinvestigatedboththegeneticandagevariables,sincesomeofthebreeddifferencesfoundmayhavebeensimplymanifestationsofdifferentratesofdevelopmentandwouldhavedisappearedifourtestshadbeencarriedoutatalaterage.Suchaninteractionbetweenrateofdevelopmentandheredityisprobablymoreimportantinyounganimalsthaninolderones.Wemust,however,rememberthatthereisapossibilityofsometransferofeffectfromone
however,rememberthatthereisapossibilityofsometransferofeffectfromonesituationtoanother.Conceivably,puppieswhofailedintheirfirsttestsbecauseofimmaturityalsodidpoorlyinlatertestsbecauseoflackofmotivation.Thus,far-reachingeffectsmightfollowfromsuchseeminglytrivialfactorsastheexactschedulingofthetests.
BARRIERORDETOURTEST
Thebarriertestwhichwasgivenat6weeksofagewasthefirstperformancetestforthepuppies.Itwasalsotheirfirstexperienceoutsidetheirownrearingroom,asidefromtheconfinementthattheyexperiencedinsmallcagesinthehallwhiletestswerebeingsetupinside.Consequentlywehadanopportunitytoexperimentwithatotallyunsophisticatedpuppy,andweattemptedtodevelopatestwhichwouldbesuitableforanimalsofthisageandatthesametimeshowuswhetherornottherewassomenativeproblem-solvingabilitywhichdidnotdependonpreviouslearning.
ThetestwasbasicallythesameasthedetourproblemdevisedbyKoehler(1927)foravarietyofanimals,anddetailsofpreliminarytraininghavealreadybeendescribedinchapter1.ThefirstrealproblemwaspresentedonDay3.Onthisdaythepuppyfoundabarrierbetweenhimandthedishoffood.ThisbarrierwasawoodenFrame,0feetlongand3feethigh,coveredwithpoultrywire,and
PROBLEM-SOLVINGBEHAVIOR
227
madeopaquewithheavypaperexceptforaslitonefootwideimmediatelyinfrontofthepuppy.Thusthepuppycouldseethefoodandtheexperimenter,butithadtomoveawayfromandoutofsightofthefoodinordertoreachthisreward.Theendsofthebarrierwereclearlymarkedbysupportswhichextendedoutonthepuppy'ssideofthebarrier.
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Fig.10.1.—Problemsinthebarriertest.Thistestwasperformedinanarena12X27feetinsize.Thebarrierwasopaque,exceptforawire-coveredopeningonefootwideimmediatelyinfrontofthegoal.Inordertoreachthegoal,thepuppyhadtomoveawayfromit.
Apuppycouldmakeaperfectscorebyrunningdirectlyaroundtheendofthebarriertothefooddish.Ifitstoppedorreverseditsdirectionanerrorwascounted.Inaddition,thetotaltimerequiredtoreachthefoodandthenumberofvocalizationsthatthepuppymadeineachminuteofthetestwererecorded.Ifthepuppydidnotgettothefoodwithin10minutes,theexperimentercalledthepuppyaroundtothefooddishandallowedittoeat.
Onthefourthdayofthetestthebarrierwasextendedoneitherendsothatitwasthreetimesaslongasonthefirstday.OnthefifthdaythebarrierswereconvertedintoaUshape,withonesideoftheUparalleltotheoriginalsideofthebarriersothatthegoalwasnowinadifferentlocation.Threetrialsweregivenoneachdayofthetest,andallpuppiesthushadanopportunitytolearnonesituationbeforeproceedingtothenext.
Itwasextremelyinterestingtowatchthepuppiesworkoutsolutionstothesesimpleproblems.Afewanimalsimmediatelyranaroundtheendofthebarrier,withoutmistakes.Othersranfirsttooneend,tookalook,thenreturnedtotheotherend,tookasecond
otherend,tookasecond
look,andthenrantothefood,usuallybackaroundtheendwheretheyfirststarted.Stillothersmovedonlyashortdistancefromthefood,whichwasofcourseinDiebehindthebarrier.Such
puppiessoonbegantorunbackandforthandtopawvigorouslybut:uallvonthewire,vocalizingastheydidso.Sometimesthiswouldgoonf:alminutes.Thenthepuppywouldstop,look
andrunaroundtheendtothefooddish.Vocalizationi^noffrustration,andnopuppiessolvedtheprob-whilevocalizing.
gdevelopedwithoutpreviousexperience:Anadultdogwouldimmediatelysolvesuchproblemsbvtakingonelookandrunningaroundthebarriertothefood.AsshowninTableI1.onlyavervfewpuppieswereabletodothis,someSoutofi3purebredpuppiestested.Ifthecapacityforsolvingadetourpreminfactbedevelopedwithoutexperience,thismusthave
occurredinonlyaverysmallproportionofpuppiesofanybreed.Ontheotherhand,ifthecapacityisdevelopedbvexperience,thereshouldbeamuchhigherpercentageofsuccessonthenextdaywhenorbutlongerbarrierispresented.Fourtimesasmanypuppiesmadeperfesonthefirsttrialofthesecondtestastheydidon
thefirst,andlargebreeddifferencesbegantoappear.Basenjisimprovedagreatdealmorethananyotherbreed,andbeaglesand1terriersweresecond.Thecockerspanielsandsheltiesshowednoimprovement.Thesediffere:emtoresultfrom
ditjnstofrustratingsituations.Basenjisatthisageare
usuallyhighlyactiveandwelldevelopedphysically,whilethepuppiesofmostotherbreedsarestillfatandclumsy.Inmar.thecodhfailedwouldsimplyliedownandgoto
sleepuntilthetestperiodwasover.ThebasenjisremainedactiveandEthusmorelikelvtosolvetheproblembvchar.
puppic_-.bletosolvethethirdproblem
apedbarrier|withouterrors.Eventhenumberofsuccessfulnsiderablvreduced.Thisindicatesthatpuppiesofthiselimitedcap.,aralization.Inoneofthepre-
liminaryexperiments,thestraightbar:simplyrotated1S0:in
thesameroom,andthepupp:edtothisasifitwereanen-
-ituatio:thedifl.Dnbetweenthebreeds
rer:Ecuterriersandbeaglesr.
andcockersandsheltiiL
.usionscon.g:helackofgeneralizationareborne
outbythecorrelationsbetweentlhenall
breedsandhybridsareconsidered,performancesonthelongand
PROBLEM-SOLVINGBEHAVIOR
229
TABLE10.1
NumberofAnimalswithExcellentPerformanceontheDetourTest—FirstTrialsOnly
Breed
Xt'MBER
Tested
XiuberofErrors
0■
Total
PerCent
shortbarriersarecorrelatedat.16,butthecorrelationbetweenperformancesonthelongbarrierandtheU-shapedbarrierisonly.07.Correlationswithinthepurebreedsandhybridsarehighlyvariable.ThebehaviorofthepuppiesindicatedthateasilylearningProblem1mightactuallybeahandicapindealingwithProblem2,becausethepuppymightturntoosoonwhenrunningaroundthelongbarrierandthusbecomeconfused,whereasananimalwhichhadmadeseveralmistakeswouldhaveexploredtheapparatusmorethoroughlyandthusrecognizechangesmorequickly.
MANIPULATIONTEST
Asweworkedwiththebasenjisweobservedthattheywereconsiderablymoreskillfulwiththeirpawsthantheotherbreeds,sometimesusingtheminanalmostcatlikefashion.Themanipulationtest
wasdesignedtomeasurethisdifferenceobjectively.Thepuppieshadbeenpreviouslytrainedtoruntoawoodenboxcontainingafooddish(seegoal-orientationtest,chap.9).Duringthefollowingweektheywereconfrontedwiththeproblemofremovingthedishfromthebox,whichwasnowcovered.
Onthefirstproblem,thetopoftheboxwascoveredwithhardwareclothsothatthepuppiescouldseeandsmellthefood,butcouldreachitonlvbvpullingornosingthedishoutthroughtheopensideofthebox.Onthefirsttrial,thedishprotrudedenoughsothatthepuppycouldeasilygetthefoodbystickingitsnoseintothetopofthedishandforcingitoutward.Verynearly100percentoftheanimalswereabletodothis.Thispreliminarytrainingwasrepeatedoneachdavofthetestsothatthepuppieswouldberewardedbysuccessandfoodatleastonceperday.
Ontheseconddav.thepuppvwentthroughthefirsttrialasbefore,butonthesecondtrialfoundthedishfartherbackinthebox,makingitmoredifficulttopullout.Onthethirdday,thedishwasstillfartherbackbutwasattachedtoasmallwoodendowelandastring,sothatthedishcouldbepulledoutwiththestring.Theanimalcouldalsopawitoutdirectly,butthiswasquitedifficulttodo.Thetestonthefourthdaywassimilartothatonthethird,exceptthatthedishwasstillfartherbackinthebox,makingitalmostimpossibletopulloutthedishexceptwiththestring.Finally,onthefifthdaythewholeproblemwaschanged.Thistimetheboxhadnobottom,anditsoneopensidewasagainstthewallsothatthepuppieshadtopulltheboxoffthedishratherthanpullingthedishoutofthebox.
dishoutofthebox.
Therewereavervlargenumberoffailures,sothatthetestisbestanalyzedintermsofproportionsofsuccessesratherthaninthoseoftimerequiredtosolvetheproblems.
AglanceatFigure10.2indicatesthattheperformanceofthebreedswasgenerallvconsistentonallpartsofthetest.Basenjisalwaysdidthebestandcockerspanielstheworst.Beagles,wire-hairedterriers,andsheltieswereintermediate,theirrelativeranksfluctuatingsomewhat.Thechiefeffectofthedifferentformsoftheproblemapparatuswasthatthepresenceofthestringmadethesolutioneasierforallbreeds.
Oneofthemostinterestingobservationswastheeffectofrepeatedfailureuponthebehaviorofanyparticularanimal.Onthefirstfailureitwouldpersistentlytryavarietyofwavstogetatthefood,scratching,nosing,andevendraggingtheheavyboxaround.Onthesecondtrialitwouldmakeamuchbrieferattempt,andbythethird
PROBLEM-SOLVINGBEHAVIOR
231
orfourththepuppywouldusuallygouptothebox,takeonelook,andthenreturntothegatetowaitouttheremainderofthetwominutesallottedtothetrial.Thustheanimalveryquicklyformedhabitswhicheffectivelypreventedanyfuturesuccess.Thispointsuptheimportanceofsuccessinenhancingmotivation.Theresultsare,ofcourse,consistentwiththeknowneffectsofreinforcementonthemaintenanceorextinctionofconditionedresponses.
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Fig.10.2.Resultsofmanipulationtestonsuccessivedays.Notethatbasen-jisareconsistentlythebest,cockerstheworst.
Thesignificanceofthisphenomenoninrelationtotheeffectofheredityuponbehavioristhatitdemonstratestheimportanceofmaintaininghighmotivationinordertobringoutthemaximumgeneticcapacitiesoftheindividual.Ifananimalissubjectedtoaproblemevenslightlybeyonditspowersattheoutset,itmaysimplylearntoinhibitapproachandmanipulativebehaviorwhichhasnotbeenreinforced.Aslightlylessdifficultproblemattheoutsetoftrainingcouldmakethesameanimalintoahighlypersistentindividual.Weobservedthatapuppywhichhadconsistentlysucceededinthistestforseveraltrialswouldrespondtoadifficultproblemwithanalmostdesperateeffort,andwouldstillbeattackingtheboxattheendofthe2-minuteperiod.
Becausethereweresomanyfailures,wecontinuedthetestinan
232BREEDDIFFERENCES
attempttofindoutwhetherdogscouldlearnbyfollowingahumanexample.Theanimalswhichfailedweredividedintotwogroups,experimentalsandcontrols.Withtheexperimentalsthehandlerattemptedtoshowthepuppythesolutionbyscratchingontheboxwithhisfingerandmovingit.Manypuppiesbecameveryexcited,andsometimesjoinedinthescratching.However,therewaslittleevidencethatthepuppieslearnedtoperformthetaskindependently.Somepuppiescouldprobablybetaughtinthiswaywithconsiderabletimeandpatience,butthemethoddoesnotworkefficiently.
AMAZETESTFORDOGS
Bytheageof13weekspuppieshavealargerepertoryofresponsesandcanlearnspatialrelationshipswithconsiderablespeed.Atthisagetheywereintroducedtoa2-weektestingperiodona6-unitmaze.Thepatternofrightandleftturnsinthismazecouldbereadilyreversed.Halfthepuppiesfromeach
leftturnsinthismazecouldbereadilyreversed.HalfthepuppiesfromeachlitterweretestedwiththearrangementRLLRRRandtheotherhalfonLRRLLL(Fig.10.3),thepuppiesbeingalternatedsothatanyscentcuesfromthepreviousanimalwouldbeconfusing.
Themazewasconstructedofwoodenframescoveredwithpoultrymeshinanattempttosimulateapathwaythroughadensethicket.Previousexperimentswithenclosedmazeshadnotworkedwellbecauseofthepuppies'apparentdistresswhenconfinedwithinopaquebarriers.
OntheMondayclosesttoits13-weekbirthday,thelitterwasbroughttoaholdingcageoutsidethetestingroom.Eachpuppyinturnwasplacedinthefinalsectionofthemazeandallowedtoemergeandeatasmallportionoffoodwhiletheexperimenterstoodby.TheprocedurewasrepeatedonTuesdayinordertohabituatethesubjectstothetestsituationandtobuilduptheirmotivationtoreachthegoalbyrepeatedreinforcement.Judgingfromtheirbehavior,thepuppiesweremotivatednotonlybythefoodbutalsobyescapefromarestrictingspaceandbytheopportunitytocomeincontactwiththeexperimenter.Asecondperson,theobserver,satonaraisedplatformbehindascreenandrecordedthesubject'sresponses.
MazerunscommencedonWednesday.Theexperimenterplacedthepuppyintheinitialsection,thenwalkedrapidlyaroundtheoutsideofthemazeonthesidewiththemostblindalleys.Experimentersweredirectednottoattracttheattentionofthesubjectsor
PROBLEM-SOLVINGBEHAVIOR
toprovideanycuestothecorrectpathatthesuccessivechoicepoints.
Recordsweremadeofthetimeinsecondsrequiredtorunthemazeandofthenumberoferrors,definedeitherasreversalsorcompletestops.Eacherrorwasrecordedonaplanofthemazeas
FINISH
Fig.10.3.—Floorplanofthemazetest,left-handpattern.Externalprojectionsresultedfromtheuseof6-footsectionsinerectingthemazeandhadnoeffectontheperformanceofthepups.
aconsecutivenumber,sothatalinedrawnbetweenthemwouldgiveacomplete
aconsecutivenumber,sothatalinedrawnbetweenthemwouldgiveacompleterecordoftheanimal'smovementsthroughthemaze.Theaveragerunningtimeanderrorscores(excludingDay1)weretakenastheprincipalmeasuresofindividualperformance.However,thesecompositescoresgaveaninadequatepictureofperform-
234BREEDDIFFERENCES
anceonthemaze.Forexample,ananimalwhichlearnedthemazegraduallyandslowlywouldreceiveapproximatelythesameaverageerrorscoreasonewhichmadealargenumberoferrorsatfirstandthenmadeaquickreductionandranconsistentlythereafter.Also,onthebasisofotherperformancetests,weexpectedthattheprincipalgeneticdifferenceswouldshowupinthewaysinwhichtheanimalssolvedtheproblemratherthantheendresult.Wethereforescoredthetestsinmanyways.
Asitturnedoutsixofthese,inadditiontotheaveragetimeanderrorscores,showedimportantbreeddifferences.Thesewere:(1)minimumtime;(2)minimumerrors;(3)rangeoftime(probablyreflectingminimumtime);(4)rangeoferrors(relatedtominimumerrors);(5)thespeedscoreonthefirstday;andfinally(6)thehabitscore,whichreflectedthetendencyoftheanimaltoformastereotypedpatternofrunningthroughthemazeduringthelatterpartofthetest.Inaddition,duringthefirsttwodaysofpreliminarytraining,theobservergavethesubjectsaconfidenceratingbasedonbodypostureandtailcarriagejustafterthepuppiesfoundthemselvesinthemaze.Thisgaveanopportunitytomeasurethepossibleeffectsofemotionalresponsesonmazeperformance.
Whenfirstintroducedintothemaze,apuppyusuallyattemptedtofollowtheexperimenter,thenstoodforamomentbythewiremesh,andfinallybegantorunaroundrapidlyinsidetheapparatus,apparentlysearchingforawayout.Ifhewasnotimmediatelysuccessful,hemightbecomeemotionallydistressedandbegintoyelp.Aswithpuppiesonthefirstbarriertest,behaviorbecamequitestereotypedatthispoint,thepuppyrunningbackandforthandpawingatthebarriers.Foxterrierssometimestriedtobitetheirwayout.Finallythepuppywouldworkitswaythroughthemaze,eatthefish,andbecarriedbacktoitslittermates.
Onsubsequentdays,performanceimprovedrapidly.Afewsubjectsafter4or5trialswereabletosolvethemazevisuallybyobservingthepathaheadthroughthetransparentwalls.Butcareful,slow,errorlessprogressionthroughthe
thetransparentwalls.Butcareful,slow,errorlessprogressionthroughtheapparatusneverpersisted,becausetheseanimals,likeotherswhichneverdevelopedavisualsolutionatall,soonadoptedastereotypedhabitofalternatingrightandleftturns,thusmakingtwoerrorsoneachtrial.Afewindividualsformedthehabitofalwaysturningtoonesideeventhoughthismightinvolveentering4blindalleyspertrial.
AverageerrorsandtimesforthefivepurebreedsareshowninFigures10.4and10.5.Thetwofamiliesofcurvesareverysimilar,anddifferencesbetweenbreedsaremanifest,particularlyduring
PROBLEM-SOLVINGBEHAVIOR
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BREEDDIFFERENCES
thefirstdays.ElliotandScott(1963)performedacomplexanalysisofcovarianceonthisexperiment,takingintoaccountthepossibleeffectsofbackgroundconditionssuchasconditionsoftestingandrearing.Inthisdetailedanalysisofthedata,thevarianceassociatedwithbreeds,matings,litters,andindividualswascalculatedforeachscore.Inaddition,theproportionsofvariancerelatedtoenvironmental,error,andbackgroundfactorswerecalculated.Theseincludedroomtemperature,ageofmother,orderoflitter,littersize,sexoflittermates,sex,bodysize,andemotionalfactors(measuredbvtheconfidencerating).
TABLE10.2
PercentageofTotalVarianceofMazeScoresRelatedtoBreed,Mating,Litter,andBackgroundVariables
MinimumTime
MinimumErrors
Range
Time
RangeErron
Habit
jpeed
Sumofsquares
Breeds:
Total
Residual
Habit*
Background
Matings
Litters
Individual:
Habit*12
Background8
Sumofexplainedvariance55
Remainingunexplained
individualvariance45
7
9
56
44
4
3
49
51
3
3
48
52
517
99
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118
6
34
66
458
3810
4
2411
9
6
771
29
Portionsofbreedandindividualvariancerelatedtohabitscore.
Whenthebackgroundvariancewassubtracted,therewerenosignificantbreeddifferencesintheaverageerrorandtimescores,confirmingouroriginalimpressionthattheseareinadequatemeasuresofperformance.Significantbreeddifferencesremained,however,intheminimumtimeandminimumerrorscoresandinthespeedscoreonthefirstday—theremainingvarianceduetobreedrangingfrom11to15percentofthetotal.Significantdifferencesalsoremainedintherangeoferrorsandrangeoftimesconwellasthehabitscore,forming7to9percentofthetotal(Table10.2).Incontrast,thetotalvarianceduetobreeds,includingthatassociatedwithbackgroundfactors,wasintheneighborhoodof20percentformostofthese6measuresofperformance,althoughthatofthehabitformationscorewasonlv9percent,duetothefactthatalmostallthedifferenceswerecausedbyonebreed,thebeagle.
PROBLEM-SOLVINGBEHAVIOR237
Thehighestproportionofexplainedvariance,71percent,wasobtainedwiththespeedscore,whichisbasedonthefirstday'sperformance.Theothervariables(compoundedfromseveraldays'scores)standatapproximately50percent.Thedifferenceisaccountedforbythelargeeffectofbackgroundfactors(24percentofthetotalvariance)associatedwithbreedonthespeedscore.Wecanconcludethatbackgroundfactorsassociatedwithbreed,suchaslittersize,orderoflitter,ageofmother,waistcircumference,confidence,andtemperature,havetheirmaximumeffectonthefirstday'sperformance.Thissuggeststhatsuchfactorsmighthaveanimportanteffectonsuccessmotivationintestsinwhichinitialfailureswerepermitted,suchasthemanipulativetest.
Inmostofthemeasures,thereisabout50percentofunexplainedindividualvariance,presumablycausedbyindividualgeneticfactorsandunmeasuredenvironmentalfactors,suchaspreviousexperienceandrandomdistractions.To
environmentalfactors,suchaspreviousexperienceandrandomdistractions.Totaketheminimumtimescoreasanexample,aboutone-fifthofthetotalvariance(19percent)isassociatedwithbreeddifferences.Ofthis,aboutone-fifthiscausedbymiscellaneousbackgroundvariablespeculiartothebreeds—sex,sizeoflitter,andorderoflitter.Differencesbetweenmatingswithinabreed,whicharealsopresumablygeneticinorigin,accountfor12percentofthetotalvariance.Excludingthevarianceassociatedwiththehabitscore,thevariancewhichcanbedefinitelyassignedtogeneticfactorsis21percent,plusanunknownamountofindividualgeneticvariancewithinthebreeds.
Fromthesedataonecancharacterizethebreedsinthefollowingways,rememberingthatconsiderableoverlapexists.FoxterriersandShetlandsheepdogsmakemoreerrorsandconsequentlyshowlongertimesthantheotherthreebreeds.OnthefourmeasuressummarizedinFigure10.6,beaglesappeargenerallysuperiorandShetlandsheepdogsinferior,withtheotherthreeintermediate.Thesuccessofbeaglesisattributedtotheiravoidanceofstereotypedhabitsandcharacteristicrapidrandominvestigationoftheirsurroundings.Althoughtheyoftenresultinpoorinitialperformance,theseformsofbehaviorcontributetorapidsolutionofthemaze.TheShetlandsheepdogsappearedtimidandhesitantinthemazeanddevelopedstrongstereotypedhabits.Theothernotablefeatureofthedataisthegoodperformanceofbasenjisonthefirstday.Basenjisappearmoreobservantandlessexcitedthantheotherbreeds,asifmakingmoreuseofvisualcues.
Thusheredityseemstoaffectperformanceinthistestlargelybydeterminingemotionalreactionsaffectingconfidenceandthechoice
BREEDDIFFERENCES
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Fig.10.6.—Relativeperformanceofdifferentbreedsinthemaze.Bestperformersattopofscale.X'sdenotemeansofallbreeds.
ofbehaviorpatterns.Theactualorganizingprocessesinthecentralnervoussystemseemtobelittleaffected,exceptinthecaseofthetendencyinallbreedsexceptthebeagletoformstereotypedhabitsrapidly.
CUERESPONSEANDDELAYEDRESPONSE
Eachofoursubjects,beginningat22weeksofage,wasgivenaseriesofthreerelatedtestsinaT-mazeinordertodiscoverwhateffectgeneticdifferencesmighthaveonthisformofproblemsolving.Animportantpartofsolvinganyproblemistheassociationofparticularcueswithappropriateresponses,orlearningtodiscriminate.LearningtogooncuetoonearmortheotherofaT-mazetoreceiveafoodrewardisrepresentativeofthisbasicclassofproblems.
TheapparatusisshowninFigure10.7.Subjectswererestrainedinthestartingbox,whichhadameshdoorandpermittedaclearviewoftherunwayandthediscriminativecues.Thesewere12X30-inchhingedpanels,eachpaintedblackwitha3-inchwhitestripedownthemiddleandmountedattheentrancestotheescapecor-
PROBLEM-SOLVINGBEHAVIOR239
PROBLEM-SOLVINGBEHAVIOR239
ridoroneachside.Bypullingcords,theexperimentercouldmoveonepanelortheotherthroughanarcofabout30°.Movement,ratherthanlevelofilluminationorpattern,waschosenasthediscriminativestimulusbecausedogsattendreadilytomotion,anditwashopedthatlearningwouldbemorerapidthanwithconventionalstationarystimuli.Themovingpanelalsomadesomenoisewhichservedtoattracttheattentionofthesubjects.
Fig.10.7.—T-mazeusedforcue-response,discrimination,anddelayed-responsetests.
Abarrierextendingdownthemiddleoftherunwayforcedsubjectstochooseasidebeforetheycouldseewhichofthecorridorswasopen.Thebarrierwashingedsothataportioncouldbeswungtoeitherside,thusblockingoneoftheexitcorridorsandforcingtheanimaltogototheoppositeside.Equalnumbersofforcedtrialstobothsideswereusedasatrainingprocedureforthreedaysbeforediscriminationtestingwasbegun.Forcedtrialswereinterposedunderspecifiedrulesintothediscrimination-learningserieswhenspatialpreferencesseemedtobeinterferingwithlearning.Inordinarytesttrials,retracingandcorrectionoferrorswaspermitted.
Afteremergingfromtheapparatus,dogscouldruntothevicinityofthestartingboxandreceivefood.Somedogs,includingsomewhichlearnedreadily,seldomateinthetestsituation.Escapefrom
BREEDDIFFERENCES
themazeenclosureandhandlingbytheexperimenterwereapparentlysufficientinsomeinstancestomotivateacquisitionofadiscriminatedresponse.
Preliminarytraining(motivationtest).—Thethreedaysofpreliminarytrialsservedadualpurpose,habituationtotheapparatuspreparatorytodiscriminationtrainingandatestofmotivationaldifferencesbetweenbreedsandhybrids.Oneachofthreeconsecutivedays,thesubjectsweregiven10forcedtrialsintheorderofRLRRLRLLRL.Themovingcuewaspresentedoneachtrial;timewastakenfromtheopeningofthestartinggatetoemergencefromtheapparatus.Theresultsofthistestwereusedinchapter7toillustratethemethodofcomputingstaninescores.Forcertainpurposes,wehavealsochosentopresentresultsasspeedscoresobtainedbymultiplyingby1,000thereciprocalofthetotaltimeinsecondsfor10trials.
TheaveragestaninescoresforthethreedaysaresetforthforeachbreedinFigure10.8.Allbreedsshowday-by-dayimprovement,andthefivepurebreedsformtwodefiniteclusters:beagles,foxterriers,andspanielsrunfasterthanbasenjisandShetlandsheepdogs.
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PROBLEM-SOLVINGBEHAVIOR
241
Cueresponse(discrimination).—Onthedayfollowingcompletionofthemotivationtest,testingforadiscriminatedresponsewasbegun.Eachsubjectwasgiven16trialsperdaywiththebarrierinacentralpositiontoallowrunningtoeitherside.Twoseriesoftrialsweregiven:thefirstterminatedeitherwhenacriterionoflearningwasattainedorafter128trials;thesecond,givenonlytosubjectswhichmetthecriterion,consistedof50additionaltrials.InordertoequalizeinsofaraspossiblethelevelsofperformanceattheendofSeriesI,threeindependentlysufficientcriteriaweresetupforitstermination.Arunofconsecutivecorrectresponses,computedaccordingtothetablesofGrant(1947),wastheusualbasisfora"pass."Inthissystem,thelengthofthecriterion-runincreasesastotaltrialsaccumulate.Asecondcriterionwas14correctoutofthe16trialsononeday.Finally,attheendofthe128trials(theupperlimit),atotalof79ormorecorrectresponsesovertheserieswassufficienttoindicatebetterthanchanceperformanceatthe1percentlevelofsignificance.The50additionaltrialsgiventosubjectswhichmetthecriterionmeasuredconsistencyofresponseandprovidedsomeoverlearningaspreparationforthede-laved-responsetestwhichfollowed.
Performanceonthecue-responsetestcanbemeasuredinseveralways.InTable10.3aredataontheattainmentofthecriterionbythefivepurebreeds.
TABLE10.3AttainmentofCriterioninCue-ResponseTest
Thevalueofthechisquareforcomparinganimalsmeetingthecriterionbeforetrial64withallothersis22.686with8degreesoffreedomandP<.01.Becauseofthesmallexpectednumbersinsomecells,comparisonsbetweenbreedsaresomewhatrisky;butitissafetoconcludethatourstrainofShetlandsheepdogswasnotasgoodindiscriminationaseitherwire-hairedterriersorbeagles.
Onedifficultywiththetechniqueoftrainingtoacriterionisthat
242BREEDDIFFERENCES
somesubjectsdidnotlearntheproblemduringthelimitednumberoftrialswhichcouldbeallowedforanyoneprocedure.Inretrospect,webelievethatmanyofthefailureswouldhavemetthecriterioniftraininghadbeencontinuedfortwoadditionaldays(160trialstotal),buttherulescouldnotbechangedinthemiddleoftheexperiment.
Thetotalnumberofcorrectresponsesisanothermeasureofperformancewhichhascertainadvantagesbecauseeveryindividual,includingfailures,receivesadeterminatescore.Undertherulesofprocedureadopted,itwaspossibleforasubjecttocompletethetestinfourdaysbymeetingthecriteriononthefirstdayandreceiving50confirmatorytrialsonthefollowingthreedays.Sincesomesubjectsweretestedonlyfortheminimumof64trials,wehavecalculatedtheresultsintermsofcorrectresponsesoutof64.Afewanimalsacquiredthediscriminatoryresponseduringthepreliminarytrainingwithforcedrunsandobtained60ormorecorrectresponsesoverthefourdays.Others,particularlyamongthebasenjisandShetlandsheepdogs,werestillperformingatachancelevelafterfourdays.Onlystaninescoresof7orbetterindicatesignificantlearning,butscoresinthemiddlerangemayrepresentanimalsonthewaytomeetthecriterion.
Meanstaninescoresforcorrectresponsesoverthefirstfourdaysofcue-responsetrainingwere:wire-hairedterriers5.95;beagles,5.75;cockerspaniels,4.58;Shetlandsheepdogs,4.42;andbasenjis,4.39.Nonedeviatefarfromthemean,andtheoveralldifferencesbetweenbreedswerenotsignificant.Amongspaniels,sheepdogs,andbeagles,however,individuallittersdeviatedsignificantlyfromthebreedmeans.Whetherthiswascausedbycommonexperientialfactorsorbycharacteristicsofaparticularmatingisnotknown.
Delayedresponse.—Subjectswhichmetthecriterionforcueresponsewere
Delayedresponse.—Subjectswhichmetthecriterionforcueresponseweretestedinthesameapparatusondelayedresponse.Forthisprocedure,theappropriatepanelwasmoved,acurtainwasthendroppedoverthedooroftherestrainingcage,andthedoorraisedfollowingaspecifiedintervaloftime,afterallpanelmotionhadceased.Thesubjectwas,bvthisprocedure,forcedtorespondintheabsenceofthediscriminativestimulus.Thedelayed-responsetest,originatedbyHunter(1913),hasbeenwidelyusedtoassesstheresultsofbrainlesions,particularlyinthefrontalregions,andwewereinterestedinpossibledetectionofhereditarydifferencesinbrainfunction.
Obviously,therearemanydifficultiesinageneticexperimentinapplyinganytestwhichdependsuponpriortraining,andespecially
PROBLEM-SOLVINGBEHAVIOR
243
whensubjectsareeliminatedbylackofsuccessinpreliminarytraining.Norealmeasureofdelayedresponsecouldbeobtainedfromsubjectswhichdidnotmeetthelearningcriteriaofthecue-responsetest.Yetwecannotconcludethatthesenon-learnersweredeficientinattributesmeasuredbydelayedresponse,forthegroupofanimalsreceivingdelayed-responsetrainingwasabiasedsampleofourtotalgroup.Hence,itisimpossible,onthebasisofourexperiment,tocometodefiniteconclusionsregardingthedistributionofdelaved-responseabilityamongdogbreeds.However,thedataarestillofinterestbecauseofthegreatamountofindividualvariationshown.
TABLE10.4Delayed-ResponsePerformanceofFivePureBreeds
Thedelayed-responsetestwasdesignedasa"power-test"toprobetheupperlimitofeachdog'sability.Thus,themeasureadoptedwasthemaximumlengthofdelayinsecondspermittingacorrectresponseintheT-mazeundertheproceduredescribed.Delayintervalswere1,5,10,15,30,60,120,and240seconds.Amaximumof40trialswasallowedtomeetthecriterionat1-seconddelay;30trialswasthelimitforlongerdelays.Oncealevelwasfailed,testingwasdiscontinued.AsummaryoftheresultsofthistestisshowninTable10.4.Itisapparentthattherangeinanyonebreedisgreat.Amongthecockerspaniels,oneindividualpassedthetestatadelayof240seconds,anintervalwhichplacedastrainonthememoryoftheexperimenters,but32percentwereconfusedbythebriefestpossibledelay.TheShetlandsheepdogshadthepoorestrecord,but
thebriefestpossibledelay.TheShetlandsheepdogshadthepoorestrecord,butsofewweretestedthatitisnotlegitimatetoconsiderthemasanadequatesampleofthebreed.Infact,noover-alldifferencesbetweenthebreedscanbedemonstratedbythechi-squaremethod.Oncetheoriginalhurdleoflearningthediscriminationissur-
244BREEDDIFFERENCES
mounted,theprobabilityofsuccessondelayisaboutequalforallbreeds.Itisnotequalforalldogs.Over28percentfailtomeetcriterionontheshortestdelay,andabout32percentareabletomeetonlythisrequirement,failingonlongertrials.About40percentcandelay5secondsormore,whileanoccasional"genius"reaches60,oreven240seconds.Partofthesuccessisduetotheholdingofafixedattitudeduringthedelay.Theanimalaimsitselfwhenthestimulusispresentedandpullsthetriggerlater.Thisisnotthewholestory,however.Somesubjectswithsuccessatlongdelaysactuallycircledintherestrainingcageduringthedelay,andmanymovedtheirheadsfromsidetosideorpawedatthestartinggate.Thepointofthisexperimentisthatapower-testcanuncovergreaterindividualdifferenceswithinaspeciesthandoesatestoflearningwhichiswithintheabilityofallsubjects.Otherexperimentsinourlaboratoryhaveshownthatevenprolongedpracticedoesnotappreciablyincreasethemaximumdelayed-responsetimeofadog.Understabletestingconditions,ananimal'slimitfluctuateswithinarelativelynarrowrange,perhapsbetween15and20secondsorbetween20and30seconds.Butthistestwithitsdemonstratedabilitytodetectindividualvariationfailedtodemonstratebreeddifferences.Thusthehereditarydeterminationofdelayed-responseabilityisneitherprovednordisproved.Aselectionexperimenttodeterminetheheritabilityofthecharactermightyieldimportantresults.
THETRAILINGTEST
Thistestwasdevelopedinanefforttostudyvariationsinthetrackingbehaviorthatissocharacteristicofdogs.Thedifficultiesofstandardizinganoutdoortestatdifferenttimesoftheyearandundervaryingweatherconditionsweresogreatthatwedevelopedacompletelyartificialindoortest.
Thereisnodoubtthatbreedsdifferintheircapacitiestofindpreyundernaturalconditions.Preliminaryexperimentswithbeaglesinanoutdoorsituationindicatedthatifananimalhadfoundanobjectinaparticularplace,onthesecondtrialitwentdirectlytotheoriginalplaceandstartedsearchingfromthere.Wesetupourexperimentalapparatustotakeadvantageofthisfact.
there.Wesetupourexperimentalapparatustotakeadvantageofthisfact.
Thenextproblemwastosetupsomesortofartificialtrailwhichcouldbeexactlyduplicatedintestaftertest.Wetooksome1-inchboards,10feetlongand2incheswide,andattachedaluminumplatestothemat1-footintervals.Wethenlaidatrailalongthe
PROBLEM-SOLVINGBEHAVIOR245
metalplatesbvplacingadropoffishjuiceinthecenterofeachwiththeendofaf-inchwoolendowel,beginningatthepointwherediedogwastobestarted.AspoonfuloffishinasmallSyracusewatchglasswasplacedatthefarendoftheboard.
Thenextstepwastotraintheanimalstoassociatetheartificialtrailwithfindingareward.Onthefirstdayanexperimenterledthedogthatwastobetestedovertheentireloftinwhichthetestwastobegivenandlethimeatatthefuturestartingpointofthetrail.Theideaherewastolettheanimalbecomereacquaintedwiththeroom,whichwasthesameoneinwhichithadbeenpreviouslytestedonthedetourandmazetests.
Onthesecondtrial,atrail20feetlongwaslaidout,startingfromthepointwheretheanimalhadbeenfedthedaybefore.Wefoundthatmanydogsstartedoffinthewrongdirectionand,inordertomakesurethattheyobservedthetrail,wesurroundedthestartingpointwithaU-shapedfencewhichforcedthemtomoveintherightdirection.Nevertheless,manyanimalsfailedtofindfoodwithinthetimelimit.Iftheydidnotsucceed,theywereplacedonaleash,leadtothefish,andallowedtoeat.Thisprocedurewasrepeatedonceonthefirstday.Onthefollowingday,2trialsweregivenwithouttheU-shapedfence.Onthese4trialsthedoghadtheopportunitytoassociatethescentedboardwiththerewardoffishatitsend.Manyanimalswouldrunalongtheboardwiththeirnosesdirectlyoverthedropsoffishjuice.
Thenextdaywebegantestsontrackselection.Twobrancheswereaddedontheendofthetrail,ascentedonewhichledtothefishandanother,unscented,whichledtoanemptydish.Ifthedoghadassociatedthesightofthetrailwiththefoodreward,hemightaseasilytakeonebranchastheother.MostofthedogsrantotheforkoftheVandbegansearchingfromthere.Thenextpartofthetestwasmoredifficult.AsecondVwasaddedatthelastpointwherethefishhadbeenfound,butthistimethebranchontheoppositesidefromthefirstheldthereward.
thereward.
OnthefinaldayasimpleY-shapedapparatuswassetupinadifferentpartoftheroomandthedogsgiventrialswiththerewardfirstononesideandthenontheother,totestwhetherthedogscouldgeneralizetoanewlocation.Inall,therewere3trialswithasinglechoicepointandonewithadoublechoice.
Thewholetestwassetupsothattheonlyreliablecuetothelocationoftherewardwasthescenttrail.However,thedogscouldanddiduseavarietyofmethodsforsolvingtheproblem.Theycould,forexample,learnthattherewardwasalwaysattheend
BREEDDIFFERENCES
ofoneofthetrailsandgofirsttotheendsandcheckthese.Asecondtypeofvisualsolutionconsistedoflookingaroundtheroomastheyranoverit,payingnoattentiontothetrail.Thebeaglesusuallyemployedstillathirdmethod,circlingrapidlyaroundtheroomuntiltheyapparentlydetectedanairbornescent.Thentheydroppedtheirnosestothegroundandinvestigatedthefloorinchbyinchuntiltheylocatedthefish.
Theresultsindicatedthattheproblemaspresentedbyuswaslearnedbyfewdogsduringthebriefperiodoftraining.AsTable10.5shows,only7dogsoutof143solvedthelastproblemperfectly
TABLE10.5
AnimalsShowingPerfectPerformanceontheFinalTrialoftheTrailingTest
byfollowingdirectlyalongthefish-scentedtrail.Theseanimalsweredistributedthroughoutallthebreedsexceptthefoxterriers.Failuretofollowthetrailclosely,however,mustnotbeconfusedwithfailuretosolvetheproblembyoneofthealternativemethods;27subjectshadnofailuresonanytrials.
Onesurprisingresultwasthatthecockersandsheltiesdidaswellasthebeaglesonthetest(seeTable10.6).Terriersandbasenjis
TABLE10.6
RelativeRanksofBreedsonPerformanceonMostDifficultTrialofTrailingTest(Trial7)
AverageTime(sec),SuccessfulAnimals
1.Beagle51.4
2.Cocker53.9
3.Sheltie54.6
4.Basenji74.5
5.Foxterrier77.8
PerCentofSuccesses
1.Sheltie56
2.Cocker53
3.Beagle50
4.Foxterrier30
5.Basenji23
didlesswell,anditsoonbecameapparentthatthepoorperformanceofthebasenjiswascausedchieflybytimidity.
Astheexperimentwenton,weobservedthatsomeanimalswere
PROBLEM-SOLVINGBEHAVIOR
247
apparentlyfailingthetestbecauseoffearoftheartificialtrailitself.TheyrefusedtocrossthearmsoftheYinordertogettothefood;andwhenledtothegoal,theyvigorouslyresistedbeingforcedtocrosstheboardtrack.Inthemostextremecasesthedogsnevercrossedthearmsofthetrailin4consecutivetrials.Weusedthisbehaviorasameasureoftimidity.
AsshowninTable10.7therearemanymorecasesoffearreac-
TABLE10.7DistributionofFearReactionsinTrailingTest
TABLE10.7DistributionofFearReactionsinTrailingTest
tioninbasenjisthanincockerspaniels.Ifthebasenjiswhichfailedbecauseoffearreactionareexcludedfromthesummary,verylittledifferenceremainsbetweenthetwobreeds.Therefore,thefearreactiontotheapparatusaccountsformostofthedifferencebetweenthescoresofthecockerspanielsandbasenjis.
Fearofapparatusisnottheonlyfactorproducingbreeddifferencesinperformance,sincethefoxterriers,whichmakefewtimidityresponses,werealsopoorinthetrailingtest.However,resultswithothertestsinwhichstrangeapparatuswasusedindicatethatfearwasfrequentlyacomplication.Evenafterextensivehabituation,somesubjectsavoidedapparatusandwereexcessivelydistractedbysightsandsoundsinthetestspace.Thismatterisdiscussedfurtherinchapter14.
THESPATIAL-ORIENTATIONTEST
Theseriesofproblem-solvingtestswasclimaxedbyaprocedurewhichwenamedthespatial-orientationtest.Fundamentally,theapparatusconsistedofanelevatedgoaltableonwhichfoodwasplaced.Accesstothefoodwaspossibleonanyonetrialbyonlyonesetofthreerampsleadingupfromtheground.Theconstructionwassuchthatanimmediatevisualsolutionwaspossibleifthe
BREEDDIFFERENCES
subjectsutilizedvisualcues.Itisoftenstatedthatsomebreedsareguidedpredominantlybysight,othersbyolfaction;andtheapparatusdesignwasintendedtodetectsuchdifferences.Inordertominimizedisturbanceproducedbyunfamiliarobjectsandplaces,theequipmentwassetupineachhomepenonedaypriortotraining.
Anobjectiveofthetest,inadditiontoclarificationofhypothesizeddifferencesinutilizationofvisualcues,wastherelationshipbetweenmotivationalfactorsandsuccessinreducingerrors.Measuresofrunningspeedduringthetestandofthepersistenceofapproachbehaviorfollowingcompleteblockingoffofthefoodwereincludedforthispurpose.
Testdesign.—ThearrangementoftheequipmentisshowninFigure10.9.Thisapparatus,constructedofheavywood,wasset
Fig.10.9.—Apparatususedinthespatial-orientationtest.
upforeachlitterinitsregularlivingspace.Thegoalcagewasawoodenframecoveredonthreesidesbvheavybrowncanvasoverawiremesh.Inalatermodel,plywoodsideswereused.Wingsextendedlaterallyonbothsidesoftheentranceandpreventeddogsfromedgingaroundthetableintothecage.Theyalsoservedtoemphasizethepositionoftheopenside.Thecagewasrotatedonthegoaltablesothatonepathwaywasopenatatime.Thegoaltablewas36incheshighand30inchessquareontop.Theinter-
PROBLEM-SOLVINGBEHAVIOR249
mediatetableswere28incheshigh.Rampswere5feetlongand20incheswide.Thefreespanofthe18-inchbridgeswasabout5feet.Justprevioustotesting,allmembersofalitterwereremovedtosmallretainingcagesoutsidethelivingquarters.AnimalswereintroducedintothetestareaoneatatimethroughthedoorshowninFigure10.9.Theapparatus,withtheexceptionofthethree-sidedcage,wasplacedwiththesubjectsatleast24hoursbeforetrainingwasbeguninorderthattheymightbecomeaccustomedtoit.Itremainedinthependuringtheentireperiodoftestingsothatallsubjectshadanopportunityforthoroughexploration.
Experimentationwasdividedintothreeparts:preliminarytrainingtomeetacriterion(aminimumof2daysuptoamaximumof12);testingonasetofstandardproblems(6days);andpersistencetesting(1day).
Preliminarytraining.—Preliminarytrainingwascarriedoutintwostages.Inthe
Preliminarytraining.—Preliminarytrainingwascarriedoutintwostages.Inthefirststage,thedogwasreleasedintothepenbyanassistant,whiletheexperimenterstoodbesidetheapparatusholdingadishcontainingateaspoonfulofcookedherringpieces.Thefoodwasplacedonthegoaltablewiththecageinplace,andguidanceandassistanceweregivenasneededtoinducethedogtowalkuparampandobtainfood.Trainingwasgiveninrotationonallrampsuntil,on3consecutivetrials,thesubjectwalkedupandreceivedfoodwithin1minutewithoutanyactualhandlingbytheexperimenter.From3to20trialswererequiredtoattainthiscriterion.
Inthesecondtrainingstage,theapparatuswassetupwithonlyonerampinplace,andthegoalcagewasturnedsothattheopensidecorrespondedwiththisramp.Foodwasplacedinthegoalcage,andtheanimalreleasedintothepen.Theexperimenterremainedoutsidethepen,partiallyconcealedbyawoodenbarrier.Theprocedurewasthesameasthatintestingexceptthattherewasnochoiceoframpstoascend.Rampsandgoal-cagepositionwererotatedaftereachtrialuntil3consecutivesuccessfultrialswerefinished.Asuccessfultrialwasdefinedasreachingthegoalwithin2minutes.Onunsuccessfultrialstheexperimenterenteredandledthesubjecttothegoal.
Testandscoring.—Twodifferentarrangementsoftheapparatuswereemployed.Duringtrainingandthefirstthreedaysoftesting,thetablesweresetupforProblem1asshowninFigure10.9.OnDay4throughDay6theapparatuswasrotated180°.ThiswascalledProblem2.
Thethreepathwaystothegoalweredesignatedas(D)direct
250BREEDDIFFERENCES
ramp;(S)straightrampandbridge;and(L)L-shapedpathoframp,table,andbridge.Theunitofperformancetakenforanalysiswasasetof3consecutivetrials,eachwithadifferentcorrectpath.Twosets(6trials)weregiveneachdayfor6days.Sets1through6onProblem1occupieddays1through3.Sets7through12onProblem2weregivenonDay4toDay6.
Recordsofbehaviorincludedacountoferrorsandtimeinsecondstoacorrectsolution.Errorsweredefinedas(1)climbinganincorrectramp,(2)retreatingfromthecorrectpathway,(3)circling,runningbackandforth,andothermovementsnotpartofadirectprogressionfromramptoramp,(4)leapingdirectlyatthegoaltableortheelevatedbridges,and(5)failingtoleapdirectlydownfromtheelevatedportionofanincorrectpathway.Atfirstanattemptwas
downfromtheelevatedportionofanincorrectpathway.Atfirstanattemptwasmadetorecordeachtypeoferrorseparatelyonadiagram,butitwasfoundthatthevarioustypeswerepositivelycorrelatedandonlysumsaretreatedinthispaper.RepetitionsofType-1errorswithinasingletrialwere,however,recordedseparately,sincethisappearedtorepresentaparticularlymarkedpersistenceofanincorrectresponse.
Thetimebetweentheanimal'sentranceintotheexperimentalfield(definedbyalinedrawn6feetfromtherampnearesttotheentrance)andthereachingofthefoodwasthesolutiontime.Thelogarithmofthistimewasthetimescoreforeachtrial.Theaverageofthesetimescoresgivesthelogarithmofthegeometricalmeanoftheactualtimesinseconds.Alimitof5minuteswassetforeachtrial,butthetrialwasdiscontinuedatanytimewhenasubjectforaperiodof1minuteeitherremainedmorethan6feetfromtheapparatusorstayedinoneplacewithnoattempttosolvetheproblem.
Persistencetest.—OnDay7thesubjectsweretestedforonetrialonProblem2withtheopensideofthegoalcageturnedawayfromthethreeapproachesandcoveredwithawirescreentopreventanydogfromleapingdirectlyontothetable.Adishcontainingfoodwasplacedinsidethecage.Acountwasmadeofthenumberofattemptstogetatthefood.Forthispurposeanyentryontoaramporstandinguptoanypartoftheapparatuswasconsideredasanattempt.Thetestwascontinuedfor5minutesoruntil1minutepassedwithoutanyattemptstoreachthegoal.
Resultsofspatial-orientationtest.—InTable10.8arelistedmeanerrorscores,adjustedtimescores,andpersistencescores,allexpressedinstanines.ThescaleshavebeenorientedsothatahighEscoreindicatesgoodperformance(fewerrors);ahighTscore
TABLE10.8ComparisonsbetweenPureBreedsonSpatial-OrientationScores
*Notincludedinnumbertested.
indicatesaspeedysolutionoftheproblemandhencefastrunning;andahighPscoremanyattemptstoreachthegoalontheinsolvableproblem.Theadjustedtimescores(V)takeintoaccounttheadditionalrunningtimeattributabletoextradistanceproducedbyerrors.Themeanregressionoftimeonerrorswascomputedandtheadjustmentmadeaccordingtothefollowingequation:T'—T—0.0713AT,whereT'istheadjustedtimescore;Tisthetimescoreinlogseconds;andA7isthenumberoferrors.
seconds;andA7isthenumberoferrors.
Beforeconsideringthedifferencesbetweenbreedsindetailsomeofthegeneralfeaturesofthetestwillbeconsidered.Amongthe121purebreddogswhichweretested,16failedpreliminarytrainingandwereeliminated.DisqualificationswereespeciallyprevalentamongtheShetlandsheepdogs,whereonly11outof19couldbetested.Thisbreedalsowasthepoorestperformerintermsoferrors.
TherawerrorscoresforthefivepurebreedsareshowninFigure10.10,whichalsodepictsresultsforthecockerspaniels(mostsuccessful)andShetlandsheepdogs(leastsuccessful).TheconnectedpointsforSet1throughSet6formatypicallearningcurve;errorsrosewhentheapparatuswasrotatedandfellagainafterpractice.ThemoststrikingcurveisthatoftheShetlandsheepdogsonSet7throughSet12.Rotationoftheapparatusproducedaverygreatdecrementinperformancewhichremainedthroughoutthetest.Somesheepdogs,however,performedwell.Figure10.11showstheindividualerrorscoresofthebestandpoorestsubjectamongthem.Theextremeindividualsamongthespanielsarealsoshown.Therangeofperformancewasgreat.SH-2953andCS-2724solvedtheproblemswithaminimumofretracingandrandomactivity;CS-1913showedalearningcurveverymuchlikethegroupaverage;SH-1945didnotimprovesystematically,thoughitscoredwellonTrialSet4.
BREEDDIFFERENCES
20
15-
10
5■
0-
345678910IISETOFTRIALS
12
Fig.10.10.—Rawerrorscoresforthecombinedfivepurebreeds(solidcircles)onthespatial-orientationtestcomparedwithscoresforsheltiesandcockerspaniels(opencircles).
3456789
SETOFTRIALS
10II12
Fig.10.11.—Individualerrorscores,spatial-orientationtest.
PROBLEM-SOLVINGBEHAVIOR
253
Despiteindividualvariability,differencesbetweenbreedsinerrorscoresforbothseriesoftestswerefoundtobehighlysignificant(Table10.9).Evidencewasalsofoundforsignificantlittereffectswithinbreeds.Sincethetestwascarriedonoutdoorsundervaryingweatherconditions,itispossiblethatacommontestenvironmentwaslargelvresponsible.
Differencesbetweenbreedsonadjustedtimeandonpersistencewerealsosignificant,althoughlittereffectswerenotfound.Itisevidentthatthebreedswiththehighestscoresonpersistence(P)arenotnecessarilvthosewiththefewesterrorsorfastesttimes.Product-momentcorrelationcoefficientsbetweenpersistenceandperformanceonProblem2areshownbelow:
persistenceandperformanceonProblem2areshownbelow:
E2P,r=.040(degreesoffreedom,88),7YP,r=.259(degreesoffreedom,88).
Thesecondofthesecorrelationsreachesthe5percentsignificancelevel.Itindicatesaslighttendencyforthefasterdogstobemorepersistentinaccordwiththehypothesisthatbothmeasureswerecloselydependentuponmotivation.
TABLE10.9AnalysisofVarianceofSpatial-OrientationMeasures
•Variationsinthenumberoflittersareattributabletoaccidentallossofdataandtovariationsinthenumberofsubjectsgiventhepersistencetest,tP<.05XP<-01
Itis,ofcourse,impossibletoestimatedirectlytherelationofspeedpersetoerrors,sincetheadjustedtimescoreswerecomputedbyaprocesswhichinvolvedsubtractionofthatportionofthetimescorewhichcouldberelatedtoerrorscores,andthenon-adjustedtimescoresarecorrelatedwitherrorsbecauseeacherrorlengthensthedistancerun.Thescoresusedinthestatisticalanalysis,however,weretransformationsoftheactualtimeinsecondsmadetobringthedataintoamorenormaldistribution.Itcanbeshownthattheexpressionforadjustingtimescores,T'=T—bE,isequivalentto
adjustingtheactualtimesbytheexpressionV=t/kE,wheretistimeinseconds.ThecorrectiontermisanexponentialfunctionofEratherthanalinearfunction.Slowdogsdotendtomakemoreerrors,andthecorrectiontermshouldbecorrespondinglyexpandedforhigh-errordogsinordertoadjusttheirtimescorestoanerror-freebasis.
Evenaftertransformationandadjustment1anassociationremainedbetweenhigherrorsandslowtimeswhichisapparentinTable10.8.CorrelationcoefficientswerecalculatedbetweenEiandT'i,E2andT'2afternormalizationofthescoresandseparationofthewithinbreedsandbetweenbreedssumsofsquaresandcrossproductsasfollows:
SampleDegreesofFreedomEiT\EiT'i
Totalsample102.333.349
Betweenbreeds4.610.798
Withinbreeds98.273.079
Withinbreeds98.273.079
Thereisastrongtendencyfortheslowerrunningbreedstomakemoreerrors,butwithinbreedsthecorrelationislowornegligible.Theover-allcorrelationappearstobelargelyspurious.
Effectofpracticeongeneticeffects.—Repeatedtrialsonthespatial-orientationapparatusresultedinincreasedcorrelationoferrorscoresobtainedinconsecutivesetsoftrials.Figure10.12showstheproduct-momentcorrelations(inter-trial)betweenconsecutivesetsforthepurebreddogsasagroup.Thereliabilityofthistestdidnotreachthelevelofourbesttestsasthemaximumcorrelationwasabout.60.Onthesamefigurearedepictedtheintraclasscorrelationscomputedtrialbytrial.Althoughlowerinmagnitude,allintraclasscorrelationsexceptthoseforsets1,3,and6aresignificantatbetterthanthe.01level.Duringthefirstpartoftesting,theintraclasscorrelationsfluctuated,buttheywererelativelysteadyduringthesecondportionofthetestperiod.Itwillberememberedthatanintraclasscorrelationmeasurestherelativecontributionofbreeddifferencestototalvariance.Onemustconcludethattrainingdoesnotdecrease,andpossiblystabilizes,thecontributionofhereditytoindividualvariation.Thepointisimportant,foritissometimesassumedthatchangeinabehaviorpatternfollowingpracticeisevi-
1Thequestionmayberaisedconcerningthevalidityofcorrectingtimescoresbythedescribedmethod.Ascatterplotorerrorsagainstlogtimeshowedgoodfittoalinearrelationasjudgedbyeye.Thecalculatedvalueoftheregressioncoefficientwasabouttentimesitsstandarderror.However,noclaimismadethatthetransformationismorethanastatisticalconvenience,andabettermathematicalmodelmightyieldbetterresults.
PROBLEM-SOLVINGBEHAVIOR
255
1.00
LU
5.75
.50
SPATIALORIENTATIONERRORS
O-OINTERTRIAL••INTRACLASS
/°-o
/°^°N
sO
456789SETSOFTRIALS
12
Fig.10.12.—Reliability(inter-trialcorrelation)improvesasthetestprogresses,butbreeddifferences(intraclasscorrelation)remainconstantinthespatial-orientationtest.
denceagainstitsheritability.Theargumentfollowsthelinethatdemonstrationofmodifiabilitybytrainingmakesitunnecessarytoaccountforanyvariancefromheredity.Thelogicofthisargumentisclearlyfalseandexperimentaldatacontradictit.
CONCLUSIONS
Interpretationofmanyoftheseproblem-solvingtestsisrendereddifficultbythefactthatnotallsubjectsmetpreliminarycriteriafortesting.Thesefailureswerenotevenlydistributedamongthefivebreeds,hencetheactualsampleswerebiased.Theeffectwasprobablytodecreasecalculatedvaluesofgeneticeffects,sincethefailurescamepredominantlyfrombreedswhichhadlowaveragescores.
Sincecorrelationsofmeasuresoflearningandofmotivation,particularlyinthespatial-orientationtest,werenothigh,itdoesnotseemlikelythatallvariationsinproblemsolvingweresecondaryeffectsoffearfulnessinthetestsituation.Yetinconductingthetests,theexperimentersoftenobservedavoidingbehaviorinpoor-scoringsubjects.Thepoorperformanceasagroupofbasenjisoncue
poor-scoringsubjects.ThepoorperformanceasagroupofbasenjisoncueresponseandShetlandsheepdogsonspatialorientationappearedtobelargelyafunctionoffearfulness.Thisexplanationdoesnotaccountforpoorscoresofterriersonspatialorientation.
256BREEDDIFFERENCES
Certainlynoevidencewasfoundforageneralfactorofintelligencewhichwouldproducegoodperformanceonalltests.OnthispointweagreewithSearle(1949),whocomparedmaze-brightandmaze-dullratsonavarietyoftests.Thegenetictransmissionofproblem-solvingabilitywillbediscussedinchapter12,butitcanbestatednowthatgeneticcontrolappearstobelargelyamatterofnon-allelicinteractionswithrelativelysmalladditivegeneticeffects.Suchafindingisnotunexpectedwhendealingwithsocomplexaphenotype.
Eachofthedifferentproblem-solvingtestsproducedinterestingideasandresults.Thefirstbarrierordetourtestgivenat6weeksofageindicatedthatthecapacityforinsightorsolvingaproblemwithouttrial-and-errorisdevelopedbyexperienceratherthanappearingspontaneously.Sinceyoungpuppiesatthisagehaveverylittlecapacityforwidegeneralization,theirinsightsarelimitedtoproblemsverysimilartotheirpreviousexperiences.
Themanipulationtestemphasizedtheimportanceofsuccessandfailureinincreasingorreducingmotivation.Onceananimalhaslearnedtofailitisextremelydifficulttogethimmotivatedenoughtomaketheefforttosolveevenasimpleproblem.
Inthemazetestwemadeadetailedanalysisofthevariouseffectsofenvironmentalandotherbackgroundfactors.Theresultssuggestthattheserandom,uncontrolledfactorsareindeedimportantindeterminingproblem-solvingbehavior,aspsychologistshavelongsuspected.However,therestillremainedinthistestahardcoreofvarianceattributabletobreeddifferencesandthustoheredity.
Thecue-responseanddelayed-responsetestswereunusualinthattheyshowednobreeddifferences,butdidindicatewideindividualdifferences.Theseweretestswhichmostclearlydependedonpureintelligence.Theresultsindicatethatinthisareaindividualdifferenceswithinabreedmaybemoreimportantthandifferencesbetweenpopulationmeans.
Thetrailingtestemphasizedtheimportanceofemotionalfactorsindetermining
Thetrailingtestemphasizedtheimportanceofemotionalfactorsindeterminingperformance.Thebasenjisshowedafearofstrangeobjectswhichaccountedforalmostallthebreeddifferencesshowninthistest.Thesamereactionaffectedtheirbehaviortoalesserextentinanyofthetestsinvolvingstrangeapparatus.
Finally,thespatial-orientationtestshowedthatpracticeneednotreducegeneticvariation.Whilethetotalvariancemightbereducedastheanimalsbecomemoreexpert,theproportionofvarianceattributabletobreedsremainedconstant.
Withtheexceptionofthecue-responseanddelayed-response
PROBLEM-SOLVINGBEHAVIOR257
tests,allthetestsshowedclear-cutbreeddifferences,manyofthemquiteimportant.Thisfindingraisestheproblemofwhethertherearegeneraldifferencesinintelligencebetweenthebreeds.CanwetakethesumofthesetestsasasortofcanineIQanddeterminetherelativecapacitiesofeachbreed?
Inthefirstplace,ahumanintelligencetestincludesdozensandsometimesahundredormoreproblemswhichthestudentsolveswithinanhourorso.Thisispossiblebecausethestudentshavebeensubjectedtoyearsofprevioustraininginsimilarproblems,anditismeaningfulbecausetheireducationalandenvironmentalbackgroundshavebeenreasonablysimilar.Comparingsuchatestwithourproblem-solvingexperimentswithdogs,itisfairtosavthateachofthecaninetestsisequivalenttoasinglequestiononanIQtest.Furthermore,thetestsaredoneatdifferenttimesanddifferentages.Itisimpracticaltogivedogsthesamevarietyandintensityoftrainingtowhichhumanpupilsaresubjected.Forallthesereasons,thecanineresultsaremuchlessaccuratethanthoseobtainedbyahumanIQtest.
Nevertheless,itisinterestingtoputalltheresultstogetherandlookattheover-allpicture(seeTable10.10).Inthefirstplace,thereisnobreedwhichcomesoutuniformlvwiththehighestrank.Evenonindividualtests,abreedmaybefirstinonepartandlastinanother.Inthemazetest,forexample,beaglesachievedthebestminimumscoresbutperformedbadlvonthefirsttrial.
Ingeneral,thefourhuntingbreeds(beagles,basenjis,terriers,andcockers)performedbestonthetests.Thisisprobablvbecausemostofthetestsweredeliberatelydesignedtotestindependentcapacitiesmotivatedbyfoodrewards;anditisnoteworthythatthebeagle,whichisnormallyusedforhuntingwithoutdirection,showsthebestover-allperformanceintermsofnumberoffirstranks.
direction,showsthebestover-allperformanceintermsofnumberoffirstranks.Bycontrast,theShetlandsheepdogs,whoseancestorshavebeenselectedfortheirabilitytoperformcomplextasksunderclosedirectionfromtheirhumanmasters,performedratherbadlv.Indeed,inmanyofthetests,thesheltiesgavethesubjectiveimpressionofwaitingaroundforsomeonetotellthemwhattodo.Furthermore,whileallthehuntingbreedsarestronglymotivatedbyfood,sheepdogsingeneralhavebeenselectedawayfromthistrait.Thedifferencebetweensheltiesandotherbreedsinthisrespectisstronglybroughtoutinthesimpletaskofrunningtoafoodreward(seeFig.9.4).
Obviously,abetteranswertothequestionofdifferencesinproblemsolvingabilityneedstobefound.Suchexperimentswouldin-
258BREEDDIFFERENCES
TABLE10.10RanksoftheDifferentBreedsinVariousProblem-solvingTests
Test
Detourtest:
Shortbarrier
Longbarrier
U-barrier
Manipulationtest:
Movingdish
Stringpulling(1)
Stringpulling(2)
Uncoveringdish
Mazetest:
Speed
Minimumerrors
Lackofhabitformation
T-mazeanddelayed-responsetests
Speed
Discrimination
5-seconddelay
Trailingtest:
Success,mostdifficulttrial....
Speed,mostdifficulttrial
Spatial-orientationtest:
Fewerrors
Speed
Persistence
Totalfirstandsecondranks.
Breed
Basenji
Beagle
Cocker
Sheltie
FoxTerrier
555
3244
555
555
13
4.53
2
222
2422
243
2
22
4
5
4.54.53
10
eludemoreofthebreedswhicharethoughttobeunusuallyintelligent,suchaspoodlesandbordercollies,andthetestingprogramshouldincludetrainingforcomplextaskssimilartothoseforwhichthesebreedsareusuallyemployed.Onthebasisoftheinformationwenowhave,wecanconcludethatallbreedsshowaboutthesameaveragelevelofperformanceinproblemsolving,providedtheycanbeadequatelymotivated,providedphysicaldifferencesandhandicapsdonotaffectthetests,andprovidedinterferingemotionalreactionssuchasfearcanbeeliminated.Inshort,allthebreedsappearquitesimilarinpureintelligence.Ontheotherhand,wehaveevidencefromthedelayed-responsetestthatthereareenormousindividualdifferenceswithinbreedsfordevelopingcertaincapacities.Whetherornottheseareinheritedcanonlybedeterminedbyselectionandcrossbreedingexperimentswithinbreeds.
PARTIII
INHERITANCE
OFDIFFERENTIALCAPACITIES
AMONGHYBRIDS
CHAPTER11
THEINHERITANCEOFBEHAVIORPATTERNSSINGLE-FACTOREXPLANATIONS
Aswepointedoutinchapter3,thebehaviorofdogshasbeenprincipallymodifiedinconnectionwithagonisticandinvestigativebehavior.Thelatterisdifficulttomeasureunderlaboratoryconditions,sincemostoftheinvestigativebehaviorofdogshastodowithhuntingandcanonlybeseenadequatelyunderfieldconditionswhereitisalmostimpossibletokeeprandomenvironmentalfactorsfrominterferingwithanexperiment.Furthermore,manyofthesepatternsofhuntingaredevelopedonlyafterextensivetraining.
Ontheotherhand,thepatternsofagonisticbehavioraremucheasiertostudy,sincetheyappearoverandoveragainunderlaboratoryandkennelconditions.Thetwobreedswhichwerechosenforthecrossshowedwidedifferencesinthisrespect.Cockerspanielshavebeenselectedfornon-aggressiveness.Occasionallya"mean"cockerwillappearinthebreed,butthisisconsideredaseriousfault,andsuchanimalsarenotusedforbreeding.Shynessortimidityisalsoconsideredafaultinthisbreed,asitisinmostothers,sothatcockerspanielsasagrouparerelativelynon-aggressiveandconfidentintheirrelationstopeople.
Thebasenjibreedisbycontrasthighlyaggressive,althoughnotsomuchsoasthewire-hairedterriers.Whenfirstdiscovered,basenjisweresometimescalled"Congoterriers."Alsoincontrasttothecockers,youngbasenjisrearedunderourconditionsshowedagreatdealoftimidityat5weeksofage:runningaway,yelping,snappingwhencornered,andgenerallyactinglikewildwolfcubs.ItisprobablethatintheAfricanjunglevillagessuchwarinesshasconsiderablesurvivalvalue.Inspiteofthisearlytimidity,basenjipuppiestamedownveryrapidlywithhandlingandhumancontact.
262DIFFERENTIALCAPACITIES
GENETICANALYSISOFBEHAVIORALTRAITS
GENETICANALYSISOFBEHAVIORALTRAITS
Ouroriginalpredictionwasthatallbehaviortraitswouldprovetobeaffectedbymanygeneticfactors;i.e.,bypolygenicsystems,andwethereforedesignedourexperimentsothattheresultscouldbeanalyzedaccordingtotherelativeamountsofvariationproducedbygeneticfactorsinthehybridsandpurebreeds(Chapters12,14).Astheresultscamein,however,wefoundthatsomedifferencesinbehaviorpatternsseemedtobeinheritedasiftheywereproducedbyoneortwogenes,sothattheresultsofthecrosslookedlikethosefromasimpleMendelianexperimentandverysimilartothoseobtainedfrommeasuringasimplephysicaltraitinthesamecross.Forexample,allbasenjisareshorthairedandallcockersarelonghaired.Whenthetwobreedsarecrossed,thepuppiesintheFigeneration,whetherfromcockerorbasenjimothers,allhaveshorthair,indicatingthatshorthairisdominantoverlong.Ifthisresultisproducedbyasinglegene,wewouldexpectthatthebackcrosstothebasenjiswouldallhaveshorthair,thatapproximatelyone-halfofthebackcrosstocockerswouldhavelonghair,andthatone-fourthoftheF2?swouldalsohavelonghair.Asshowninchapter13,thiswasactuallythecase.
Inmanyexperimentswiththeinheritanceofphysicaltraits,earlyexperimentersdeliberatelychosecharacteristicsinwhichtherewasnooverlapbetweentheparentstrains,simplyforconvenienceandeaseofanalysis.However,wewereunabletofindanysinglebehaviortraitinwhichtherewasnooverlapbetweenthebreeds.Aswehavepointedoutbefore,selectionhasemphasizedorde-emphasizedcertainbehaviortraitsbuthasnotcreatedanythingnew.Inmanycasesselectionhassimplymodifiedtheamountofstimulationrequiredtobringoutaparticularbehaviortrait.Basenjiscanbestimulatedtofightwithrelativeeaseandcockersonlywithdifficulty,butitisquitedifficulttofindanamountofstimulationwhichwillcause100percentofbasenjistobecomeaggressiveandleaveallcockersunaffected.Consequentlythereisalwayssomeoverlapbetweenthebreeds.Thismeansthatwhenweanalyzetheinheritanceofbreeddifferencesinbehaviorwearealwaysforcedtoworkwithdifferencesrangingfrom50to90percentandtoallowforconsiderablevariabilitywithineachbreed.WecanneverthelesscomparetheresultswithmodelsofsimpleMendelianinheritanceinvariousways,andthischapterdescribestheoutcomeofsurveyingthedataontheassumptionthatsomeofthedatamaybeexplainedasa
BEHAVIORPATTERNS263
resultofsingle-factorinheritanceanddiscontinuousvariationratherthan
resultofsingle-factorinheritanceanddiscontinuousvariationratherthanmultiple-factor(polygenic)inheritanceandcontinuousvaria-
tion.
METHODSOFGENETICANALYSIS
ThechiefpurposeofexperimentswithhvbridizationistodiscoverwhetherornotthepatternofinheritancefollowsMendeliantheory.Herewehaveachoiceofanalvsisbytwomethods:quantitativeinheritanceorqualitativeinheritance.Mostofthebehavioraldatalookslikecasesofquantitativeinheritance,sincebehaviorisusuallymeasuredoncontinuousscalesoffrequency,latency,orspeed.Ontheotherhand,therearecertaincasesinwhichbehavioriseitherpresentorabsentandapparentlyconsistentwithqualitativeinheritance.Fromamathematicalviewpointthesetwotypesofdatacanbedescribedasbeingdistributedeitherinmultiplecategoriesoralternatecategories.Thelatterisoftenreferredtoasadichotomousdistribution,incontrasttoacontinuousdistribution.Whicheverdistributionispresent,thedatamustgiveindicationsofbeingexplainablebyareasonablysimpleMendelianhypothesisinordertomakepossibleanyfurtheranalysisalongtheselines.
Quantitativeinheritance:analysisofvariance.—Castle&Wright(Castle,1921)developedaformulaforestimatingthenumberofgenesinvolvedinaparticularcross,basingtheircalculationsontwomajorassumptions.Thefirstoftheseisthatthegeneshavesimpleadditiveeffects.Suchanassumptionisoftenareasonableone,asitisinthecaseofthenumberoftimeswhichadogjerksontheleashduringtraining.Ifonegenecausesacertainnumberofjerks,thenasecondgenemightwelladdafewmore.Ifthesecondgeneshouldinsteadcauseapercentageincreaseinthenumberofjerks,transformingthedataintoastaninescalewillcausethiseffecttoappearadditive.
Thesecondassumptionisthateachgenehasaneffectequaltothatofeveryothergene.Thisisapureassumption,andthereisnowayofverifyingitunlessthegenescanactuallybeidentified.Thismeansthattheresultofsuchanalysisalwaysgivesanestimate,andaminimumestimateatthat.Theformulathereforecanbeusedmostconservativelytodistinguishbetweensingle-factorandmultiple-factorinheritance.
Becauseoftheseassumptionsthemethodhascertainlimitations.Itwillnothandlecasesofcomplexinteractionbetweengenessincetheanalysisofsuchaninteractionrequiresthatthepresenceor
interactionrequiresthatthepresenceor
264DIFFERENTIALCAPACITIES
absenceofeachgeneberecognizableinsomeway.Also,itwillnotapplytocertainspecialpatternsofinheritancelikethatseeninplayfulaggressiveness,wheretheFi'sandF2'sshowthesameamountofvarianceandoverlapbothparentstrains(the"Tryoneffect").
TheformulasforanalyzingbackcrossandF2generationsaregiveninTable11.1InthisnotationAisthedifferencebetweenthemeansoftheparentgenerations,andor2isthevariancefromthemeanofeachpopulation.Mather's(1949)formulaforKisamoregeneralformofthesemathematicalstatements,butitsuseisstillsubjecttothesamelimitations.
Asappliedtoourparticularexperiment,certainmodificationsneedtobemade.Oneisacorrectionfordifferencescausedbymaternaleffectsand/ortheselectionofdifferentparentsinthereciprocalcrosses.ThiscanbedonebysubtractingthedifferencebetweenthemeansoftheFi'sfromthatoftheparents,leavingonlythetruebreeddifferences.Inaddition,thevariancecausedbythesameeffectscanberemovedbysubtractingthevarianceduetothedifferencebetweenthemeansofreciprocalcrossesintheFiandF2generations.ThemostaccurateestimateofthenumberofgenesinvolvedisthatbasedonthecorrectedvariancesoftheFiandF2populations,sincewehavethelargestnumbersinthesetwogroups.Workingformulasforthesecorrectionsaregivenbelow:
A=(xPl-xP)-(xBCsf1-Xcsbf)
9_nlV2BCSFi+n2(T2cSBFi<Jp—
Fln
ap—
1n
QualitativeorSimpleMendelianInheritance.—Thefollowingmethodscanbeappliedonlywherethereissomeevidenceofarealdiscontinuityindistributionsuchthatthedatacanbelegitimately
BEHAVIORPATTERNS265
BEHAVIORPATTERNS265
dividedintotwocategories.Theyapplyparticularlywelltocasesinwhichmeasurementsarebasedonthepresenceorabsenceofabehaviorpattern,andanimalscanbeclassifiedaseithershowingthepatternornotshowingit.Sincetransformingthedataintothestaninedistributionwillinevitablyobscurethepointsofdiscontinuity,thebestevidencefortheexistenceoftwocategoriescomesfromtherawdata.Herewearefacedwithanewdifficulty;nowhereinourdatawasthereacaseinwhichtherewasnooverlapbetweenthetwoparentstrains.Wearethereforefacedwiththeproblemofmodifyingthemethodsusuallyappliedtotheanalysisofqualitativeinheritance.
Inadichotomousdistribution,themeanisalwaysthesameastheproportionofindividualsinoneclassortheother;i.e.,inapopulationcomposedof0.5animalsshowingatraitand0.5notshowingit,themeanis0.5.Itisalwaysthemean,orproportion,whichisusedintheconventionalanalysisofdatafallingintotwocategorieswithnooverlapbetweentheparentstrains.
Wecanextendanalysisbycomparisonofmeanstopopulationsinwhichoverlapexists,usingthefollowingformulabasedonacomparisonbetweenthemeansofbackcross(BX)andparent(P)strains,
——>or—-z
UpxPl—xPl
Table11.2givestheexpectedratiosforvariousnumbersofgenes.Thecalculatedfiguresarethesamewhetherornotdominanceisactuallyinvolved,sincedividingthedataintotwocategoriesineffectassumesdominance.Ifonlyonefactorisinvolved,thefigureisthesamewhetherornotheterozygosisispresentintheparentstrains(Scott,1954).Thereforethismethodprovidesatestofasingle-factortheorywhichcanberapidlyappliedtoanydata.Onecanalsousetheformulatocalculatetheoreticalratiosinthesegregatinggenerations,basingestimatesontheempiricaldifferencebetweentheparents.Naturally,thevalidityoftheresultswilldependonthesizeandrepresentativenessofthesamplesmeasured.AsimilarformulacanbeappliedtothedifferencesbetweentheFiandF2means,withthelimitationthattheexpecteddifferencesarenotasgreat.However,inourexperiment,thesearethelargestpopulationsanddeserveattention.
Liketheformulasforquantitativeinheritance,thesemustalsobecorrectedfor
Liketheformulasforquantitativeinheritance,thesemustalsobecorrectedfordifferencesduetomaternaleffectsandaccidentalselectionofdifferentstrainsinreciprocalcrosses.Thiscanbedone
DIFFERENTIALCAPACITIES
TABLE11.2
TheoreticalRatiosfortheDifferencebetweenBackcrosses,
andtheDifferencebetweenFVsandF2's,Comparedtothe
DifferencebetweentheMeansofParentalStrains
bysubtractingthedifferencebetweentheFipopulationsfromboththatoftheparentalandbackcrosspopulations.InthecomparisonofFiandF2populations,thiscorrectioncanbeeliminatedontheassumptionthatbothareequallyaffected.ThecalculationismadebysimplysubtractingthemeanofthecombinedF2SfromthatofthecombinedFipopulations.
ThisgeneralmethodwillalsoapplytotheTryondistribution,inwhichtheFiisas\ariableastheF2andthereappearstobeacentralthreshold.ThereisnodifferencebetweenthemeansoftheFiandF2,butthatbetweenthetwobackcrossesgivesanestimateofthenumberofgenesinvolved(seeTable11.2).
Thelimitationsofthemethodarequitesimilartothoseofanalysisofvarianceappliedtoquantitativeinheritance.Thebasicassumptionsarethoseofequalandadditiveeffectsofgenes,atathresholdinthiscaseinsteadofoveranextendedscale.Likethequantitativemethod,thisonewillnotapplyifgeneeffectsarenon-additiveorextremelyunequal.Theformulahastheadvantage,particularlyusefulwithourdata,ofnotbeingaffectedbyheterozygosityintheone-factorcase(Scott,1954).Inshort,liketheCastleandWrightmethod,itchieflyprovidesatestofsingle-factorversusmultiple-factorinheritance,andthenumberofgenesbevondoneisonlyaminimumestimate.
THEINHERITANCEOFWILDNESSANDTAMENESS
Therelativewildnessofthebasenjisisexpressedintwoobvioustrails.Oneisinavoidanceandvocalizationinreactiontohandlingas
BEHAVIORPATTERNS
267
youngpuppies,andtheotheristhetendencytostruggleagainstrestraint,whichappearsinmanydifferentsituations,butisparticularlymarkedinleashtraining.
Bothcockerspanielsandbasenjis,however,arereadilytameableasyoungpuppies.Thegeneraltraitoftameabilityisabasicone,becauseitmusthavebeeninvolvedintheoriginaldomesticationofthedog.Ifdomesticationoccurredbutonce,itislikelythattherewasanearlyselectionforwhatevergenesfortamenesswerepresentinwildwolvesatthattime,andthatthesegeneswouldthenceforwardbepresentinalldogbreeds.Ifdomesticationoccurredmorethanonce,orifdomesticationoccurredfrommorethanonespecies,wewouldexpectthatdifferentgenesmightbeinvolved.Ifthisweretrue,thereisapossibilitythatanFicrossmightbemuchwilderthaneitherparent,or,ifbothfactorsfortamenessweredominant,thatexcessivelywildindividualswouldappearintheF2orotherhybridgenerations.
Inheritanceofavoidanceandvocalization.—Wemaythinkofthehandlingtestasaseriesofmildtostrongstimulationswhichmaycauseayoungpuppytobefearful.Thestrongeststimulusisthatofwalkingrapidlytowardthepuppy,andtheweakestiswalkingawayorkneelingwithanoutstretchedhand.Thetestscorereflectsthenumberoftimeswhichsuchstimulationpushesthepuppyoverathresholdintothefearfulbehaviorofrunningawayoryelpingwithfright.Somepuppiesbecomefearfulonlyunderthestrongeststimulation,whileothersreactwithfeartoanythingwhichthehandlerdoesandtherebyreceivemuchhigherscores.
table11.3
ScoresforAvoidanceandFearfulVocalizationat5WeeksofAgeinResponsetoaHumanHandler
268DIFFERENTIALCAPACITIES
AscanbeseeninTable11.3,about62percentofthecockersshownofearfulreactionsatall,whereasallbasenjisshowatleastsomefearfulbehavior,withagreatdealofvariabilityintheamountproduced.TheFigenerationisverysimilartothebasenjis,withonlyoneanimalshowingnofearfulreactions,andwecanthereforeconcludethatthedifferencesareproducedbyoneormoredominantgenes.Onthisbasiswecanconstructthehypotheticalresultsofasingledominantgene.Thebackcrosstothedominantbasenjisshouldbelikethe
singledominantgene.Thebackcrosstothedominantbasenjisshouldbelikethebasenjis,whereasthebackcrosstotherecessivecockersshouldbeintermediate.Finally,theF2*sshouldbehalfwaybetweenthebasenjiandcockerbackcross.
Theactualobservedpercentagesfitthishypothesisfairlywell,andbetterthantheyfitthatoftwodominantgenes.Onthebasisofthisevidence,wecansaythatasingledominantgenecausingwild-nessinthebasenjiaccountsfortheobservedresultsreasonablywell.
Consequently,thecontrastinggenefortamenessinthecockersmustbearecessiveone.Thisfitsourgeneralideasaboutmutations,since,inallanimalandplantspecies,mostofthewild-typegenesforstructureandcoloraredominantratherthanrecessive.Also,theFihybridsdonotshowexcessivewildness,indicatingthatbothcockersandbasenjishavethesamegeneralgenesfortameness.Thisisevidenceinfavorofaremotecommonancestryforbothbreeds,althoughitcannot,ofcourse,excludethepossibilityofseparatedomesticationswhichacquiredthesamegenesfortamenessfromthewildwolfpopulation.
Inheritanceofthetendencytofightandjerktheleash.—Intheroutineofour"SchoolforDogs,"thepuppieswerecarriedeverywhereuntiltheywere16weeksofageandwerereadytobemovedoutdoors.Atthistimebothdistanceandtheirincreasingsizemadeitnecessarytoteachthemtofollowonaleash,asdescribedinchapter9.Beaglesandcockerspanielsusuallywentalongreadilyandpeacefully,butbasenjisoftenpulledbackstronglyontheleash,attemptedtobiteitintwo,orjumpedintotheair,shakingtheirheadslikeatroutontheendofafishingline.Oneofthescoresobtainedfromthisbehaviorwasthenumberoftimesthataparticularpuppyfoughttheleash.Thefinalresultsshowedbigdifferencesbetweencockerspanielsandbasenjis(Table11.4).Furthermore,therewerelargedifferencesbetweenthetwoFipopulations,thehybridstendingtoactliketheirmothers.Thisdifferencewascarriedonintothesecondgenerationtoalesserdegree.Itlooksasifthereisanimportanteffectofeitherthematernalenvironmentordifferencesbetweentheparentsofthereciprocalcrosses.Theformerseemsat
BEHAVIORPATTERNS
TABLE11.4TendencytoBiteandJerkLeash(inStanines)
269
269
BreedorHybrid
Basenji
CSBF,
Backcrosstobasenji.CSBF2
Cockerspaniel
BCSFx
Backcrosstococker.BCSF2
Variance
1.86
0.681.021.82
1.600.781.931.69
firstglancemostlikelybecauseofthestrongresemblancestotheirmother'sbehaviorinbothgenerations,butthisisnotcorrect,aswillbeshownlater.
Nevertheless,thereisstillevidencethatbiologicalheredityhasaneffect,becausethehybridsarenotexactlyliketheirmothers,andthereisincreasingvariabilityinthebackcrossandF2generations,aswewouldexpectfromMendeliansegregation.
InspectingthedatawecanformthehypothesisthatthegeneticfactororfactorsinvolveddonotshowdominanceandthatwearethusdealingwiththesimplestformofMendelianinheritance.Whenthedataareanalyzedbythequantitativemethod,estimatesofthenumberofgenesinvolvedcanbeobtainedfromthebackcrossandF2generations.Theseagreefairlywellwitheachother,forwederivethefigure1.07fromtheF2dataandtwoestimatesof1.60and0.48fromtheseparatebackcrosspopulations.Averagingthebackcrossestimatesgives1.04,andwecanconcludethattheinheritanceofthedifferenceinbehaviorbetweencockersandbasenjiscanbeexplainedbyonegenewithnodominance,complicatedbylargedifferencesbetweenreciprocalcrosses(seealsochap.12).
complicatedbylargedifferencesbetweenreciprocalcrosses(seealsochap.12).
INHERITANCEOFOTHERPATTERNSOFAGONISTICBEHAVIOR
Playfulaggressiveness.—Inthehandlingtestsgivenat13and15weeksofage,acharacteristicreactionofthepuppieswastorushtowardthehandler,leapingagainsthimorupathishands,andnippingplayfully.Whenpatted,thepuppyusuallyturnedaroundandpawedorwrestledwiththehand,chewingonitgently.Itisobviousthatapuppyofthisagereactstoanoutstretchedhumanhandinmuchthesamewayasitreactstotheplayfulapproachofanotherpuppy.Whentwodogsinteractinthiswaytheyrearup,
DIFFERENTIALCAPACITIES
throwtheirforepawsaroundeachother'snecks,andattempttowrestleeachothertotheground,bitingandchewingoneachother'snecksandears.
Aswehaveseeninanearlierchapter,cockerspanielshavebeenselectedagainstviolentaggressivebehaviorintwoways.Oneisbyselectionforcrouchinginresponsetoanupraisedhand,andtheotherisforthehighlyrestrainedbitingor"softmouth"usefulinretrieving.Aswemightexpect,cockerspanielsrespondtohandlinginamuchmoresubmissiveandlessviolentwayandconsequentlyreceivelowerscoresforplayfulfightingthandobasenjis.
Whenwegraphthescoresofthecockers,basenjis,andhybrids,wefindapatternofinheritancewhichisdistinctlydifferentfromanyofthosewehavesofarexamined(Fig.11.1).Mostofthebasenjisre-
T
67STANINE
PLAYFULAGGRESSION
Fig.11.1.—Distributionofstaninescoresforplayfulfightingat13-15weeksofage.NotethehighlyvariableFx,overlappingthecompleterangeofbothparentbreeds.Arrowsindicatemeans.
ceivehighscoresforaggressiveness,andmostofthecockersreceivelowscores.Unexpectedly,theFihybridsincludebothhighandlowscoresandarchighlyvariable,andtheF-'sareverysimilartotheFi's.Thebackcrossestothebasenjishavealargepercentageof
aggressiveanimals,andthebackcrossestothecockershavealowpercentage.
Fromtheviewpointofgenetictheory,wewouldexpectthatbothpurestrainswouldshowlittlegeneticvariability.Likewise,thefirstgenerationhybridsshouldallhavethesameheredity,eachanimalreceivingthesamegenesfromeitherparent.TheF^'s,ontheotherhand,shouldbegeneticallyvariable,becausethegeneshavebeensegregatedorsortedoutintotheparentalandhybridtypes.Inthisactualcasetheparentbreedsarevariable,theFi'sarehighlyvariable,andtheF2'snomorevariablethantheFi's.HowcanwereconcilethiswiththetheoryofMendeliangenetics?
Thesimplestexplanationisthatwearedealingwithathresholdofresponsetostimulation.Thepuppiesareeitherstimulatedtoplayfulfightingornot.Iftheyhavealowthreshold,asinthebasenjis,theyreactwithplayfulbitingandchewingtotheslightesthumanstimulus,butiftheyhaveahighthresholdlikethecockers,theyrarelyreachthisthresholdanddolittlebitingorchewing.TheFi'shaveanintermediatethreshold;sothatthismayormaynotbereachedduringthetest.ConsequentlytheFi'smayshoweitheralargeamountofplayfulfightingoralmostnone,justasinthetwoparentaltypes.Thesecondgenerationhybridsshouldcontainallgenetictypes;buttheintermediateones,orheterozygotes,shouldrespondinthesamewayastheFi's,sothattheF2generationwillshowvariabilityexactlyliketheFi.Ontheotherhand,eitheroftheback-crossgenerationsshouldhavefeweroftheintermediateorheterozygoustypesthantheFi'sandconsequentlybemoreliketheparentgenerations.
Theonlywaytoestimatethenumberofgenesinvolvedistocalculatetheexpectedandobserveddifferencesbetweenthetwoback-crossgenerations.Forexample,ifonlyonegeneisinvolved,50percentofthebackcrossshouldbeheterozygous,andaccordingtoourtheoryhalfoftheseheterozygousanimalswouldfallintoonetypeandhalfintheother.WheretheFi'sarehalflikeoneparentpopulationandhalfliketheother,andonlyonegeneisinvolved,theback-crossshouldbethree-fourthslikeoneparentandone-fourthliketheother.Iftwogeneswereinvolved,onlyone-fourthofthebackcrosswouldbeheterozygous,whichwouldmeanthatthebackcrosswouldbeseven-eightslikeoneparentandone-eighthliketheother(Table11.2).
Thetheoreticalresultsmustbeadjustedtoallowforthefactthatthereissomeoverlapbetweenthetwopurebreeds.Theobservedre-
DIFFERENTIALCAPACITIES
suitisclosertothatexpectedfortwofactors,inwhichtheback-crossesarequitefarapart,thanitisforonefactor.Wecanconcludethattheinheritanceofthisparticulartraitcanbeexplainedbythehypothesisoftwogenes,eachofwhichlowersthethresholdofstimulationbyapproximatelythesameamount(Fig.11.2).This,of
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STIMULATION
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BX/CSCS
INHERITANCEOFPLAYFULAGGRESSIVENESSINPUPPIES
Fig.11.2.—Theoccurrenceofplayfulfightingtransformedtoascaleofthresholdofstimulation.Thisgraphisbasedonrawscores,withathresholdarbitrarilylocatedatthepointofmaximumseparation.Scoresforthepurebreedsarebasedonlyonthoseanimalscloselyrelatedtothehybrids.NotethatFjandF2arealmostidenticalandintermediatebetweenthetwoparentstrains.
course,doesnoteliminatethepossibilitythatthereisamorecomplextypeofinheritanceinvolved.Ourresultsindicateonlythattheresultscanbeexplainedonthebasisoftwogenesactinginthemannerdescribedabove.
Thisunusualbutbasicallysimplesortofinheritanceturnsupfairlyfrequentlyinbehavioraldata.ItwasprobablyoverlookedintheearlyclassicalstudiesofMendeliaogeneticsforseveralreasons.
BEHAVIORPATTERNS273
Onewasthefactthattheearlygeneticistswereinterestedprimarilyinthemodeofchromosomaltransmissionratherthanthenatureofanyparticulartrait,andsotheyusuallydisregardedanyinheritedtraitwhichdidnotgiveclear-cutdifferencesbetweenstrains.Anotheristhatthresholdphenomenaaremuchmorefrequentandmoreobviousintraitsofbehaviorthanintraitsofformandcolor,althoughthegeneticsofcolorcanalsobeanalyzedintermsofthresholds.Amousemaybeeithercompletelycolorless(asinanalbino)orallblack,andwecansaythatthereisathresholdforthebiochemicalprocessofpigment
cansaythatthereisathresholdforthebiochemicalprocessofpigmentformationwhichisreachedonlywhenaparticulargeneispresent.However,itisdifficultorimpossibleforanenvironmentalfactortoaffectthisthresholdinsuchawaythatamousecouldbeshiftedfromonecolortoanotherbyanenvironmentalaccident.Abetterexampleistheinheritanceofthenumberofsacralvertebraeinthemouse,wherecertainpuregeneticstrainshavevariablenumbersofsuchvertebrae,presumablyproducedbyrandomenvironmentalfactorsactingearlyinembryonicdevelopment.Theconceptofathresholdraisedorloweredbygeneactionandenvironmentalfactorsisthereforebasicingenetics.
Inordertohavethetypeofinheritanceshowninthisexample,withahighdegreeofvariabilityinbothFi'sandF2*s,theremustnotonlybeathresholdbutonewhichiseasilyaffectedbyenvironmentalfactors,conditionswhicharealwayspresentinbehavior.IftheFihybridsfallclosetothethreshold,theabovepatternofinheritancewillautomaticallyappear.
Thefrequencyofthiskindofinheritanceisthereforedependentnotonlyonthresholdsbutonthefactthatthesethresholdsareeasilyaffectedbyenvironmentalfactors.
Barklessness.—Oneofthestrikingcharacteristicsofthebasenjibreedisthefactthatthesedogsrarelybark.Wecanonlyspeculateastowhythistraitwasdeveloped,sinceitwasalreadypresentinthebreedwhenitwasbroughtoutofAfrica.Itispossiblethatbarking,whichisanalarmsignalgivenbydogswheneverastrangeanimalorpersonapproachestheirhometerritories,isnotconducivetosurvivalintheAfricanforests.Leopardsarereputedlyfondofdogmeat,anditmaybethatthedogwhichbarkssimplyattractsattentiontohimselfandcomestoanuntimelyend.AlthoughtravelershavedescribedbasenjisasbeingverynoisyintheirnativeAfricanhabitat,especiallyatnight,noneofthesoundsproducedarelikebarks,beingvariouslydescribedas"crowing,""yowling,"and"howling."Thissuggeststhatthebasenjismayhavedevelopedsoundswithunusualacousticqualities.Thebarkingofmostdogs,as
274DIFFERENTIALCAPACITIES
analyzedonthesonograph,consistsofasuccessionofshort,sharp,monotonoussounds,whichareveryeasytolocalize.Thatis,barkingconveysaccurateinformationastothelocationofthebarkinganimal.Ontheotherhand,soundswhichvaryinpitch,loudness,anddurationaremuchmoredifficulttolocalizewithrespecttodirectionanddistance,asanyonewhohashadexperiencewith
withrespecttodirectionanddistance,asanyonewhohashadexperiencewiththevocalizationsofcoyoteswillrecognize.Whiledistinctlydifferentfromcoyotes,thebasenjisoundshavesimilarqualitiesofvariabilityandmayservethesameadaptiveandprotectivefunction.Inanycase,basenjisbarkverylittlecomparedtootherdogbreedsand,wheneverdifferentbreedsofdogslivetogether,thebasenjis'relativesilenceisextremelynoticeable.Asastrangerwalksbythedogrunsatourlaboratory,achorusofbarksarisesfromagroupofcockerspanielsandfromanearbygroupofShetlandsheepdogs.Inapenbetween,alitterofbasenjislookupwithoutopeningtheirmouths.
Darwinthoughtthatwolvesdonotordinarilvbarkandthatwhentheydoitisbecausetheyhavelearnedthehabitfromdogs.Allmodernobserversofwolvesunderanyconditions,whetherinzoosorintheremotewilderness,agreethattheybark,althoughnotasmuchasmanydogbreeds.Thebarklessnessofbasenjisisthereforenotaprimitiveancestraltraitbutratheranewandunusualcharacteristic,producedbysomesortofselection.
Ourbestdataontherelativebarkingcapacitiesofthedifferentbreedscomesfromthedominancetestinwhichwetookeachpairoflittermatesandletthemcompeteforaboneduringaperiodof10minutes.Whilethevweredoingthiswerecordedthevocalizationsofeachanimal,includingbarks,whines,andgrowls.Wehavesuchdatafrom5,11,and15weeksofage.AscanbeseenfromFigure11.3,themaximumamountofbarkingoccursat11weeksinallbreeds,withthepossibleexceptionoftheShetlandsheepdogs,inwhichtheamountofbarkingseemstobestillrisingat15weeks.Thegraphalsoshowsthatthecockerspanielsat11weeksdothemostbarkingofanybreedandthebasenjisdotheleast.
Obviously,basenjis(oratleastthestrainwhichwehave)arenotcompletelybarkless.Whensufficientlvexcited,theywillbark.Table11.5showsthatbasenjisbarkedduring20percentoftheopportunitiesgiventhemduringthedominancetest,whereasthecockerspanielsbarkedduring6Spercent.Thebasenjisusuallygaveonlyoneortwolow"woofs"whentheydidbark,theaveragenumberbeingabouttwo.At11weeksofage,thelargestnumberofbarksgivenbyanybasenjiduringthedominancetestwas20,andthenexthighestnumberwas12.Morethanthis,thesoundwhichthebasenjis
BEHAVIORPATTERNS
275
200180160
C/M40J
or
<I20CD
6loo
8060
4o^
20
/\
/
//
//////
//...:^:;
\
\
/
\
/
\
•cs
•BEA
••SH
••WH
BA
IIAGEINWEEKS
15
10
IIAGEINWEEKS
15
Fig.11.3.—Occurrenceofbarkingduringthedominancetestsatdifferentages.Upper:averagenumberofbarks.Lower:percentageofanimalsbarking.(Notethatthesetwocharacteristicsarenotdirectlyrelated.)
DIFFERENTIALCAPACITIES
makehasadifferentqualityfromthatinotherbreeds.Thustherearethreedifferentaspectsofwhatlooksoffhandtobeasimplebehaviortrait.Oneisthethresholdofstimulation—veryhighinthebasenjiandverylowinthecockerspaniel.Asecondtraitisthetendencytobarkonlyasmallnumberoftimesratherthantobecomeexcitedandbarkcontinuouslyasdomanycockers.Themaximumnumberofbarksrecordedforacockerina10-minuteperiodwas907,ormorethan90aminute.Stillathirddifferenceisthetonequality,whichwe
TABLE11.5
TABLE11.5
PerCentofAnimalsBarkingperOpportunityComparedwithExpectedPercentage
didnotattempttoanalyze,astheequipmentnecessaryforproducingasoundspectrogramwasnotavailablewhenwestartedtheexperiment.
Inanalyzingtheeffectsofheredity,wefirstfindthattherearenoimportantdifferencesbetweenthesexeswithregardtothistypeofvocalization.Analyzingtheinheritanceofthetwotraitsisthereforereasonablysimple.TheFigenerationshowsalmostasmanyanimalsbarkingasdothecockerspaniels(Table11.5)butnotasmanyanimalsbarkingtoexcess(Table11.6;Fig.11.4).Thereisnogreatdifferencebetweenpuppiesbornofbasenjimothersandthosebornofcockers,sothatwecanruleoutthepossibilitythateithersex-linkedinheritanceorlearningbyexamplefromthemotherhasanygreatimportance.
TABLE11.6PerCentofAnimalsBarking19orFewerTimesat11Weeks
BreedorHybrid
Basenji
Cocker
F,
F,
Backcrosstococker..Backcrosstobasenji.
NumberTested
PerCent
95.218.451.353.018.862.9
BEHAVIORPATTERNS
277
Thislooksasifthetraitofbeingeasilystimulatedtobarkisinheritedasadominantone.Ifwenowcomparethepercentageofanimalswhichbarkedduringeachopportunitywiththepercentagecalculatedbyassuminginheritancethroughasingledominantgene,wefindareasonablycloseagreement,andinfactabetteragreementthanwithatwo-factortheory(Table11.5).Thisdoesnotmeanthat
20
10
BASENJI(42)
COCKERSPANIEL(49)(7animalsmorethan600)
F,(39)
F2(66)
cf"*"«■m.
BACKCROSSTOCOCKER(16)
BACKCROSSTOBASENJI(35)
100200300400500
Fig.11.4.—Distributionofbarkingtoexcessat11weeksofageinthepure
Fig.11.4.—Distributionofbarkingtoexcessat11weeksofageinthepurebreedsandhybrids.Thefigureshowsthenumberofanimalsproducingagivennumberofbarks.Notethatalmostallbasenjisbarkedlessthan10times.
thepossibilityofalargernumberofgenesiscompletelyruledout.Atesttocheckthiswouldrequireamuchmorecomplicatedexperimentandlargernumbersofanimals.Themostthatwecansayisthattheresultscouldbeexplainedinthisfashion.
Ifwenowlookattheinheritanceofthetendencytobarktoexcess(Fig.11.4),wefindadifferentsituation.TheFi'sarenowintermediatebetweenthetwoparentstrainsandtheF2'sverymuchliketheFi's.Thislookslikeacasewherethehybridsbetweentwostrains
278DIFFERENTIALCAPACITIES
haveageneticconstitutionclosetoathreshold.Consequently,eachanimalmaybepushedoverthethresholdorheldbelowitbyafewchanceenvironmentalfactors.Theresultsfromthebackcrossagreewiththishypothesis,sincethebackcrosstothebasenjisismorelikethebasenjisandthebackcrosstothecockersismorelikethecockers.Again,theresultscouldbeexplainedastheresultofasinglegene.
Insummary,theapparentlysimpletraitofbarklessnessturnsouttoinvolveatleastthreecharacteristics,ofwhichtwowereanalyzed.Thesetwoinvolvedifferentgeneticmechanisms;and,whiletheyaffecteachother,theydonotcombineinanysimplefashion.Obviously,adogwillnotbarktoexcessifitdoesnotbarkatall,andtheappearanceoftheformertraitisthusconditionalonthepresenceofthelatter.Consequently,theeffectsofthetwotraitstogethercannotberepresentedbysimpleaddition.Furthermore,thesetraitscanbestbedescribedintermsofprobabilitiesratherthanabsolutes.Givenaparticularsortofopportunity,suchasthecompetitionoverabone,thereisa20percentchancethatabasenjiwillbarkat11weeksofageanda68percentchancethatacockerwillbark.Theinheritanceofthistrait,likesomanyothers,illustratestheextremecomplexityofbehaviorwhichcanresultfromtheactionofasmallnumberofgeneticfactorsactingindifferentways.
Theresultsalsoraiseaninterestingquestionregardingthephysiologicalmechanismbehindthetraitofexcessivebarking.Someanimals,giventhestimulusofanotherpuppyinacompetitivesituation,willbarkafewtimesandthenstop.Otherscontinuetobark,becomingmoreandmoreexcitedandtaking
thenstop.Otherscontinuetobark,becomingmoreandmoreexcitedandtakingonanalmosthystericaltone.Itlooksasiftheymaybestimulatingthemselvesbytheirownbarking.Ifso,thiswouldaccountforthe"either-or"behaviorinbarking—eitherafewbarksoragreatmany.Excessivebarkingisnotonlyinterestingasagenetictraitbutalsoasitgiveshintsofthenatureofemotionalstimulation.
INHERITANCEOFDIFFERENCESINSEXUALBEHAVIOR
AllthemembersofthegenusCanishavesimilarpatternsofsexualbehavior,aswehaveshowninapreviouschapter.Oneofthepeculiaritiesoftheirbreedingcvcleisthefactthattheperiodofestrusorreceptivityinthefemaleisprecededbybleeding.Inwolvesandcoyotesthebleedingmaybeginquiteearlyintheyear,inJanuaryorFebruary,andtherearesomereportsofwolvesinwhichthisbeganinDecember.Actualmatingofwolvesusuallytakesplace
BEHAVIORPATTERNS279
inlateJanuaryorFebruaryandisnotrepeateduntilthefollowingyear.
Incontrast,thefemalesofmostbreedsofdomesticdogshaveestruscyclesatanyseasonoftheyearandapproximately6monthsapart.Thecycleisregulatedbyhormones.Afterpregnancyandalsoafteracycleinwhichnoeggsarefertilized,thecorpusluteumoftheovarycontinuestosecreteprogesteroneforseveralmonths,suppressinganyfurthercyclesaslongasitfunctions.Thelengthofthecycleisthereforeregulatedbythelengthoftimeduringwhichthecorpusluteumpersists.
Thebasenjiisdifferentfromotherdogbreedsinthatfemalescomeintoestrusataparticulartimeofyear,closetotheautumnalequinox,andshowonlyonecycleperyear.Theinheritanceofthistraitisparticularlyinterestingbecausewecanbepositivethatourparentstocksaregeneticallypureinthisrespect.Wehavenorecordsofcockersshowingseasonalcyclesandnorecordsofbasenjisshowing6-monthcycles.
However,whenwelookatindividualrecordsindetail,weseethatthereissomevariabilityinbothstocks.ThemodalmonthforthebasenjicycleisSeptember,andthevastmajorityofbasenjiheatcyclesbeginduringthelasttwoweeksofSeptemberandthefirstweekinOctober.Moreover,acertainnumberofcyclesbegininlateAugustandafewaslateasNovember.Thismeans,ofcourse,thattheintervalbetweencyclesisnotexactly12months.Thesamedogmaycome
theintervalbetweencyclesisnotexactly12months.Thesamedogmaycomeintoestrusearlyoneyearandlatethenext,sothatwehaverecordsofintervalsasshortas10monthsandaslongas14,withthegreatmajorityfallingbetween11and13.
Whenwelookatcockers,weseethatthe6-monthcycleisonlyanapproximation.Someindividualshavequiteregularcycles,comingintoheatatapproximatelythesametimeseachyear,asshowninFigure11.5.Othersaremorevariable.Theintervalmayrunanywherebetween3and11months,withthemodeatapproximately6months.Thismeansthattheshortestcyclesofthebasenjiscanoverlapsomeoftheexceptionallylongcyclesofthecockers.Thereisnoindication,however,thatthecockersshowanyremnantoftheannualspringcycleoftheirwolfancestors,orthatbasenjiseverruntwocycles6monthsapart.
Inordertostudytheinheritanceofthistrait,weretainedallthefemalehybridsuntiltheyhadgonethroughatleasttwocycles.AfewoftheFifemaleswhichwereparentsoftheF2Sweresaveduntiltheywereseveralyearsold,andwewerethusabletogetrecordsonmanyrepeatedcyclesfortheseindividuals.
DIFFERENTIALCAPACITIES
Theactualrecordswereresultsofweeklyexaminations,atwhichtimeswelookedfortheonsetofbleedingandnoteditdown,ifpresent.Thedatesarethereforeonlyaccuratewithinaweek,sincebleedingmighthavebegunasmuchas6daysearlier.Therearecertainpossibilitiesoferrorinthataslightamountofbleedingcouldbeoverlooked.Inafewcasesthishappenedandtheanimalsbecamepregnant.Insuchcasesweestimatedtheonsetoftheestruscyclebycountingback63daysandadding1week.
46810
04I2C5)
0415(15)
I670(n)
I670(n)
468101672(10)
MONTH
Fig.11.5.—Monthinwhichbleedingbeganinfiverelatedcockerspaniels:mother(0415),doublegrandmother(0412),and3daughters.Numbersinparenthesesindicatenumbersofcyclesobservedineachanimal.Notethatsomeanimalswerehighlyvariable,butsome(1667and1672)ranfairlyregularcvclesat6-monthintervals.
OurresultsshowedthattheFifemalesweredifferentfrombothparentstocks.Manyofthemhadtwocyclesinthelatterhalfoftheyearintheperiodofdeclininglight.AfemalemightcomeintoheatinJulyandagaininSeptemberifshewasnotmatedandmadepregnant.Femalesmightalsocomeintoheatinthespring,andinthoseanimalswhichwerekeptseveralyears,ourrecordsshowtwopeaks,inFebruaryandAugust.Sincethevmightskipthespringperiod,however,theFi'swerecapableofhavingevclesquitefarapartaswellasquiteclosetogether.Inshort,theFihybridsare
BEHAVIORPATTERNS
281
morevariablethaneitheroftheparentstrains,althoughfromthestandpointofgenetictheorytheyshouldallbealike.Theexplanationisobvious.TheFi'shaveinheritedthebasenjitendencytorespondtodeclininglight,buttheyhavealsoinheritedthecockertendencytoruncyclesevery6months.Theinteractionofboththesetraitsproducesahighdegreeofvariability.
Whenwelookattheotherhybrids,weseethattheF2isquite
BASENJI
BXCOCKER
246t10•1214
MONTHS
Fig.11.6.—Intervalsbetweenfirsttwoestrusperiods(inmonths).NoteindicationsofsegregationinthebackcrosstothebasenjiandwidevariationintheFvFi'salsoshowedcyclesofintermediatelengthinlaterperiods.
similarinvariabilitytotheFi,sothatacomparisonofthesetwogenerationsgivesusnocluestotheinheritanceofthetrait.Thebackcrosses,however,appeartoshowMendeliansegregation.Aboutone-halfthebasenjibackcrossesshowlongcycleslikeabasenjiandaboutone-halfshowshortercycleswhicharetypicaloftheFihybrids.Thebackcrossestothecockers,ontheotherhand,arequitesimilartocockers.Wecanthenformulateahypothesisthatthebasenjitypeofcycleisinheritedasasingle-factorrecessive,withthe
282DIFFERENTIALCAPACITIES
heterozygotesshowingthepeculiartypeofinteractiondescribedabove.SinceveryfewoftheFi'shavecyclesaslongas11months,wecantentativelyclassifyallindividualshavingcyclesof11monthsorlongerasbasenjitypesandthentestourhypothesisinthebackcrossandF2generations.Inthebackcrosstothebasenjisthetheoreticalratiomatchestheobservedratioalmostperfectly.IntheF2generationtherearenotasmanyanimalswithlongcyclesaswemightexpect,whichbringsupthepossibilitythattherecouldbetwofactorsinsteadof
expect,whichbringsupthepossibilitythattherecouldbetwofactorsinsteadofone.However,thetwo-factorhypothesisfitstheback-crossquitepoorly(theprobabilityofgreaterdeviationfromtheexpectedratioisonlytwoinonehundred).Bycontrast,theone-factortheoryfitstheF>considerablybetter,withaprobabilityof.08(Scott,Fuller,andKing,1959).
Wemaythereforeconcludethatthemostprobablegeneticexplanationoftheobservedfactsisone-factorinheritance.Thepossibilityoftwo-factorinheritanceisnotdefinitelyexcludedhowever,sincewedidnotdothecrucialexperimentforaone-factorhypothesis,i.e.,repeatedbackcrossestotherecessive.
Thereareseveralimportantconclusionsthatcanbedrawnfromthesedata.Thefirstisthatwehaveaclear-cutcaseofahighlyvariableFiwhichcannotbeexplainedbypossibleheterozygosisoftheparents.TheexplanationthereforeliesinthephysiologyofgeneactionratherthaninMendeliansegregation.Second,wehavesomeclearindicationsastowhatthisphysiologycouldbe,i.e.,onememberofagenepairfromthebasenjicausingaresponsivenesstolightchangesandtheothermemberfromthecockerspanielproducingatendencytorun6-monthcyclesinadditiontothefirsteffect,withbothmembersofthepairinteractingwitheachothertoproducethefinaleffect.Itshouldalsobenotedthatthisisquiteadifferentkindofexplanationfromthethresholdhypothesis,whichexplainsasimilarvariabilitvoftheFiscoresonplavfulaggressiveness.Finally,thiscaseshowshowthesimplestsortofMendelianinheritance,thatinvolvedinonepairofgenes,canproduceahighlycomplexandvariableresultonbehaviorbyactinguponphysiologicalprocesseswhichaffectbehaviormoredirectly.Aswehaveseeninalltheabovecases,suchcomplexityseemstobecharacteristicofgeneticeffectsuponbehavior.SuperimposeduponthealmostinfinitevariabilitypossiblefromMendelianmechanisms,wehaveastillgreatervariabilitymadepossiblethroughthephysiologicaleffectsofgenes.Ofcourse,thismakesithighlyunlikelythatanytwoindividualsinageneticallyvariablepopulationwilleverbehaveexactlyalike,eveniftheyareplacedinidenticalenvironments.Italsomakestheexact
BEHAVIORPATTERNS283
geneticanalysisofanysortofhighlycomplexbehavior,suchassuccessinproblem-solvingsituations,almostimpossiblebypresentmethods.
EFFECTSOFTHEMATERNALENVIRONMENT
InalmosteverytestthatwedidtherewassomedifferencebetweenthereciprocalcrossesintheFi's,andthesedifferenceswereperpetuatedintheF2inmanycases.Therearethreedifferentwaysinwhichsuchdifferencescouldbebroughtabout.
Sex-linkedinheritance.—Ifatraitisproducedbyasex-linkedrecessivegene,thistraitshouldappearinallthemalesandnoneofthefemalesbornfromrecessivemothersmatedtodominantfathers.Inthereciprocalcross,theFi'sfromrecessivefathersshouldallbeliketheirdominantmothers.Ifsex-linkedinheritanceispresent,itcanbeeasilyrecognizedbythefactthatthereisanimportantdifferencebetweenmalesandfemalesinoneoftheFipopulationsbutnotinthatfromthereciprocalcross.
Noindicationofthissortwasfoundinanyofthe40variablesselectedfordetailedstudy.Thelackofanycaseofsex-linkedinheritanceinbehaviorcharacteristicsinasampleofthissizeshouldnotsurpriseus,sincethereare39pairsofchromosomesinthedogandonlyoneoftheseincludesthesexchromosomes.Assumingthatthereareequalnumbersofgenesonallchromosomes,averylargenumberofgeneswouldhavetobestudiedtofindevenonecaseofsex-linkedinheritance.Thelargenumberofsex-linkedgeneswhichhavebeenfoundinmanisprobablyrelatedtothefactthatthistypeofinheritanceisveryeasytorecognizeinfamilypedigreescomparedwiththepatternofinheritanceproducedbyarecessivegenefromanotherchromosome.
Accidentalselectionofdifferentstrains.—Thereiseveryindicationthatagreatdealofindividualandstrainvariabilityexistswithinthepurebreedsofdogs,andinselectingthe4pairsofparentsforeachcrosswemayhaveaccidentallyincludedtwodifferentsortsofanimals.Withsuchaccidents,wewouldtheoreticallyexpectthattheresultingdifferencebetweenthetwoFicrossesmighteitherbeinthesamedirectionasthedifferencebetweentheparentstrainsorintheoppositedirection,dependingpurelyonchance.Thelatterseemstohavebeenthecasewithregardtophysicalsize.Bychance,weincludedanunusuallylargebasenjimaleandoneortwolargecockerspanielfemalesamongtheparentsintheBCScross.Theresultwasthattheoffspringborntotheseanimalswere,ontheaverage,larger
284DIFFERENTIALCAPACITIES
thanthoseborntothebasenjimothers.Thus,thedifferencebetweentheFi'sisintheoppositedirectionfromthatoftheparents.Wewouldtheoreticallyexpect
theoppositedirectionfromthatoftheparents.WewouldtheoreticallyexpectthatsuchadifferencewouldbeperpetuatedintotheF2generation,butthisisnottrue(Table11.8).ThattheF2'sarealikeisaccountedforbythefactthattheexcessivelylargeFianimalswerenotchosenasparents.
Ifchancehadworkedintheoppositedirection,wemighthaveselectedparentsfortheFigenerationwhosegeneswouldproduceadifferenceinthesamedirectionasthatbetweentheoriginalpurestrains.Inthiscase,accidentalselectionasacauseofthedifferencecouldnoteasilybedistinguishedfromthematernalenvironment.
Effectsofmaternalenvironment.—Ifamotherinfluencesthebehaviorofheroffspring,eitherbysomeprenatalenvironmentaleffectorbyapostnataleffectinvolvinglearningfromthemother,wewouldexpectthattheeffectwouldbeusuallytomaketheoffspringmorelikethemother.Aspointedoutabove,thereisnowayofdistinguishingthiseffectfromthatofstraindifferencesinanyindividualcase,butwecanmakeatestoftheover-allexperiment.Ifselectionofstraindifferencesweretheimportantfactor,wewouldexpectthatinhalfoftheteststhedifferencesbetweentheFi'swouldbeinthesamedirectionasthatbetweentheirparentsandintheotherhalfdifferenceswouldbeintheoppositedirection.Asitturnedout,12outof40testsshowedunlikedifferences,while28outof40showedlikedifferences.Thus,wehaveevidencethatsomesortofmaternaleffectshaveplayedanimportantpartinbehavior.
Ifsucheffectsdoexist,theyshouldbecontinuedintotheF2generationinanundilutedform.Examiningtheactualdata(Table11.7),wefindthatthereisonecaseinwhichthedifferencesintheFiandF2generationsareverynearlyaslargeasthosebetweentheparents.Thisistheattractionscoreonthehandlingtestat13and15weeksofage,whichischieflybasedonthenumberoftimeswhichadogfollowsorcomestowardanindividual.Therewouldbeampleopportunityforpuppiestolearnsuchbehaviorfromtheirmothers,asexperimentersandcaretakersenteredtheirpensweekafterweek.
Anothercasewithalessobviousexplanationisthevocalizationandtimescoresof6-week-oldpuppieswhenconfrontedwithabarrierbetweenthemandtheirfood.InthesecorrelatedscoresthedifferencesareinthesamedirectioninbothFiandF2andseemtobelittlereducedinthelattergeneration.OthertestsinwhichthereisaconsistentmaternaleffectpersistingtotheF2generation,arethetrailingtest,thetimescoreinthespatial-orientationtest,andthespeedscoreinthedelayed-responsetest.Inthefirsttwo,thediffer-
BEHAVIORPATTERNS
285
TABLE11.7
TestsInvolvingPersistentDifferencesbetweenMaternalLines(StanineScores)
Test
Attraction
Noises,barriertest
Trailing
Spatialorientation,time
Motivation,speed
Reactivity,investigation
Reactivity,escape
Heartrate,adult
Heartrate,bell
Leashcontrol
encebetweentheF2'sisconsiderablyreduced,indicatingthelossoftheeffectandprobablecomplicationsbygeneticfactors.
Severalscoresonthereactivitytestsgiveindicationsofimportantmaternaleffects,particularlythescoresoninvestigativebehaviorandattemptsatactive
effects,particularlythescoresoninvestigativebehaviorandattemptsatactiveescape.Likewise,theadultheartratescoreshowsaveryimportanteffect,asdoesoneoftheotherheartratescores.Finally,theleash-controltest,involvingthetendencytobiteandjerkaleash,showsalargeandconsistenteffectwhichisverylittlereducedinthesecondgeneration.
Inconclusion,threeofthetests,theattraction,heartrate,andleashcontrol,giveevidenceofunusuallyimportantandpersistenteffectsrunningthroughthematernalline.Thereisanobviousexplanationofhowthesecouldbeproducedintheattractionscore,andeventheheartratemayrepresentalearnedemotionalreactiontohandling.Theeffectofleashcontrolismoredifficulttoexplaininsuchtermsand,asindicatedabove,mayactuallybeanaccidentalresultofstrainselection(seechap.12).
RESULTSOFANALYSISOFOTHERTESTS
Performancetests.—Someoftheperformancetestswhichwedevisedweresodifficultthatalargenumberofpuppiesfailedtosolvethem.Thisautomaticallyforcedthedataintoatwo-categorydistributionoffailuresandsuccesses,andthisinturnsuggestedthepossibilityofanalysisbythemethodsofqualitativeinheritance.
Inthebarriertestgivenat6weeksofage,basenjisshowmuchmoreabilitytosolvetheproblemwithoutmistakesthandocockerspaniels.Likewise,inthemanipulationtests,thebasenjisshowcomparativelyfewfailuresandcockerspanielsshowalargenumber.
a.:"i-i^-±.Z---Z-n
However,there:rnplepatternofMendelianinheritanceap-
parentinthehybridpopulations.Thereasonsforthisarefairlyobviousinthemanipulation:meanimalsstartoffwellonthe
simp].andfailasthetestagetharder,pr^ise::'
alackofcapac:::anlmaUdopoorlyattheoutsetan:
a:7esctwoverydifferenttypesofreactionstothesituationprobablyinvolvequitedifferenthereditarvmechanisms,andtheycertainlyleadtocomplexres
Mostoftheotherperformancetestsweresodesignedthatall
Mostoftheotherperformancetestsweresodesignedthatall
alswouldsucceedandobtainsomesortofscoreonacontinuousscale.TheseresultsfMycouldbeanalyzedbythemethodsof
quantitativeinheritance,butherea^ainnoneofthedenceofanysimplernofMendelianinheritancesuch
forthistypeofanalysis.Therearestillothermethodswhichcanbeusedtoanalyzesuchdata,namelythecalculationoftheamountsofvarianceduetobreeddifferences,andtheresultsarepre5anotneichapter.
;—Thesizenaretheoretically
welladaptedtoanalysisbythe:sofquantitativeinheritance.
However,eventhispartofthimentiscomplicated,firstbythe
factofstraindifferencesreferredtoaboveandsecondbyhybridvigor.BoththeF7sandFi'sareontheaverageverynearlyasbigas
ops,thelargerofthetwoparents.TheincreasedbodysizeoftheF:canbeattributedtohybridvigor,andtheFa'sareinturnaffectedbvthissamehvbridvi^orinthattheirFimothershadunusuallyabundantmilksuppliesandgavethemexcellentcare.Xe
bslthebackcrossandF.generationsdoshowgreatervariation
thantheF:'s.asmightbeexpectedfromMendeliansegregation
TableUS.Calculationsbaseduponthisgiveapproximateesti-
TABLE11.8
DBTMBrnaxofAdultWeightMeasurement5Coc::sHybbids(S:si5=9kg.)
BEHAVIORPATTERNS
287
matesofonegeneaccountingforthedifferencebetweenbasenjisandcockerspaniels.
spaniels.
Theheartrateofyoungpuppiesalsoshowsacontinuousdistributionandevidenceofincreasedvariationinthesegregatingpopulations(Table11.9).Thegeneralpatternofinheritancelookslikeoneofnodominanceexceptthatthebackcrossgenerationsarealmostexactlyliketheirmaternalparents.AnalysisoftheF2datagivesafigureoflessthanonegene;butitispossiblethatifthevariancewereadjustedinvariousways,theresultwouldbemoreclear-cut.Atanyrate,theevidenceindicatesthatnotmorethantheonegeneisinvolved.
TABLE11.9
DistributionofAverageHeartRates,11-16Weeks,ConvertedtoStanines
THEDEVELOPMENTANDDIFFERENTIATIONOFBEHAVIOR
Aswesawinourstudyofthedevelopmentofthetraitsofbarkingandbarklessness,themaximumdifferencesinthattestsituationappearedat11weeksofage.At5weeksthebasenjisandcockersweretoomuchaliketomakeageneticanalysispossible,andby15weeksbothbreedshadbeguntobarksolittlethatgeneticanalysiswasagainimpossible.Thefollowingexamplesgiveanevenmoreclear-cutcaseofthedevelopmentofdifferencesinbehavior.
Inheritanceofthetendencytobequietwhileweighed.—Onceperweekeachpuppywasplacedonaplatformscaleforoneminuteandgivenmildforcedtraininginbeingquiet,asdescribedinchapter9.Figure11.7showsthedevelopmentofthebehaviorofbeingcompletelyinactivefor1minute.By11weeksofageapproximately70percentofthecockerspanielskeepquiet,andthisproportionclimbsslowlythereafter.Bythesameagethepercentageofbasenjisreaches
DIFFERENTIALCAPACITIES
approximately20percentandstaysatthesamelevel.Wecanthereforesaythatthebehaviorofthetwobreedshasbecomedifferentiated,althoughsomeoverlapbetweenindividualsstillremains.
Wecannowanalyzetheinheritanceofthetraitatthetimewhenmaximumdifferencesappear,usingmethodsforqualitativeinheritance.Inordertogiveasomewhatmoreaccurateestimate,wecanaveragethescoresat14,15,and16weeksofage.Theaccuracycanalsobeimprovedbyincludingonlythose
weeksofage.Theaccuracycanalsobeimprovedbyincludingonlythosecockersandbasenjiswhicharemostcloselyrelatedtotheparentsinthecross;itturnsoutthattheyaresomewhatmoredifferentfromeachotherthanarethetwo
i.o-
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Fig.11.7.—Changeswithageofproportionofanimalsratedascompletelyquietfortheone-minuteperiodwhileweighed,inthecockerandbasenjibreeds.
fortheone-minuteperiodwhileweighed,inthecockerandbasenjibreeds.
generalpopulationsofeachbreed.Analyzingthisresult,wegetfigureswhichapproximatethosewhichwewouldexpectfromtwo-factorinheritance,withthecockerspanieltendencybeingrecessive.Thefiguresdepartwidelyfromwhatmightbeexpectedifasinglefactorwasinvolved.
Theinheritanceofposturalresponses.—Aspartofthesametest,theinitialpostureofthepuppyasitwasplacedonthescalewasrecorded.Therearefourpossiblebehaviorpatterns:lyingflat,crouchingwiththelegsbentandheaddown,sitting,andstanding.
Inthecockers,behavioronthescaleisrelatedtothetendencyofthebreedtolieflatwhenthreatened,whichgoesbacktotheirmedievaluseinsettingbirdsforthenet.As"setters"theyweresupposedtolieflatupontheground.However,thetopofthescalewas
BEHAVIORPATTERNS
289
only10.5X12inchessquare,notanidealplaceforlyingflat,especiallyastheanimalsgrewolder,sothatthefavoritepositionofthecockerspanielpuppieswasusuallysitting.
AsFigure11.8shows,puppiesofbothbreedsinitiallyrespondby
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TH,SOCIALIZATION
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Fig.11.8.—Thedevelopmentanddifferentiationofposturalresonsesinthecockerandbasenjibreeds.Themajorityofcockerseventuallysitwhileweighed,butthemajorityofbasenjisstand.
DMTBENTIALCAPAOTES
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Fig.U.S.—Continued.
lyingflatonthescaleandcontinuetodothisthroughtheneonatalperiod.Duringthetransitionperiodtheybegintoadoptothertypesofposture.At3weeksofagebothbasenjisandcockershaveatendencytocrouchinsteadoftoliedown,butsomeofthemarebe-
ginningtositaswell.Bv5weeksofagethemostcommonpostureiscrouching,whilethefrequencyofsittinghasdeclined.Crouchingreachesitspeakat5weeksinbasenjisbutnotuntil7weeksincockersandthereafterdeclinesinbothbreedswithverylittledifferencebetweenthem.Ascrouchingdisappearsitisreplacedbystandinginthebasenjisandbysittinginthecockers,sothatat16weeksofageabout70percentofthecockersaresittingandnearly90percentofthebasenjisarestanding.Thecurveforsittinginthecockersisstillrising,indicatingthatthebehaviorhasnotbeenfullydifferentiatedinthisbreed.However,inbothbreedsthepercentageofanimalsstandingisprettywellstabilized.
Analyzingtheratiosbasedonscoresat14-16weeks,whenthetendencytostandismostcompletelydifferentiatedbetweenthetwobreeds,wefindthattheratiosfitwhatmightbeexpectedifthereweretwogenesinvolved,thoseforthecockerspanielbeingdominant.Thefitisnotasgoodasitwasinthetraitofbeingquiet,butthismayresultfromthefactthatbodysizehassomeeffectonthepostureonthescales.Inbothcockersandbasenjis,thereareconsistentlymorefemalesstandingthanmales,probablybecausetheirsmallersizemakesiteasiertodoso.Likewise,theF2animalssometimesbecameunusuallylargeduetotheexcellentnutritionprovidedbytheirFimothers,andfeweroftheF^'stookthestandingposturethanmighthavebeenexpectedfromasimplegenetictheory.
Oneinterestingresultoftheexperimentisthatthebehaviorofthecockerspaniels,whichlookslikeasimplebehaviorpatternoflyingquietlyonthescale,isactuallymorecomplex.Beingquietisinheritedasarecessivetrait,theFi'sbeingactivelikebasenjis.Thetendencytoadoptsomeotherposturethanstanding,ontheotherhand,isinheritedasadominanttrait,withtheFi'sbeingliketheircockerparents.Weareobviouslydealingwithtwodifferenttraits,andthisisbackedupbythefactthatthereisnocorrelationbetweenthemintheF2puppies,inwhichbothtraitscanappear.Sinceourresultsindicatethatatleasttwogenesareinvolvedineachoneofthesetraits,thegeneticmechanismisquitecomplex.ThechanceofgettingananimalgeneticallyidenticaltooneoftheoriginalpurebreedsintheF2generationis(0.25)4,or1in256.Sincewe
theoriginalpurebreedsintheF2generationis(0.25)4,or1in256.Sinceweonlyhad74animalsinthisgeneration,itisquitelikelythatnoneofthemwereexactlyliketheoriginalpurebreedinrespecttothistrait.
Theotherinterestingresultofthisexperimentisthealmostdiagrammaticillustrationoftheprocessofdifferentiationofbehaviorresultingfrommaturationandtraining.Thegraphsshowallpuppies
292DIFFERENTIALCAPACITIES
startingoutverymuchthesameandgraduallybecomingmoreandmoredifferentuntilfinallytheyshowthebehaviorwhichweordinarilythinkofasbeingcharacteristicofthebreed.
SUMMARY
Theseanalysesoftheinheritanceofsimplebehaviortraitsshowthatinheritancecanbeexplainedinmanycasesonthebasisofoneortwogenes.Thisissomewhatsurprising,aswewouldexpectthatanythingascomplexasbehaviorwouldbeaffectedbymanygenes.Weshouldremember,however,thattheseparticulardifferencesinbehaviorwereproducedbyartificialselectionandthattheeffectofageneonacharacterasvariableasbehaviorcouldprobablynotberecognizedunlessitwasquitealargeeffect.Abreederchoosingbetweentwodogsusuallycannotdistinguishbetweenbehavioraldifferencesproducedbyheredityandthoseproducedbytrainingandotherenvironmentalexperiences.Unlessageneproducesarelativelymajorresult,itislikelytopassunnoticedandbelost.Minormodifyingfactorsseemtohavetheirchiefimportanceincontributingtoindividualandstraindifferenceswithinabreed.
Weshouldalsorememberthatthebehaviorpatternis,inonesense,anaturalunitofbehavior.Allselection,whetherartificialornatural,isdoneonthebasisofeffect,andthemodificationofbehaviorpatternshavingspecificfunctionsisconsequentlythemostdirectwayinwhichselectioncanaffectbehavior.Ofallthemeasuresofdifferenceinbehavior,thoseinvolvingsimplebehaviorpatternsaremostlikelytohavedirectandreasonablysimplegeneticexplanations.
Whilethepossibilityofsingle-factorinheritanceisthusareasonableone,thisconclusioncannotbefinalintheabsenceofacriticaltestforsingle-factorinheritance,namelv,asecondbackcross.Confirmationwillthereforehavetoawaitfurtherexperimentation.Assumingthatthesingle-factorexplanationisavalidone,weshouldpointoutthatitworksbestwhenappliedtocasesinwhich
validone,weshouldpointoutthatitworksbestwhenappliedtocasesinwhichsimplebehaviorpatternsareeitherpresentorabsent.Thisisconsistentwiththetheoryofathresholdofresponsetostimulationmodifiedbygeneaction.
Ontheotherhand,thetheoryofathresholdmodifiedbyasinglegene,orIn-theadditiveactionofseveralgenes,doesnotapplytoanycaseofathresholdofsuccessfuladaptationtoacomplexproblem-solvingsituation.Heretheunderlvingprocessesofgeneaction
BEHAVIORPATTERNS293
appeartobemuchmoreintricate.Thereisevidenceinthecaseoftheinheritanceoftheannualbreedingcyclethattheactionofevenasmallnumberofgenescanproduceextraordinarilycomplexeffectsthroughinteractiononaphysiologicallevel.Beyondthis,thecombinationoftwosimplyinheritedpatternsofbehaviormultipliesthenumberofpossiblegeneticcombinationsforthewhole.Evenasmallnumberofgenescanthusproduceanenormousamountofvariabilityinapopulation.
Whilebothsimplequalitativeandquantitativeinheritancearesometimesfoundinrelationtosimplepatternsofbehavior,thecombinationofthesepatternsintocomplexadaptivepatternsthroughlearningandproblemsolvinginevitablyresultsinanextremelycomplexgeneticsituation.Themultiple-factortheoryofgeneticeffectsofbehavioriscorrectinthesensethateachbehaviorpatternappearstobeaffectedbyadifferentsetofgenes.Ontheotherhand,extremelycomplexeffectscanbeexplainedbyasmallnumberofgenes,sothatthegeneticmechanismsareprobablybasedonafinite,andpossiblyrelativelvsmall,numberofmutations.
Wealsofindthatbehaviorhastobedeveloped:thatitonlyappearsatparticulartimesindevelopmentandunderparticularenvironmentalconditions.Theinheritanceofasimplephysicaltraitlikelongandshorthairseemstocontradictthisfinding,butthecontradictionisonlyanapparentone.Eveninthiscasewefindthatthetraitundergoesdevelopmentbecausepuppiesatbirthhavehairwhichismuchthesamelength,andbeforebirththereisatimewhenthefetushasnohairatall,shortorlong.Thisemphasizestheimportantfactthatgeneticcharacteristicsorphenotypesarenotinastrictsenseinherited,butalwaysdevelopedundertheinfluenceofgeneticandenvironmentalfactors.Thebigdifferencebetweenbehaviorandtheanatomicalcharacteristicsusuallystudiedbygeneticistsisthatthegreatbulkofbehavioraldevelopmentoccursafterbirthratherthanbeforeandthatbehaviorcontinuestodevelopanddifferentiate
ratherthanbeforeandthatbehaviorcontinuestodevelopanddifferentiatethroughoutlife.
Inthischapterwehaveindicatedtwodifficultiesindealingwiththedata.Oneoftheseisthatmostofthemathematicalmethodsusedsofarassumethattheparentpopulationsarepurebreeding,althoughwehaveeveryreasontobelievethatthedogbreedsaregeneticallyvariableinmanyrespects.Theotherdifficultyisthatofapplyingquantitativemethodstocasesinvolvingcomplexinteraction,whetheronthegenetic,physiological,orbehaviorallevels.Inthenextchapterweshallattempttodealwiththesedifficultiesby
294DIFFERENTIALCAPACITIES
theuseofquantitativemethodswhichdonotdependupontheassumptionofhomozygosity,andwewillalsoseeifthesespecializedmethodsapplytotheinheritanceofcomplexpatternsofbehaviorwhereitishighlylikelythatmanygeneticfactorsareinvolved,andhencethatsomeofthemareheterozygous.
BEHAVIORINHYBRIDS:COMPLEXBEHAVIOR
Inpreviouschapterswehavedemonstratedthatbreedsofdogsdiffersignificantlyintheirscoresonalargenumberofbehavioraltests.Onoccasion,therelativeimportanceofthebreeddifferenceshasbeenexpressedasanintraclasscorrelation,definedastheproportionoftotalvarianceascribedtobreeds.Correlationsof.2to.5werecommon;20outof34variablesanalyzedinTable14.3fallwithinthisrange.Onsomemeasuresthedegreeofoverlapbetweenthebreedswasconsiderable,butexampleswerealsofoundofalmostcompleteseparationofscoresinsomebreeds.Inthischapterweshallattempttoextendthissortofanalysistohybrids,andparticularlytocasesofcomplexbehaviorinwhichnosimplepatternofinheritanceisapparent.
Thegeneralbiologicalsignificanceofestimatesofgeneticeffectsderivedfrombreedcomparisonsislimitedbythepeculiaritiesofthematingsystembywhichbreedsareformedandmaintained.Apurebreedisfarfrombeingahomogeneousgroup.Thecockerspaniels,beagles,andShetlandsheepdogsshowedsegregationatcoatcolorloci,thebeaglesforhairlength,andallbreedsshowedheterogeneityinbloodtype(CohenandFuller,1953).Thus,tousebetween-breedvarianceasameasureoftheeffectsofheredityandwithin-breedvarianceasameasureofenvironmentaleffectsissimplificationwhichcouldleadtoerror.Ifsomeofthebehavioralvariationbetweenmembersofthesamebreedisgenetic,theintraclasscorrelationtendstounderestimatetheimportance
breedisgenetic,theintraclasscorrelationtendstounderestimatetheimportanceofheredity.Ontheotherhand,fixationwithinabreedofspecialcombinationsofgenescouldproducepeculiaritiesofbehavior.Suchcombinations,maintainedbyrestrictingmatingswithinabreed,wouldbegeneticinthebroadsense.Inarandommatingpopulation,thesecombinationswouldbe
295
296DIFFERENTIALCAPACITIES
brokenupbecauseoftheindependentassortmentofchromosomesandthepeculiaritiesofbehaviorassociatedwiththemwouldberare.Ifthisargumentholds,breeddifferencesmightprovideanexaggeratedestimateoftheimportanceofheredityforbehavioralvariationinapopulationwithamoreopenbreedingsystem.
METHODS
Breedingplan—geneticimplications.—Inordertoextendourinformationonthetransmissionofbehavioralcharactersthroughgenes,crossesweremadebetweenbasenjisandcockerspaniels.Thesetwobreedswerechosenforthehybridizationstudybecausetheyshowedmarkedphenotypicdifferencesonmanytestsandwerealsoaboutasremotelyrelatedasanytwobreedscouldbe.ItwillberecalledthatfourofourfivepurebreedsoriginatedintheBritishIslesandthatthebasenjisisofAfricandescent.Historicalevidenceindicatesthattherehasbeennogeneticinterchangebetweenthebasenjisandthecockerspanielsforatleastseveralcenturiesandpossiblyforthousandsofyears.Wewerealsoawareofconditionswhichmadethesetwobreedslessthanidealforageneticexperiment.Preferablythestocksemployedasparentsforacrossshouldbepure-breedinginastrictgeneticsense,atleastforthelociofinterest.Itisunlikelythatthisconditionwasmetinourbreedsexceptpossiblyforlocicontrollingbarklessnessandanannualbreedingcycle,butitisalsotruethatonmanyphenotypicmeasuresthedegreeofoverlapbetweenthebasenjisandcockerswasverysmall.Anotherdifficultyarosefromtheneedtobreedfromasmallnumberofparentsbecauseofkennelspacelimitations.Inahighlyinbredstockoneparentisgeneticallyequivalenttoanyotherofthesamestock,butinavariablepopulationthechoiceofparentsintroducesasamplingerror.SamplingerrorwaspossiblyresponsibleforsomeofthedifferencesfoundbetweenreciprocalFicrosses,thoughanalternativeexplanationinvolvingmaternaleffectshasnotbeenexcluded.
Asdescribedinchapter1,thebasenji-cockerspanielcrosswasessentiallyanordinaryMendeliancrosswithcertainmodificationsmadenecessarybythenatureofouranimals.ReciprocalbasenjiXcockermatingsweremadetoproducetwoFi's,eachofwhichwasbredinterseandbrothertosistertoproduceanF2population.Ideally,backcrossestotheparentalstrainswouldhavebeenmadeinreciprocalfashion,butlimitationsofspaceandtimeledustobreedinonlyonedirection,Fimalestoabasenjiorcockerdam.This
COMPLEXBEHAVIOR297
crossenabledustocompareoffspringofpurebreddamsbyFiandpurebredsires.
Sincethepuppieshadnophysicalorsocialcontactwiththeirsires,anydifferencebetweentheCSBFiandtheCSBXBbackcrossorbetweentheBCSFiandtheBCSXCSbackcross(seeFig.1.1)canbeattributedtothegeneticcontributionsofthesires.TheplanalsoallowedfortwocomparisonsbetweenbackcrossandF2groupswithcommonsires(Fi)butdifferentdams(Fiorpurebred).WefoundthattheFifemalesprovidedbettercarethaneithertypeofpurebred,thisbeingreflectedinlowerinfantmortality.Furthermore,offspringwereassociatedwiththeirdamsfor10weeks,offeringampleopportunityforlearningandimitation.Thus,thefindingofanydifferencebetweenFa'sandthebackcrossesfromthesamesirecanreasonablybeascribedinparttonon-genetictransmissionfromdamstooffspring.
Analysisbygroups.—Thedatafromthehybridsweretreatedintwoways—bygroupandbymating.ThegeneralprocedureisavailableinvarioussourcessuchasWright(1952)andFalconer(1960).Intheanalysisbygroup,weprovisionallyassumedthatbasenjisandcockerspanielswerepurebreedingforthemajorlociproducingbehavioraldifferencesbetweenthesestrains.Basenji,cockerspaniel,andFihybridgroupswereconsideredgeneticallyhomogeneousandallsiresordamswithinagroupasgeneticallyequivalent.Furthermore,wepredictedthattheheterogeneousF2andbackcrossgroupswouldbemorevariablethanthehomogeneousparentalandFigroupssincegeneticvariationbetweenmembersofthesegroupswouldbesuperimposeduponenvironmentalvariation.Theseexpectationswerenotoftenrealized,andaconsiderationoftheoutcomeofspecificmatingswithoutrespecttothegroupclassificationoftheparentswasfrequentlymoreenlightening.Nevertheless,onmanymeasuresinwhichthespanielsandbasenjisdifferedsharply,wefoundthatthemeansofthehybridgroupswerearrangedinanorderlyfashioncorrespondingtothegenetic
groupswerearrangedinanorderlyfashioncorrespondingtothegeneticcontributionoftheoriginalpurebreeds.Hadtheoriginalstocksbeenmorenearlyiso-genous,theresultswouldhaveprobablybeenevenmoreconclusive.
Analysisbymatings.—Inthistypeofanalysis,itisnotnecessarytoassumethattheparentstockswerehomozygous.Onthecontrary,wecantreatthedataasthoughtheparentscamefromamixedpopulation.Twomethodswereusedintheanalysisofoutcomesofspecificmatings.Regressionsbetweenthemean(d)ofoffspringfromamatingandthephenotypicscoresoftheirsire(s),dam(d),andmidparentoraverageofsireanddam(mp)were
298DIFFERENTIALCAPACITIES
computed.AregressionequationoftheformXj=a+bXPshowstherelationshipbetweentheaverageoftheoffspringofamating(Xz)andsomescoreoftheparents(Xp).Theconstantaallowsforthefactthattheoffspringmayaveragehigherorlowerthantheparents.Theconstantb,regressioncoefficient,hasgeneticsignificance(Falconer,1960).Forexample,theregressioncoefficientbb.mpisadirectestimateofheritability(h2);bz.aandbs.sareestimatesofh2/2.Sincetheonlyconnectionbetweenthesiresandtheiroffspringisthecontributionofgenes,2bs.sisordinarilythemostdependableestimateofh2.Insomecircumstances,however,wefoundthatoursiresweretoouniforminbehaviortoprovideagoodestimate;forsometestsscoresofallparentswerenotavailableandparent-offspringcorrelationwereunobtainable.
Analysisofvariance.—Asecondmethodofutilizingdatafromspecificmatingswasbyanalysisofvariance,whichenabledustoevaluatethegeneticcontributionofindividualsiresanddams,theimportanceofenvironmentalfactorsoperatingondifferentlittersofthesameparentage,andtosomedegreethevariationbetweenthegeneticcontributionsofparentsclassifiedinthesamegroup.Thedetailsoftheprocedureandinterpretationaredescribedlaterinthischapterinconnectionwiththefightingscoresinleashtraining.
Weshalldealwiththescoresofhybridsonagroupoftestsadministeredbetween4and12monthsofage.Allofthesetestshavebeendescribedinpreviouschaptersandprovideawidesampleofkindsoftestsandgeneticresults.Someofthemwereinitiatedsomewhatlaterthanothersintheprogramandhencehavemorelimitednumbersintheparentstrains.Inthesecasestheuseofthelastdescribedmethodwasparticularlyapplicable.Analysesarereportedonthefollowingscores:leash-controlfighting,leash-controlvocalization,motivationspeed,obediencecompositescore,spatial-orientationerrors,andtotal
motivationspeed,obediencecompositescore,spatial-orientationerrors,andtotalreactivityscore.Additionalmeasuresfromthesetestsarereportedinlessdetail.Theorderofdiscussioncorrespondstothatinwhichthetestswereadministered.
TRAININGTOLEAD
Analysisl)\jgeneticgroups.—Theleash-trainingprocedureandtheresultswiththepurebreedshavebeendescribedinchapter9.Thebasenjisandcockerspanielsdifferedsignificantly,particularlyonthecategoryofdemeritwecalled"fightingtheleash."Astrainingproceededtheaveragetotaldemeritsfellprecipitouslyinallbreedsuntilby10daysmostsubjectswerewalkingwellontheleash,
COMPLEXBEHAVIOR
299
thoughbasenjiswerestillchargedwithmoredemeritsthancockers.Whenoneusesthetotaldemeritscoreover10daysasameasureofperformance,allthehybridgroupsareintermediatetotheparentalstocksandthereisnosignificantdifferentiationbetweenthem(Table12.1).Thevariances(V)oftheF2andbackcrossgenerationsaresomewhathigherthanthoseoftheparentsandtheFi's.Esti-
TABLE12.1Leash-TrainingDemerits(Stanines)ofHybrids
matingtheheritability(hr)ofthetotaldemeritscorebytheformula
h2=
VF2
V
P2
andusingpooledestimatesfromthetwoFi's,oneobtains
Thisvalueshouldbeconsideredanapproximation,however,sincetheassumptionsofhomogeneityinvolvedinthegroupmethodhavenotbeenfullymet.Furthermore,thetotaldemeritscoreisobtainedbyaddingtogethertheoccurrencesofverydifferentformsofbehaviorwhichmayhavequitedifferent
occurrencesofverydifferentformsofbehaviorwhichmayhavequitedifferentdegreesofhereditarydetermination.
Amorefruitfulattackistoconsidertheperformanceofthehybridsandtheparentalstockswithrespecttotheindividualmeasurementswhichmadeupthedemeritscore.ThesefiguresarepresentedinFigure12.1.Comparisonofthefiguresimmediatelydemonstratesthattheroleofheredityindeterminingthetypeofdemeritsdiffersgreatlyforthetests.Theparentstrainsdifferedconsiderablyinfighting(F)andposition(F)demerits,andthehybridsfellatintermediatepositions.Ifthebehaviorwereinheritedinasimpleadditivemanner,thehybridmeanswouldfallonthelinedrawnbetweentheparentalmeans,(seeBruell,1962).Thereis
:::
:-'.-r.z-'-z'n
indicationofamaternaleffect,sinceanimalsresembletheirmothersmorethantheirfathers.Neglectingthesexchromosomes,thegeneticcontributionofthesexesisequal,butthesixeshadnocontactwiththeiroffspringwhilethedamswerewiththemfor10week
Fig.12.1.—Meanscoresofhybridsonairesofleashtraining.Solid
Idenotegroupswithbasenjimothersorgrandmothers.Alinedrawn
throughacircleindicatesanF2group.Thedashedlinesbetweentheparental
meanswouldpassthroughthehybridmeansifthecharacterswereinherited
inasimpleadditivefashion.
Ontwomeasures,fightingtheleash(F)andposition(F),theparentalstocksaredistinctandthehybridsintermediate.Inbothscoresthehybridsresembletheirdamsorgranddamsmorethantheirsiresorgrandsires.Onthreemeasures,balksintheopen(B),atdoorsD.andinterference(/),theparentalscoresaresimilarandthehybridsvan*non-systematicallwOnthesixthmeas-
Lire,vocalization(V),allhybridgroupsscorewellaboveeitherparentalstock.Wegetamuchclearerpictureofthephenotypicdifferencesandpossiblegeneticmechanismsfromthisdetailedanalysisthanfromtheoverallperformancescore.
mechanismsfromthisdetailedanalysisthanfromtheoverallperformancescore.
Theleash-fightingscoreswerediscussedinchapter11whereastrongmaternaleffectwaspointedout.Thewithin-littervariancesoftheparentalandhybridgroupsaresetforthinTable12.2.UsingthevariancesoftheFiandF2,onecanestimateheritabilityas0.52.Thisisasomewhatlowerestimatethanthatbasedonthetwopurebreedsalone,0.77(seechap.14)butisofthesameorderofmagnitude.Itishigherthanthatobtainedforthetotaldemeritscore,reinforcingtheconclusionthatspecificscoresaremoremeaningfulthancomplexcombinedscores.
TABLE12.2
wlthin-llttervarianceofthefightingscoreofLeashTraining
Unfortunatelythebackcrossvariancesgiveamuchworsefittoasimplemodelthandothetotalvariancesanalyzedinthepreviouschapter;theBCS-CSvalueisunexplainablyhighandtheCSB-Bvalueistoolow.Dominanceofthebasenjigenescouldaccountforthisfindinginpart,butsuchaninterpretationisnotsupportedbythemeans,whichsupportthehypothesisofpartialdominanceofcockerspanielgenes.Similarinconsistenciesinthevariancesofthehybridsrepeatedlyturnedupinouranalysis,possiblydependentuponthescalesusedforphenotypicmeasurement,andpossiblyreflectingaccidentsofrandomsampling.Theorderingofmeansforthefightingandpositionscoresisconsistentwithgeneticdeterminationofthescores,butthewithin-groupphenotypicvariancesdonotincreaseproportionatelywithgeneticheterogeneity.Wecanseekthecluestothesourcesofwithin-groupvariationinacomparisonofrepeatedmatings.
Variationbetweenlittersofthesamemating.—Ifenvironmentalfactors(suchasthoseassociatedwithspecifictestersandmonth
DIFFERENTIALCAPACITIES
oftesting)wereimportant,wewouldexpectrepeatedlittersfromasinglematingtovarywidelyfromeachother,sinceeachlitterwouldhavehadadifferenthistorv.Ontheotherhand,ifheredityhadplavedanimportantrole,successivelittersofamatingshouldberelativelysimilar.Maternaleffectscouldalsobeconsistentfromlittertolittersothatthiskindofenvironmentaleffectcannotbeexcludedbvthefindingofconsistencyofperformancebetweenrepeatedlittersfromthesameparentage.
fromthesameparentage.
Onlyapartofoursample(F2'sandbackcrosses)wassuitableforthelitters-within-matinganalyses,sinceeachofthesegroupscontainedseveralduplicatedmatings.TheresultsobtainedwiththefightingscoresarepresentedinTable12.3.Differentlittersofapar-
TABLE12.3
AnalysisofVariance—FightingScoresofHybridsbyMatings.andLitters
ticularmatingdifferinsignificantlyamongthemselves,althoughdifferencesbetweenmatingsarehighlysignificant.Theevidenceforcontroloffightingbygeneticsorbvmaternalinfluenceisthereforestrong.
Effectofsireanddam.—Inordertodistinguishbetweengeneticinfluencestransmittedequallybvbothparentsandassociativeinfluencesderivedsolelyfromthemother,amoredetailedanalysiswascarriedoutondatafrommatingsinwhichasinglesirewasbredtotwodifferentfemalesorasingledamtotwosires.Thegroupsavailableandtheirmeansonthefightingscoreoftheleash-controltestsaresetforthinTables12.4and12.5.Wehaveheretheequiva-
TABLE12.4Leash-ControlFightingScore—OffspringofFiSiresbyDifferentDams
COMPLEXBEHAVIOR
3C3
lentoffourexperimentswithsomesubjects,thebackcrosses,appearinginboththecommon-sireandthecommon-damexperiments.LookingatTable12.4,weseethattheoffspringofFisireshavefightingscoreswhichareontheaverageintermediatetotheparents.
TABLE12.5Leash-ControlFightingScore—OffspringofPurebredDamsbyDifferentSires
Allthevariationintheoffspringcanbeattributedtothedifferencebetweendams,becausethemalesusedhadalmostidenticalfightingscores.
InTable12.5wehaveanopportunitvtoseewhetherthemaleparentsinfluencedtheamoutoffighting.Itappearstomakenodifferenceastowhetherbasenji
theamoutoffighting.ItappearstomakenodifferenceastowhetherbasenjifemalesarebredtoCSorCSBmales,butinspectionofthescoresshowthatthetwogroupsofmaleshaveextremelysimilarfightingscores.CockerspanielfemalesproduceverydifferentoffspringwhenbredtoBandBCSmales;herethemeansofthesiresdifferby2.7.Weconcludethatthetransmissionoffightingbehaviorfrommalesisdemonstratedandthattheeffectmustbegenetic.
AmoreelaborateanalysisofvarianceofthedatasummarizedinTables12.4and12.5appearsinTable12.6.Ineachofthefouranalyses,thebetween-matingsumofsquareswaspartitionedintwoways:first,accordingtoindividualsiresordams,forexample,theoffspringoftheCSBmalesinPartA;second,comparingthesignificanceofthedifferencebetweenthemeansofthetwoclassesofoffspringproduced,forexample,inPartAthedifferencebetweenCSBXBandCSBXCSB.Inallfouranalysesthelitters-within-matingcontributiontovariancewasnon-significant,whichisgoodevidencethatchangesintesters,weather,andthelikehadlittleeffectuponthescores.Thewithin-matingmeansquarewasthususedasthedenominatorinthecomputationofFratios.
WeshallnowconsiderthetwosetsofmatingsofFisirestoparentalandFidams.NoneofthecomponentsintheBCSXBCSandBCSXCSexperimentwassignificant,thoughthedifferencebetweentheoffspringofthetwotypesofdamscameclose.Atfirst
TABLE12.6AnalysisofVariance—FightingScoreinLeashTraining
Degez•teofYak:Fee:SqdakbF
CSBgrudnringCSBXBAandCSBXC5B
Sires35.824.92**
Damsinsires45.514.6;"
Typeofdam19.177.74**
Betweenlikematings...65.064.27'"
Withinmatings711.18
BCSsireswithCSandBCSdamsproducingBCSXCSandBCSXBCS
Sires2
Sires2
Damsinsires3
Typeofdam1
Betweenlikematings4
Withinmatings56
resproducingCSBandCSBXBA
Dams3
Siresindams4
Typeofsire1
Betweenlikematings6
Withinmatings59
CSdamswithBAandBCSsiresproducingBCSandBCSXCS
Dams2
Siresindams3
Typeofsire1
Betweenlikematings.4
Withinmatings44
•P<.05"P<.01
glancetheCSBXBAandCSBXCSBexperimentslookquitedifferent.Thehighlysignificantmeansquarefordifferencesbetweensirescouldindicategreatheteropreneitvinthegeneticcharacteristicsofthemalesselectedfortheexperiment.However,intheanalysisofthedamscontributions,wefindahighlvsignificanteffectduetobreedofdam(basenjivs.CSB)andheterogeneitvbetweenmatingsofthesameclass.Inspectionofthephenotvpicscoresoftheparents(Table12.4)supportstheviewthatthevariationbetweensiresisaccountedforbythedamstowhichtheyweremated.AllfourCSBhadidenticalscoresof5.0,andtheirmatingswerenon-informa-^pecttotheinheritanceoffightingthroughthemaleparent.Fortunately,intheCSdamcrosses,typeofsirewasthemajorgeneticfactorinfluencingthefightingscores.Theformal
COMPLEXBEHAVIOR
analysisconfirmsthesignificanceofthedeductionsbasedoninspectionofgroupmeans.
Thusitisdemonstratedthatleashfightingcanbeinheritedfromeitherparent,andthefailurestodemonstratedifferencesamonglittersoftheFimaleswereapparentlytheresultofacurtailedrangeofphenotvpicdifferentiation.Thematingswhichcomparedunlikeparentsmatedtocommonparents,eithersiresordams,yieldedcleare\idenceofheritabilitv.
Wearehesitanttoestimateheritabilitvofthefightingscorefromthedataavailablesincenotallconditionsrequiredbythevariousmethodshavebeenmet.Itisinteresting,however,tonotetheregressionofoffspringmeansonmidparentvalues,b'},—0.4.54=0.135.Thisvaluewascalculatedfromallthehvbridandpurebredlittersforwhichdataonbothparentswasavailable.Theregressionofoffspringmeansondamswas0.233=0.0S0,ingoodagreementwithaheritabilitvestimateofabout0.45.Theregressionofoffspringonsireswasonly0.110,buttheestimateislessaccuratebecausetheaccidentsofsamplingproducedagroupofsireswithonlvhalfthevarianceofthedams.Thevaluesarelowerthanthoseestimatedfromthegroupdifferences.
Thefightingscoreshavebeendiscussedinsomedetailbecausetheyillustrate
Thefightingscoreshavebeendiscussedinsomedetailbecausetheyillustratetheproblemsofanalyzingtheinheritanceofarela-tivelvsimplequantitativecharacterofmoderatelvhighheritabilitv.
Comparisonofvocalizationwithleashfighting.—Vocalizingduringleashtrainingisofsomegeneralinterest,sinceyelpingisaconspicuousresponseandhasbeenusedasanindexofdistressinpuppiesFredericson.1952.Itisalsoofinteresttocomparevocalizationscores,whichshowedsuchadifferentpatternofmeans,withleashfighting.Allofthehybridgroupsscoredwellabovethemeansofbothparentalstocks,whichwerequitesimilartoeachother.Thecombinationofgenesfromthebasenjiandcockerspaniellinesthusfavorstheelicitationofvocalresponsesbythemildlystressfulprocessofleashtraining.Itshouldbenotedthatvocalizationontheleashisofadifferentsortfromthebarkinganalyzedinthelastchapter.
Adetailedanalysisofthevocalizationscoreswasmadeinthesamemannerasthatusedforthefightingscores.Withvocalization,however,theoffspring-midparentcorrelationwaszero.Thedatawerethenarrangedbymatingswhichinvolvedcommonsiresordams.ItisclearfromTables12.7and12.Sthatthescoresoftheoffspringhavenosystematicrelationshipstothemeanscoresoftheparental
306DIFFERENTIALCAPACITIES
TABLE12.7Leash-ControlVocalizationScore—OffspringofSiresbyDifferentDams
TABLE12.8Leash-ControlVocalizationScore—OffspringofDamsbyDifferentSires
groups.Ananalysisofvarianceuncoverednosignificantdifferencesbetweentheseparatematings.
Wehavehereaperplexingdifferencebetweenthehybridsandthepurebreeds.Differencesinvocalizationbetweenthefivebreedswerehighlysignificant(F<.01)andwereoneofthemostusefulscoresfordiscriminatingbreedbehaviorpatterns.Furthermore,itiswellknownthatvocalizationrespondstogeneticselection.Evidenceisprovidedeachtimeahoundbaysonthetrailoratoybreedbarksshrillyatastranger.Vocalizationintheleash-trainingtest,however,occurswhentwoconditionsaremetinthesamesubject—itmustbeemotionallvarousedandvocalizationmustbereadilyemitted.Byandlarge,ourcocker
arousedandvocalizationmustbereadilyemitted.Byandlarge,ourcockerspanielswerenoisyanimals,butthevwererelativelydocileontheleashandearnedaveragevocaliza-tionscores.Thebasenjiswerehighlyexcitedbytheleashbutdirectedtheirenergiesintochannelsotherthanvocalization.Thehybridswerearousedlikethebasenjis,andvocalizationwasafavoredresponse,possiblybecauseoftheirspanielgenes.However,thequantityolvocalization,oncethenecessaryconditionsweremet,wasindependentofheredity,asdemonstratedbythelackofaparent-offspringcorrelation.
MOTIVATIONTEST
Themotivationtest,describedinchapter10,wassimplyameasureofrunningspeedinaT-inaze.Onanyonetrialabarrierforcedthe
COMPLEXBEHAVIOR
307
dogtooneortheotherarmoftheT.Fivetrialsontherightandfiveontheleftweregivenoneachofthreeconsecutivedays.Thetotalrunningtimeonthethirddavwasourmeasureofmotivation.ThemeanscoresofthehybridgroupsandtheparentalstocksaregiveninFigure12.2.Theparentalstrainsweresignificantlydifferent,andbasenjisselectedasparentsforthehybridshadmuchlowerscoresthanthebreedasawhole.Themostinterestingfeatureofthedataistheelevationofthehybridscoresascomparedwiththeparents,asituationsimilartothatofvocalizationduringleashtraining.Ifwecanexcludeanvenvironmentaleffectwhichfavoredthehybrids(whichobviouslyweretestedatadifferenttimethantheirparents),itappearsthathybridsranfaster,perhapsduetophysicalsuperioritybasedupongeneticheterosis.Wepostulateadualmechanism—first,cockerspanielgenesascomparedwithbasenjigenesincreaseattractiontofoodandtohumanbeings.(Alternativelyonecouldinterpretthedataintermsofincreasedtimidityproducedbybasenjigenes,whichisperhapssayingthesamething.)Secondly,runningspeeddependsnotonlyuponthedegreeofattractionforthereinforcementprovidedattheendoftherunway,
6.0
5.0Ll)
<S4.0
3.0
B-B(34)
CSB.B(43)
P.F2
(52)(73)
BCS-CS(30)
CS-CS(40)
Fig.12.2.—Meanmotivationspeedscoresofhybrids.PointsidentifiedasinFig.12.1.ThemeansoftheactualparentsoftheF1hybridsareconnectedbyasolidline;themeansofthetotalbreedsamplebyadashedline.
butuponphysicalvigoraswell.Figure12.2canbeinterpretedasillustratinganeffectofphysicalvigorsuperimposeduponageneticsystemcontrollingtherelativestrengthofpositiveandnegativereinforcementinthetestsituation.
DIFFERENTIALCAPACITIES
Wemadeadditionalanalysesoftheseparatehybridmatingsinanefforttoestimatethequantitativecontributionofhereditytotherunning-speedmeasure.Themidparent-offspringcorrelationwas.34±.20.Wemighttakethisasanestimateofheritability,buttheerrorofestimateisveryhigh.Analysisofvarianceofthegroupsinwhichonesirewasmatedtotwodams,oronedamtotwosires,showedconsiderableconsistency.Innoinstanceweretheresignificantdifferencesbetweenlittersofthesamemating,indicatingthatrearingandtestingconditionswerewellcontrolledoverthecourseoftheobservations.Ontheotherhand,individualmatingsdifferedsignificantlyatthe.01levelineachofthefoursetsofdataandintraclasscorrelationsof.15,.41,.24,and.24werecomputed.Allthesecomputationsagreeinsuggestingthatsomethingbetween20and30percentofthevariationinrunningspeedisheritable.Thiscompareswithanestimateof16percentbasedontheparentbreedsalone(seeTable14.3).
DISCRIMINATIONORCUERESPONSE
ThemotivationtestontheT-mazewasusedaspre-trainingfordiscriminationin
ThemotivationtestontheT-mazewasusedaspre-trainingfordiscriminationinadditiontobeingameasureinitsownright.Subjectswhichdidnotreachthecriterionwithin128trials(8dayswith16trials)wereclassifiedasfailures.InFigure12.3wepresenttheperformanceofthebasenji-cockerspanielhybridswithrespectto
DISCRIMINATIONCRITERIONATTAINMENT
FAILED
B.BCSB.B(23)(44
Fig.12.3.—Attainmentbyhybridsofcriterioninthecue-response(discrimination)test.Failureisdefinedasnotmeetingcriterionwithin128trials.
COMPLEXBEHAVIOR
309
attainmentofcriterionwithin128trials.Byusingasimplepass-faildichotomy,wefoundthedatayieldax2of25.532(F<.001).Therankingofthesixgroupsisorderlyexceptforthepurebredbasenjiswhichseemtobebetterthantheyshouldbeconsideringthatthebasenjibackcrossesweresoslowinlearning.Whenweconsiderthescoresofthespecificparents,wefindapossibleexplanation.Unfortunately,onlyfourofthesevenbasenjiparentspassedthroughthetestingprogramafterthediscriminationprocedurewasstandardized,andonlythreeofthefourmetthecriterion.Itisalmostcertainthatthebasenjisselectedasbreederswereaninferiorsampleofthebreed(forthistest).Thuswefeelsafeinconcludingfromtheorderingofgroupmeansthathereditymakesasubstantialcontributiontosuccessfuldiscriminationlearning.Theconclusionissubstantiatedbyananalysisofvarianceinthosehybridmatingswhichproduced
substantiatedbyananalysisofvarianceinthosehybridmatingswhichproducedtwoormorelitters.Ratherthanusetheattainmentofacriterionasameasureofsuccess,whichwouldhaveforcedtheexclusionoffailures,weusedthenumberofcorrectresponsesinthefirst64trials.Table12.9demonstratesthatthevariationsbetweenmatingsweresignificant(P<.05),andthatlittersofthe
TABLE12.9
DiscriminationorCueResponse—AnalysisofVarianceofHybridPerformance
P<.05P<.01
sameparentagecouldalsodiffertoaconsiderabledegree(P<.01).Eventhoughconditionsspecifictolittersareimportant,theeffectsofhereditaryfactorsshowthrough.Wehavenot,however,attemptedtoestimateheritabilityofthismeasurebecauseofourreservationsconcerningitsprecision.
DELAYEDRESPONSE
Subjectsmeetingthediscriminationcriterionweretestedondelayedresponsefollowingaseriesof50post-criteriondiscriminationtrials.Thesampleisobviouslynotrepresentativesinceinsome
DIFFERENTIALCAPACITIES
groupsupto50percentoftheindividualsneverqualifiedforde-layed-responsetesting.Nevertheless,thefindingsareofsomeinterestandhavebeenillustratedinFigure12.4.Theproportionofindividualsmeetingthecriterionatdelaysof5secondsormorefluctuatesunsystematically,buttheproportionsmeetingthecriterionataminimumdelay(1second)appearfairlysimilar,animpressionwhichisconfirmedbyanon-significantvalue(x2of8.263,5degreesoffreedom,P<.10).
DELAYEDRESPONSEPERFORMANCEOFHYBRIDS100
Fig.12.4.—Attainmentbyhybridsofcriterionindelayedresponse.Failureisdefinedasnotmeetingcriterionat1-seconddelaywithin40trials.Blackportionofcolumnsindicatespercentageoffailures(definedasnotmeetingcriterionat1-seconddelaywithin40trials;barredareadenotespercentagepassingat1-seconddelay;whiteportionshowsthepercentageattainingcriterionat5-secondsorlongerdelay.
Thesedataprovidenoevidenceforgeneticdeterminantsofshort-termmemory,butthevariationsbetweenindividualswerestriking.Themaximumdelaysatwhichcriterionwasmetbyanyonesubjectwere:basenji,15seconds;CSBXB,5seconds;Fi,30seconds;F2,30seconds;BCSXCS,15seconds;andcocker,240seconds.Individualvariationmayhaveahereditarybasiswhichcouldbeinvestigatedbyselectingbothforgoodandpoordelaved-responseper-Formance.Onecouldretainforthelow-linethoseindividualswhichlearnedthecuediscriminationadequately,butfailedwhendelaywasintroduced.Onlybysuchaprocedurecanthehigherorderabilitybedisentangledfromsimplediscriminationlearning.
COMPLEXBEHAVIOR
311
OBEDIENCETEST
Theobediencetestwasinterpretedasameasureofeaseofinhibitorytrainingonthebasisofthecomparisonbetweenthefivepurebreeds.Sincethecockerspanielsandbasenjisdifferedsharplyonthetest,onemightanticipatethatthehybridswouldbeintermediate.TheexpectationisverifiedinFigure12.5,whichshowsthe
Fig.12.5.—Meanscoresofhybridsonobedience.Highscoresindicategreaterinhibitionofmovement.PointsidentifiedasinFigure12.1.
meanscoresofparentalandhybridgroupsincludingthevaluesforthebasenjisandspanielsselectedasparentsofthehybrids.Thedataarenotperfectlyorderly,butthetrendisclear.Themoredetailedanalyses,unfortunately,arelessinformativethantheywerefortheleash-trainingtest.Theoffspringonmidparentregressionisonly.16,notreliablygreaterthanzero.Analysisofvariancefailedtouncoveraconsistentdifferencebetweenmatings,andsuccessivelittersofthesameparentagewereoftenasdifferentastwomatings.Despitethefavorablemeandifferencebetweenthebreedsandtheapparentorderlinessofthegroupmeans,weendedwitharatherunsatisfactoryoutcomeofthegeneticanalysis.Intuitivelythetestseemedtobeasgoodacandidateforhighheritabilityastheleash-fightingscore,butintuitionprovedapoorguide.
DIFFERENTIALCAPACITIES
REACTIVITYTEST
Asdescribedinchapter8,subjectsinthereactivitytestwererestrainedbylooselyfittingloopswhiletheywerestimulatedinsequencebytheentranceofanexperimenter,bythesoundofabell,andbyfourmildshocksappliedtothehindleg.Measuresincludedratingsofpostureandvariouscategoriesofbehavior,andcontinuouslyrecordedrespiration,electrocardiograms,andelectromyo-grams.Twenty-threemeasureswereselectedfordetailedanalyses,andtheresultsonthefivepurebreedshavealreadybeenpresented.
Inadditiontothesepartscores,thetotalreactivityscoreobtainedbysumming
Inadditiontothesepartscores,thetotalreactivityscoreobtainedbysummingalloftheovert-behaviorratingsisusefulasageneralbasisofcomparison.Ahightotalreactivityscoreindicatesagen-
U6
z
<
»-4I/)
TOTALREACTIVITYSCORE17Weeks
Fig.126.—Moantotalreactivityscoresofhybridsat17weeks(upper)34weeks*middle),and51weeks(lower).
COMPLEXBEHAVIOR313
erallvactiveanimal.Basenjisweresignificantlyhigheronthismeasure(meanstaninesbetween5.5and6.0)thancockerspaniels(meanstaninesbetween3.5and4.0).ThemeantotalscoresofthehybridgroupsareshowninFigure12.6.Oneinterestingfeatureofthisfigureisthechangeassociatedwithmaturity.At17weeksofage,allthehybridsareasreactiveasthebasenji;by51weeksthemeansapproachtheexpectationbasedonadditiveinheritance.TheCSBFi'sappeartobetoohigh,butthismaywellbeasamplingphenomenon.Unfortunately,thereactivityscoringsystemhadnotbeenstandardizedwhensomeoftheparentsweresubjectsintheprogram,sothatitisimpossibletoknowwhethertheparentsofthetwoFi'swereequalinreactivityscores.
Thedetailedanalysisofgroupmeansontheseparatemeasuresatthreeagesdid
Thedetailedanalysisofgroupmeansontheseparatemeasuresatthreeagesdidnotaddgreatlytotheinformationobtainedfromthetotalscorecomparison.Onthosesubscoresinwhichbasenjisandspanielsweredefinitelyunlike,thehybridstendedtobeintermediate.Inparticular,themeansofthebackcrossesandFi>'susuallyfellclosetoalinedrawnbetweentheparentmeansasinFigure12.6;theFimeansvariedmorewidelyfromtheexpectationbasedonadditiveinheritanceanduniformenvironment.Onsomescorestheparentstocksdifferedinsignificantlyandthepatternsofthehybridmeanswereirregular.AsillustrationsweshowinFigure12.7themeansforfourofthesubscoresfromthe34-weektest.Thegroupmeansforthephysiologicalmeasure(basalheartrate)fallclosetotheexpectationbasedonadditiveeffectsofgenes.Theactualmeansinbeatsperminutewere:basenji,138;basenjiback-cross,134;Fi,117;F2,114;spanielbackcross,109;andcockerspaniel,102.Similarresultsfortheheartrateofyoungpuppieswerereportedinthepreviouschapter.
Thedataforbodypositiondidnotfallasneatlyinlinewithexpectations,butallhybridmeanswereintermediatebetweenthespaniels,whoselowscoreindicatestheprevalenceofcrouching,andthebasenjiswhichalmostalwaysstooderect.
Thedistributionofbitingandtail-waggingscoreswerediscontinuoussothatstaninetransformationswerenotfeasible.Seventy-eightpercentofthebasenjisbitattheirrestrainingloops,butonly10percentofthecockersdid.Thepercentagesofbitersinthehybridgroupsformanorderlyarray,althoughthespanielback-crossesareasnon-aggressiveasthepurebredspaniels.Thedichoto-mousclassificationforgraphicpurposesintobitersandnon-bitersobscuresthefactthatthe7to10percentofcockersandcockerbackcrossesthatwereratedasbiterswereonlymarginallyso.
DIFFERENTIALCAPACITIES
Bitingisanillustrationofbehaviorwhichdoesnotappearuntilathresholdofstimulationisreached.Givenastandardstimulus,populationsdifferintheproportionwhichshowanyresponse.Oncearesponseiselicited,itcanbeexpressedinquantitativeterms.Suchcombinationsofcontinuousanddiscontinuousvariationarenotconvenientforgeneticanalysis.FormalanalysiscanbedonewithWright's(1934)thresholdmodel(seeFuller,Easier,andSmith,1950,foranapplicationofthismodeltoseizuresusceptibilityinthe
BACSB.BFt)FzBCS.CSCS
BACSB.BF,,F2BCS.CSCS
Fig.12.7.—Ontheleft:meanscoresofhybridsontworeactivity-testmeasures.ThetwoFjandF2populationswerepooled.Ontheright:theproportionofeachhybridgroupscoresas"high"ontworeactivitytestmeasures.Straightlinesbetweenparentalmeansindicatelocationofhybridmeansifinheritancewereadditive.AdditionallinesconnectparentalmeanswiththeF1tovisualize"dominancedeviation."
mouse),butitisnotusefultocarryoutsuchproceduresonsmallsamplesfromnon-inbredparentstocks.Wecansafelyconcludethatgenotypeaffectstheprobabilityofelicitingbitingundermildrestraint;but,beyondassertingtheprobableapplicabilityofathresholdmodel,wesuggestnospecificmodeofinheritance.
ThefinalpartscoreillustratedinFigure12.7isfortailwaggingandisdistributeddiscontinuouslylikebiting.Theproportionsofthetwoparentstockssurpassingthethresholdofstimulationarenotgreatlydifferent,andthehybridgroupscoresarelikewisesimilar
COMPLEXBEHAVIOR
315
toeachother,withmeansdifferinginsignificantlyfromthatofthecockerspaniels.Theincidenceoftailwaggingchangedmarkedlyoverthethreetests.Figure12.8demonstratesthatthegeneralrelationshipbetweenthegenetic
Figure12.8demonstratesthatthegeneralrelationshipbetweenthegeneticgroupsremainsroughlythesame,althoughtheproportionsshowingthebehavioraredecreasing.
100
CSB-B
F,,F2BCSCS
Fig.12.8.—Proportionofeachhybridgroupratedas"high"intailwaggingat17weeks(opencircles),34weeks(half-filledcircles),and51weeks(solidcircles).
Changesassociatedwithagingappeartoactuniformlyoverthevarietyofthegenotypestested.Ingeneral,thedifferencesbetweentheparentbreedsarenotaspronouncedasearlierindevelopment(seechap.4).
Itisnotcoincidencethatmostofthepartscoresinthehybridsfollowthegeneraltrendofthetotalscores.Theratingsystemwasdevisedtoyieldhighnumericalscoresforthedogwhichfoughtagainstrestraintandwhichrespondedactivelytoeachnewsetofstimuli.Lowscoreswereassignedforinactivityandabsenceofphysicalevidenceofarousal.Thefactthatthemeansforthetotalscoresfallinanorderlysequenceinthehybridsmaysignifythatsomecommondimensionofarousalvs.inhibitionismanifestedin
316DIFFERENTIALCAPACITIES
avarietyofways.Theprecisemannerinwhicharousalisexpressedinthereactivitysettingmaynotbeasimportantasthelevelofactivationattained.
TABLE12.10Variance—TotalReactivityScoresofHybrids
Furtherinformationonthecontributionofhereditytothereactivityscorewasobtainedbvananalysisofthehybriddatabymatings.Thegeneralformofthisprocedurehasbeendescribedabove.ReactivityscoresforthethreetestsweresummedforthisanalyLittersofamatingdifferedinsignificantlyfromoneanother—evidencethattheeffortstomaintainconstantrearincrandtesting;con-ditionsoverthecourseoftheexperimentweresuccessful.Variationattributabletomatingswashighlysignificantineachofthefoursub-experimentsintowhichwehavegroupedthedata.ThesummaryanalysisofTable12.10wasmadewithoutrespecttogeneticclassificationandincludesdatafrom21hvbridmatingswhichproduced37litters.Theintraclasscorrelationof.736isoneofthehighestfoundonanyofthetests,muchhigherinfactthanwasfoundinthepure-breedcomparisons.Itshouldbeemphasizedthatthishighvaluecomesfromtheclassificationofoffspringbyindividualparentageandnotbvthebreedclassificationoftheparents.Althoughreactivityisheritable,differentindividualsfromtheparentstrainspassonquitedifferentgeneticdeterminantstotheiroffspring.
Hadthisbeenforeseen,wemighthaveelectedtodisregardbreedboundariesinplanningmatingsandworkedentirelywithparent-offspring,sibling,andhalf-siblingcorrelations.TheheterogeneityinphenotypeofmatingsofthesametypeisillustratedforthereactivityscoreinTables12.11and12.12.Differencesbetweenmatingsofthesametvpeweresignificantintheseexperiments:CSBfXB9orCSBi(P<.01;HA2XCS6orCSBJ(F<.01;andCSe•HA!orBCSP<.05).Thenumberofdifferentmatingsistoosmalltopermitanyconclusionsontherelativecon-
COMPLEXBEHAVIOR
317
TABLE12.11
TotalReactivityRatings(Sumof3Tests):MeansofMatingsofPurebredDamsbyPurebredandFiSires
tributionsofdamandsire,butthedataareconsistentwithequalcontributions
tributionsofdamandsire,butthedataareconsistentwithequalcontributionsfrombothparents.ThedifferencebetweenreciprocalFi'scouldbeinterpretedasanexampleofmaternalinfluence,butitisequallylikelytobeanexampleofsamplingvariation.
Thesedataagainconfirmtheconclusionthatthebreedsstudied,thoughselectedinpartforbehavioralcharacteristics,arestillheterogeneous.Selection,ofcourse,hassucceededinmakingbreedssignificantlydifferentontheaverage,aswefoundinourbreedcomparisons.
TABLE12.12MatingsofFiSiresbyPurebredandFxDams
318DIFFERENTIALCAPACITIES
LJ
<X00
BACSB-B
FiF2
BCS-CSCS
Fig.12.9.—Meancorrectchoicesscoresofhybridsonthespatial-orientationtest.LinesdrawnasinFigure12.7.
SPATIAL.ORIENTATIONTEST
Aswithdiscriminationanddelayedresponseitwasnecessaryinthespatial-orientationtestforsubjectstomeetaspecifiedcriterionduringpre-traininginordertoobtainmeaningfulmeasuresonthestandardprocedure.Sincesomedogsfailedtomeetthecriterion,thecomparisonsbetweengeneticgroupswerebaseduponselectivesampling.Thetotalnumberofsubjectsenteringtrainingforeachgroupfollows,withthenumberfailingtomeetthecriterionforthetestgiveninparentheses:basenji,28(4);CSBXBA,43(4);BAXCS,24(0);CSB,28(1);BCSXBCS,32(1);CSBXCSB,41(4);BCSXCS,27(1);andcockerspaniel,28(2).
ThemeansinstaninesofthegroupsforthethreemeasuresareshowninFigures12.9to12.11.Thecockerspanielsweredefinitelysuperiortobasenjisin
12.9to12.11.Thecockerspanielsweredefinitelysuperiortobasenjisineliminatingerrors.Allofthehybridgroupsweresuperiorontheaveragetothebetterparent.ThepersistencescoresfellintoasimilarpatternexceptfortheFi'swhichwereintermediatetotheparents.Allhybridgroupsweresimilartothecockerspanielsontheadjustedspeedmeasure.Althoughthispatternofdistributionofthemeansdoesnotappearfavorableforaquantitativeanalysis,wesubjectedthecorrect-choicescorestoan
COMPLEXBEHAVIOR
319
7.0
6.0-
QJ
2
5.0-
4.0-
3.0
BACSB.BF,,F2BCS-CSCS
Fig.12.10.—Meanpersistencescoresofhybridsonthespatial-orientationtest.LinesdrawnasinFigure12.7.
analysisofvariancetodeterminedifferencesbetweenmatingsandbetweenrepeatedlittersfromthesamemating.Itwasnotsurprisingtofindnosignificanteffectofmatingssincethegroupmeansweresomuchalike.However,thedifferencesbetweenlittersofthesamematingweresignificantinthreeofthefourseparateanalyses.
Weconcludethatsomethinginthetestsituationorinthegrouplifehistoryexertedapowerfuleffectuponperformanceinthespatial-orientationtestwhichoverrodeanyinheritedvariationsinlearningability.Sincelittereffectswerenotdetectedinothermeasuresinwhichtheyweresought,itisprobablethattheeffectinthespatial-orientationtestarosefromsomefactorpeculiartothattest.
effectinthespatial-orientationtestarosefromsomefactorpeculiartothattest.Theapparatus,becauseofitslargesize,wassetupintheanimals'homepenssothatconditionsoftestingvariedfromlittertolitter.Theconsequencesofbadweather,disturbancesfromadjacentpens,etc.maybemanifestedintheanalysis.
Despitetheinappropriatenessofthedataforquantitativegeneticanalysis,webelievethatthesuperiorityofthehybridsoverthebasenjiparentsisarealgeneticeffect.Thebasenjisasagroupwerestereotypedintheirresponses,tendingtorepeaterrors.Theyalsowereeasilydistractedbyextraneousstimuliwhichincreasedtheirerrors.When25,50,or75percentofthegenotypewasofcocker
DIFFERENTIALCAPACITIES
7.0
CSB-BFt1f2BCSCS
Fig.12.11.—Meanadjustedspeedscoresofhybridsonthespatial-orientationtest.LinesdrawnasinFigure12.7.
spanielorigin,theimprovementwasnotable,althoughnotcorrelatedquantitativelywiththeproportionofspanielgenes.Againitseemedthatwhenathresholdoftimiditywassurpassed,learningwasreasonablyadequateinallsubjects.Tobesure,individualdifferenceswereconspicuousandthesemaydependuponsomeheritablecognitiveability.Themajorgroupdifferencesinsolvingthespatial-orientationproblem,however,seemtoberootedinemotionalreactivitytothetestprocedure(seediscussionof"fearofapparatusfactor,"
reactivitytothetestprocedure(seediscussionof"fearofapparatusfactor,"chapter14).
Insummary,methodsofanalysiswhichdonotdependupontheassumptionofgenetichomozygosity,confirmtheimportanceofhereditaryeffectsupontheoccurrenceofsimplepatternsofbehaviorsuchasleashfightingandemotionalreactivity.Theydonot,however,assistgreatlyintheanalysisofgenetictransmissionofthecomplexadaptivebehaviorinvolvedinproblemsolving.Importantbreeddifferencesinproblemsolvingexist,butthecomplexityofinteractionbetweenthebasiccapacitiesinvolved,bothonthephysi-ologicalandbehaviorallevels,issogreatthatthesemethodscannotcopewithit.
Hereditaryeffectsuponbehaviorrelatedtoeaseofemotionalarousal,specificemotionalresponses,andlevelofmotivationwereclearlvdemonstratedbvthehybridizationexperiment.Ontheotherhand,thecapacitiesforvarioussortsofproblem-solvingbehaviorwerenottransmittedinasimplemanner,andevidenceforheritabilitywasoftenweakorentirelylacking.Itmaybethatlearningabilitvisnotheritable,andthatthestrikingindividualvariationsobservedwerereflectionsofdifferentialexperience.Thisseemsunlikely,however,inviewofthestrongevidenceofheritability,basedonbreeddifferences.Wearereservingfinaljudgmentonthismatteruntilselectionexperimentsareperformedusingproblemsolvingasthecriterion.Atpresent,wecandefinitelystatethatpuppiesresembletheirparentsmorein"personality"thaninintelligence,perhapsbecauseprimarygeneproductshavemoredirecteffectsuponpersonality.
AGENERALINTERPRETATION
Theresultsofthehybridizationexperimentareatthesametimeilluminatingandperplexing.ThetendencyoftheFiandF2hybridstoreceivescoresintermediatetotheparents,andforthebackcrossestobeintermediatebetweentheFiandtheotherparentwasverystrong.Incontrasttotestscitedinthelastchapter,noevidenceofsegregationintodistinctphenotypicclasseswasfoundineithertheF2'sorthebackcrosses,aresultconsistentwiththeinterpretationthatthespanielsandbasenjisdifferedatmultipleloci,eachofwhichaffectedthecharacterstudied.Furthermore,thewithin-littervariancesoftheF2andbackcrosseswerenotalwaysgreaterthanthoseoftheFiandparents.Suchafindingsometimeshascausedconsternation,butthereappeartobethreegoodexplanationsofwhyweshouldnotexpectthevariancesofthesegregatinggenerationstobelargerthanthatoftheparentsandFi.First,thereisampleevidencethatthebasenjisandcockerspanielswereheterozygousatmanyloci
evidencethatthebasenjisandcockerspanielswereheterozygousatmanylociwhichaffectbehaviorsothattheassumptionofnegligiblegeneticvariationinthesepopulationsisunwarranted.Second,ifmanylociareinvolved,theproportionofextremegenotypesproducedinthesegregatinggenerationswillbelowandtheresultingincreaseinvariancewillbeindistinguishablefromsamplingerrorinasmallpopulation.Third,theheritabilityofmanycharactersislowenoughsothatasmallincreaseingeneticvarianceisindistinguishablefromsamplingvarianceexceptinlargepopulationsinvolvingmanymatings.
322DIFFERENTIALCAPACITIES
Assuggestedabove,thefindingsindicatethatadifferentexperimentaldesigninvolvingalargernumberofmatingsfromawiderselectionofbreedswouldhaveprovidedmorepreciseknowledgeconcerningthegeneticstructureofdogpopulations.Butsuchaplanwouldnothavesuppliedasmuchinformationonthecrossingofphenotypicallydistinctbreedswhichhadbeengeneticallyseparatedformillenniums.Thespanielswere,ingeneral,superiorperformersonthosetasksinwhichtheterms"superior"and"inferior"areatallappropriate.Inthetrainingprocedures,spanielsweremorereadilyinhibited,whichmaybedesirableorundesirabledependinguponcircumstances.Onmanyperformancetests,thehybridswereequaltoorsuperiortotheparentthatwasthemoreactiveorthebetterlearner.Webelievethatadual-processhypothesiswillaccountforsuchfindings.Inthespatial-orientationtest,themorereactivebasenjisarestronglystimulatedbysmallvariationsintheenvironment,andthesevariationsinterferewithsuchtasksasdiscriminationandthelearningofacorrectpath.Inthesesametestssomecockerspanielsshowlittledistractionandalsolowspontaneousactivityresultinginrelativelypoorperformance.Thehybridsofalldegreesappeartobehighlyarousedlikethebasenji,andnon-distractablelikethecocker,sothatperformanceisfrequentlysuperiorontheaveragetoeitherparent.
Thecharacteristicsofthetwoparentalstocksarereasonablyaccountedforbypastselection.Basenjis,livinginvillagesintheAfricanjungles,aregivenrelativelylittleprotection.Suchcircumstancesplaceapremiumonawarenessofminorchangesintheenvironmentandexcessivecautiontowardastrangeobjectorindividual.Cockerspaniels,ontheotherhand,haveledahighlvprotectedexistenceasEnglishhuntingdogsandashousepets.Theywereselectedoriginallyonthebasisofgreatactivityinhuntingbuteaseofinhibitionofattackongame.Thoughsuchselectionhasbeenrelaxedinmanystrains,thepopularityofthespanielasahousepetisbasedinpartuponitsreputationfordocility.
Determinationofdominancerelationshipsbetweenthegeneticsystemsresponsibleforthesephenotvpes(shynessvs.inhibition)couldbemadeonlyifagreementcouldbereachedonthescaleforphenotypicmeasurement.Ourdataindicatethattheshynessofthebasenjimaybedependentuponarelativelysmallnumberofgeneswithgenerallyadditiveeffects,andthatasimilarsysteminvolvingdifferentgenesisassociatedwiththeinhibitabilityofthecockerspaniel.Suchdualsystemscouldexplainthefactthatonsomemeasuresthebackcrossesweremorebasenji-likeormorecocker-likethan
COMPLEXBEHAVIOR323
thepurebredstocks.Abasenjibackcrosshomozygousornearlysoforshynessandalsohomozygousornearlysoforinhibitionwouldperformlesswellperhapsthanapurebredbasenjiwhichwaslessinhabitable.
Weshouldstressthatthebasenji-cockerspanielhybridswerephysicallyandbehaviorallyexcellentanimals.ThepointisimportantbecauseStockard's(1941)statementsregardingdisharmoniesintheF2ofinterbreedcrosseshavebeencitedasevidencefordangersinherentinracialcrossesinman(George,1962).Stockard,ofcourse,startedwithbizarretypesofdogssuchassalukis,dachshunds,andbulldogs,whichhaveachievedaratherperilousgeneticadjustmentastheresultoflongperiodsofselection.Itisnotsurprisingthatjaws,limbs,andbodiesoftheF2'sdidnotfittogetherverywell,althoughtoanaiveMartianseeingdogsforthefirsttime,theFs'smightappearnomorestrangethanapurebredbulldogoradachshund.Asthephotographsshow,ourbackcrossandF2groupsincludedindividualswhichconformedtononeofthet\pesrecognizedaspurebreeds,butwhichwerenonethelesshealthy,vigorous,andwelladjusted.
GOALSFORBIOMETRICALGENETICSOFBEHAVIOR
Thisisperhapsasuitableplacetorecordourchangeofattitudetowardourexperimentsaswegathereddataandsubjectedthemtoquantitativeanalysis.Atthebeginningofthehybridizationexperimentwewerelookingforgeneticmechanismstocorrespondwithhypotheticaltraits.Asdataaccumulated,itbecameclearthatcorrelationsbetweendifferenttestsgivenatdifferenttimesandplaceswerelow—inotherwords,wefoundlittleevidenceforpervasivetraitsaffectingallaspectsofbehavior.Tobesure,thefactor-analysesofRoyce(1955)andBrace(1961)uncoveredmanysignificantcorrelations,butthesewerehighestbetweenmeasurescollectedinthesametestsituation.Overtheperiodof
highestbetweenmeasurescollectedinthesametestsituation.Overtheperiodoflifewithwhichwewereconcerned,traitstructurewassomewhatfluid,andgenetichypothesesregardingheritabilitywereconsequentlyspecifictoaparticularageandtypeofmeasurement.Attemptstosecuregreaterprecisionbysubstitutingfactorscoresbasedonacombinationoforiginalscoreswerenotsuccessful.Wesomewhatregretfullycametotheconclusionthatclassicalbiometricalmodelsarenothighlyapplicabletotheinheritanceofcomplexbehaviorinsemi-naturalpopulations(casuallyselectedforbehaviorandnotsystematicallyinbred).Ifwecantransfertothedogthefindinginmicethatmuch
324DIFFERENTIALCAPACITIES
ofthegeneticvariationamonghybridsisattributabletointerlocusinteractions(Fuller,1964),wewouldexpectrelativelylowparent-offspringcorrelations.Untilbettermethodsaredevised,formalbio-metricanalysiswillbemostfruitfulinspeciesinwhichnumerousinbredlinesexist,andinwhichlargenumberscanbebredatlowercost.Insuchsituationsthebehavioralphenotypecanberigorously(andnarrowly)specified,andthesuccessofthebiometricalapproachhasbeenamplydemonstrated(FullerandThompson,1960;Broadhurst,1960;Bruell,1962;HirschandErlenmeyer-Kimling,1962).
BroadhurstandJinks(1961)haveattemptedthebroaderapplicationofelaboratemethodsdevelopedfortheanalysisoftheeffectsofgeneticsoncontinuousquantitativevariationinbehavior,basedonthetechniquesofMather(1949).Withthesemethodsitispossibletoestimatetheamountofvariationduetodominance,additiveeffectsofgenes,andinteractionbetweenthem,aswellasthatduetoenvironmentalfactors.Usingasetofincompletedatafromoneofourproblem-solvingtests(Scott,1954),theyarrivedatanestimateofheritabilityapproximatelytwiceaslargeasthatobtainedbyusandbasedonbreeddifferencesalone.Suchmethodsgiveushopethatthequantitativeeffectsofheredityonbehaviorcanbeanalyzedmoreexactlyinthefuture.Becausethesemethodsdependuponempiricalscalingofeachindividualtestandhencebecomeextremelylaboriouswhenappliedtolargebodiesofdata,theyhavenotbeenappliedhere,althoughitwouldobviouslybefruitfultousethemoncertainsetsofthesedataandtocomparetheresultswiththoseobtainedbyothermethods.
Cantheresultsobtainedinspecializedlaboratorypopulationsbeappliedtolarger,moreheterogeneousgroupssuchasdogbreedsormankind?Inparticular,weaddressourselvestotheinterpretationofheritabilities.Heredity,inthebroad
weaddressourselvestotheinterpretationofheritabilities.Heredity,inthebroadsense,isusuallyassumedtoexplaindifferencesbetweenspecies.Occasionalinterspeciescrossesareavailablefortestinggenetichypotheses,butsuchresultscanhavelittleapplicationtonaturalspecieswhicharedefinedasindividualssharingacommongenepool.Thevariationsinbehaviorbetweenracesorbreedsofthesamespeciesare,parentalinfluencesaside,primarilygenetic,butthesearereflectionsofinterallelicinteractions(epistasis)aswellasofadditiveeffectsofgenes.
Oneshouldbecautiousinapplyingquantitativefiguresforheritabilityoutsideofthespecificcontextinwhichtheywereobtained.Wequestionwhether,oncesomegeneticcontrolofacharacterhasbeendemonstrated,preciseestimationsofheritabilityhaveany
COMPLEXBEHAVIOR325
greatvalueexceptforselectionprogramswithpracticalobjectives.Hereestimatesofheritabilitvforthecriterioncharacterobtainedunderconditionspeculiartotheselectionprojecthaveobvioussignificance.
Tous,itappearsthataspecieslikethedogismostusefulinbehaviorgeneticsforstudiesofgenotype-life-historyinteractions.Suchinteractionsneednotbestatisticalabstractionsfromanalysisofvariancetables,butcanbeexpressedinfunctionaltermsbaseduponobservationandmeasurementofbehavioratvariousstagesindevelopment.Forthispurpose,agroupofpurebredstrainsofdivergentphenotvpes(excludingmonstrosities)canbeextremelyuseful.
Resultsfromsuchstudiescanbeorganizedintheformofamatrixwithvaryingnumbersofrows(ofbreeds)andcolumns(ofenvironments).Suchamatrixisgeneratedbyanyexperimentcomparingtwoormorebreedsintwoormoreenvironments.
Ourbreedcomparisonstudyinoneuniformenvironmentformedamatrixwithonecolumnandelevenrows.Forcomparativepurposesinfutureinvestigations,werecommendtheadditionofanadditionalrowintheformofa4-waycross,FiXFi,witheachF,derivedfromadifferentpairofbreeds.Insuchapopulationoneobtainsvariablegenotypeswhichfacilitatecorrelationalanalysis.Furthermore,suchageneticallydiversepopulationcanbeusedasacontrolforthegeneralityoffindingswiththepurebreeds.
Forthefuturewealsorecommendadditionalcolumnsofenvironmental
Forthefuturewealsorecommendadditionalcolumnsofenvironmentaltreatmentswhichwillenabletestingofthevalidityofvarioustheoriesconcerningtheeffectofearlyexperienceandtrainingupondifferentgenotypes.Thestandardizedenvironmentgivenourpuppieswasrestrictedinmanyways,anddifferentkindsoftreatmentsmightwellresultinthedevelopmentofcapacitieshiddeninthisexperiment.
DEVELOPMENTOFPHYSICALDIFFERENCESANDTHEIRRELATIONTOBEHAVIOR
NTRODUCTION
Inpreviouschapterswehavebeenconcernedalmostentirelywiththedevelopmentofbehaviorandtheevidencethatgeneticsproducesbehavioraldifferentiationandvariation.Thischapterisconcernedwithoneaspectofthegeneralproblemofhowgeneticsaffectsbehavior:theeffectsofdifferencesinphysique.Thisisanimportantpracticalproblem,foriftherewereaperfectcorrelationbetweenphysiqueandbehavior,thetaskofthebehaviorgeneticistwouldbeenormouslysimplified.Itisalsoaninterestingtheoreticalissue,involvingboththeconceptofpleiotropy,ormanifoldeffectsofthegene,andtheapplicationofthecontrastingconceptsoftypeandpopulationtotheanalysisofvariation.
Physiqueistheresultofgrowth,aprocesswhichhasonlvanindirectrelationshiptobehavior.Somedifferencesinbehaviorcanbeseenonlywhenphysicalgrowthliasreadiedacertainpoint,anddifferencesinsizemayhaveimportanteffectsoncertainmotorcapacities.However,thedevelopmentofsizeandotherphysicalcharacteristicscanserveasamodelfortheactionofheredity,partlybecauseitismuchclosertothephysiologicaleffectsofgenes,andpartlybecauseweknowsomuchmoreabouttheinheritanceofsizedifferences.
PATTERNSOFGROWTHINTHEDOG
Growthinrelationtoperiodsofbehaviordevelopment.—Forthefirst3weeksofitslife,apuppynormallyreceivesallitsnourishment
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327
bynursingfromitsmother.Themilksupplydoesnotincreaseasthepuppvgrowsolder,butreachesthelimitofthemother'scapacityafewdavsafterbirth.Thegeneralgrowthpatternreflectsthislimitation,andtheneonatalpuppygainsthemaximumamountinthesecondweekandslightlylessinthethird(Fig.13.1).
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Fig.13.1.—Absoluteweightgainperweekinmalepuppiesofthelargestand
Fig.13.1.—Absoluteweightgainperweekinmalepuppiesofthelargestandsmallestbreeds(beaglesandterriers).Notethatthismeasureismuchmoresensitiveandvariablethancumulativeweightcurves.
At3weeksofage,thepuppiesbegintotakesupplementalfood.Underourspecialconditionsofrearing,theynowhaveaccesstoanunlimitedfoodsupply,andthisisreflectedintheirgrowthrates.From3to7weeksofage,thereisanincreaseintheamountgainedperweek,thechangetakingplacegraduallyorsuddenlydependingonhowquicklytheindividualpuppyorbreedbecomesadjustedtosolidfood.Thereisatemporarysetbackatthetimeoffinalweaning,butforseveralweeksthereafterthepuppiesgainaconstantamounteachweek(abouthalfakilograminanaveragemalebeagle).Thedipat16weeksinFigure13.1isprobablycausedbyreactiontodistempershotsinsomeanimals,asCorbinetal.(1962),reportaconstantincrementupto18weeksofage.
Thesefactsarereflectedinconventionalgrowthcurves.There
DIFFERENTIALCAPACITIES
appeartobeupperlimitsfortheamountsofeitherliquidorsolidfoodwhichapuppycanprocess,sothatweightgaincurvesareflatupto3weeksofageandagainfrom7weeksonward(Fig.13.1).Sinceweightgainisnotproportionaltosize,percentagecurvesdeclinethroughoutdevelopment.Thecumulativeweightcurveupto16weeks,thoughsuperficiallysimilartoatheoreticalexponentialgrowthcurve,isactuallycomposedoftwostraightlinesconnectedbyacurvedportionreflectingincreasingintakeofsolidfoodbetween3and7weeks(Fig.13.2).
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Fig.13.2.—Combinedgrowthcurveforbasenjimales.Notehowvariationincreasesastheanimalsbecomelarger.
Forourpuppiestherewasasecondchangeindietat16weeks,whentheywereputoutdoorsandnolongergivensupplementsofmilkandfinch'powdereddryfoods.Mostofthebreedsshowedalessenedrateofgainduringthenexttwoweeks(Fig.13.4),butthismayhavereflectedthefactthattheywerenolongerdrinkingaquarterofakilogramofmilkbeforebeingweighed.
Alter16toISweeks,theincrementsofgrowthgraduallydecline.
PHYSICALDIFFERENCES
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Bythistimethepuppiesaremorethanhalfgrownandbeginningtoapproach
Bythistimethepuppiesaremorethanhalfgrownandbeginningtoapproachadultcapabilities,althoughtheyarejustbeginningtogettheirpermanentteethandwouldnotundernaturalconditionsbecapableofeffectivehuntingforanothermonthortwo.
Thisgeneralpatternofgrowthisadaptedtothelifeofacarnivore.Apuppygrowsasrapidlyaspossibleuntilhereachesthesizewhichenableshimtobeaneffectivehuntinganimal.Thiscontrastswiththepatternofgrowthinhumanbeings,inwhomaperiodofrapidgrowthinearlyinfancvisfollowedbyaperiodofveryslowandgradualgrowthuptoshortlybeforepuberty,whenanadolescentspurtappears.Thereisnothinglikethehumanadolescentspurtinthedevelopmentofthedog,unlessweconsidertheearlyperiodofrapidgrowthassuch.Itshouldbecalleda"puppyhoodspurt,"ifanything.
Breedandsexdifferences.—Thereisalwayssomeoverlapbetweenindividuals,butineverybreedandatanyagethemalesareontheaveragelargerthanthefemales(Fig.13.3).Bythetimetheyreachoneyear,themalesinbeagles,cockers,andsheltiesarefrom24to28percentheavierthanthefemales.Thedifferencesinterriersandbasenjisismuchless,being12and14percent,respectively.
Thesedifferencesingrowthcurvessuggestthatthefemalesmaybematuringmorerapidlythanthemalesandhenceslowingdowningrowthatanearlierage.However,ifwecomparethepercentagesofadultweightat16weeks(Table13.1),itisobviousthatthefemalesareverylittleaheadoftheirbrothersexceptinthebeagles,wherethefiguresare61percentforfemalesand55percentformales.Inbasenjisthefemalesareslightlybehindthemales.
TABLE13.1PercentageofAdultWeightReachedat16WeeksofAge
Thereisoneoutstandingbreeddifferenceinrateofmaturation:thecockerspanielsasabreedareconsiderablyaheadoftheotherfour,havingalreadygained70to72percentoftheiradultweight.
TheshapeofthecurvesinFigure13.4indicatesthatthedogshavenotquitereachedtheirmaximumweightat52weeksofage.The
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Ik..13.3.—Maleandfemalegrowthcurvesinbasenjis(above)andcockerspaniels[bilow).
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Fig.13.4.—Growthcurvesofthefivepurebreeds.Above,males;below,females.
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332DIFFERENTIALCAPACITIES
situationissomewhatcomplicatedbyestrusinthefemales,sinceanon-pregnant
situationissomewhatcomplicatedbyestrusinthefemales,sinceanon-pregnantfemalemaytemporarilygainweightasasymptomofpseudopregnancy,acommonoccurrenceinunmatedfemales.Thismayaccountfortheapparentdiscrepancyin{hefemalebasenjicurve,sinceallfemalesofthisbreedcomeintoestrusaround10monthsofage.
Differentiationofindividualdifferences.—Whenwecomparetheweightcurvesofmalesandfemales,weseethatthereisverylittledifferenceinsizeatbirth,andthattheybecomemoreandmoreunlikeastheygrowolder.This,however,ismoreamatterofchangeinabsolutethaninrelativesize,forifweanalyzethevariationofeithersexwithinabreed,thestandarddeviation,astatisticalmeasureofvariability,fansoutlikeafunnelastheanimalsgrowolder(Fig.13.2).Theupperandlowerrangesofindividualgrowthspreadoutevenfurther.Initialdifferencesinsizebecomegreaterandgreaterastheanimalsgrow,andindividualsthusbecomeincreasinglydifferentiatedfromeachother.
Canwetakethedifferentiationofgrowthcurvesasamodelforthedifferentiationofbehavioraldifferences?Theansweristhatthemodelfitsinsomewaysbutnotinothers.Theprocessofgrowthhascertainsimilaritiestotheprocessoflearning.Growthisanac-cretionaryprocess,inwhichanimalsbecomelargerbyaddingsmallamountseverydaytothatwhichtheyalreadyhave.Insomerespectslearningislikegrowth,especiallywhensmallbitsofinformationaregraduallyaddedtowhathasbeenlearnedbefore.Forexample,achild'slearningnewwordsisverymuchlikeagrowthprocess.However,theprocessofbehavioraladaptationisinsomewaysmuchmorecomplexthangrowth,beingcomplicatedbytheabilitytomakesuddenjumpsorreversalsinunderstanding,andbythecapacitytoadapttoauniformsituationinavarietyofways.Furthermore,whileanimalsmaybecomeincreasinglydifferentincertainbehavioraltraits,theymaybecomemorealikeinothers.
Thepartialresemblancebetweengrowthprocessesandlearninghasmoreimportancethanasimpleanalogy,foroneofthewaysinwhichhereditymayaffectbehavioristhroughgrowthitself.Aswesawinchapter6,sizehasadefiniteeffectonthedevelopmentofdominancerelationships.Howimportantsucheffectsmaybeisaquestionoffact,andthefactswehavearegiveninthefollowingpages.
PHYSICALDIFFERENCES333
THERELATIONSHIPBETWEENPHYSICALDIFFERENCESANDBEHAVIOR
BEHAVIOR
Therecanbenodoubtthatphysicaldifferencescanaffectbehavior.Whendifferencesareextreme,thisstatementhardlyrequiresscientificproof.Theshort-leggeddachshundrunsmoreslowlythanthelong-leggedgreyhound,andthetinyChihuahuaisunabletoclimbuponachair.Thebasicscientificproblemhereiswhetherornotphysicaltraitsalwayshaveaneffectonbehavior,andvarioustheorieshavebeenproposedconcerningthis.Oneisthetheoryofpleiotropy,ormanifoldeffects.Instudyingthegeneticsofthefruitfly,researchworkersdiscoveredmanycasesinwhichtherewasonemajoreffectofageneandmanyminorones.Forexample,Dobzhan-sky(1927)andSchwab(1940)studiedtheeffectsofvariousmutantgenesontheshapeofthespermatheca,oneofthepartsofthefruitflyskeleton.Bothcametotheconclusionthatthemajority,butnotall,ofthegenestestedhadanimportanteffectonthespermatheca.Fromsuchfactsseveralpossiblehypothesescanbedrawn.Atoneextremeisthehypothesisthateverygenewillhavesomeeffectuponeveryprocessinthebody.Thelogicbehindthisisthatanygeneispresentinthebodythroughoutlifefromthemomentofconceptionandthushastheopportunitytoaffectalllifeprocesses.
Attheoppositeextremewecanstatethehypothesisthateachgeneproducesonespecificprimaryeffectandthatpleiotropy,ormultipleaction,isdirectlyrelatedtoprimarygeneaction.Incaseswhereprimarygeneactioniswellknown,asinthesynthesisofvariouschemicalsnecessaryforlifeinthemoldNeurosporaandinbacteria,theusualsituationisalongchainofchemicalreactions,onegenebeingnecessaryforeachreaction(Beadle,1945).Thegenecanbethoughtofasoneelementinageneticcodewhosefunctionistotransferinformationtoabiochemicalsystem.Achangeinagenewhoseactivitytakesplaceearlyintheprocessmayaffectallthesubsequentparts,andmodificationofthisbiochemicalsystemmayaffectothersystemsdependentuponit,butalleffectsaretraceabletoasingleprimaryeffect.
Totakeanotherexample,basedonembryonicdevelopmentratherthanbiochemistry:thedominantgenewhichinahomozygoteproducesthedeformedpolydactylousmonsterintheguineapigaffectsalmosteverypartofthebodywithsuchseveritythattheaffectedanimalscannotsurvivebeyondbirth(Scott,1937).However,alltheseeffectscanbetracedbacktoanaccelerationofgrowthfor
afewdavsinaparticularstageofearlvdevelopment.Alltheorgansgrowingrapidl\'atthattimeareaffected.ThusthemanyactionsofthisgenecanbetracedbacktoasingleprimaryeffeI
Thesetwotheoriesarenotnecessarilymutuallyexclusive.Theremaybecertaingeneswhichhaveeffectsonallbodyprocessesandotherswhoseeffectsarehighlyspecific.Theprincipaldifferencebetweenthetwohypothesesisapracticalone.Thefirsthypotlassumesthattheinheritanceofbehaviorwillbeaffectedbyeverygeneaffectingaphysicaltrait.Thiswouldmakethestudyofbehavioralhereditvmuchsimplerbecausethecon:uldalsobetrue,andeven-beha\ioraldifferencewouldhaveanassociatedphysicaldifferencewhichcouldbeusedasamarker(Keeler.1942Ontheotherhand,ifthesecondhypothesisiscorrect,therewillbemanygenesaffectingphvsicaltraitswhichhavelittleornoeffectonbehavior.Likeanvbehavioraleffectscouldoccurwithoutvisiblechangesinformorshape.Nowletusexaminesomeoftheevidenceasitemergedfromourdogexperiment.
Theeffectofhairlengthonbehavior.—Hairlengthisacommonvariabletraitindogsandshorthairusuallyhasbeenreportedtobeinheritedasaclear-cutdominant(Dawson1937Cockerspanielsareuniformlylong-haireddogs,andanimalsbredfortheshowringaredeliberatelyselectedforlonghair,particularlyonthelegs.Ontheotherhand,basenjisareuniformlyshort-haireddogmeas-
uredthelengthofthehaironthebackbetweentheshoulderbladesofallanimalsatoneyearofage.AscanbeseenfromFiguretheresultsshowconsiderablevariabilitywithinthepurebreeds,andparticularlywithinthelong-hairedcockerspaniels.Partofthisvariabilityisproducedbvsheddingthehaircoat.Onecangetconsiderabledifferencesinmeasuringthesameanimal,dependingonwhetherthecoatismeasuredatitsmaximumlengthorshortlyaftersheddinghasbegun.Nevertheless,theshortesthairedcockerspanielshadcoatsatleastacentimeterlongerthanthelongesthairedbasen-
Thepictureisalsocomplicatedbythefactthatmalestendtohavelongerhairthanfemales,particularlyinthelong-hairedcockerspan-ThisistruealsointhewildCanidae.wherethemalesdevelopalongerruffthanthefemales.
TheF:'softhecockerspaniel-basenjicrossturnedoutverymuchasenjisexceptthatafewindividualshadslighdylongerhair.Ontheotherhand,therewasonlv
thatafewindividualshadslighdylongerhair.Ontheotherhand,therewasonlvonecaseofoverlapbetwee:andcockerspaniels,thatofoneF:malewiththesamehairlengthasacockerspanielfemale.Therewasnooverlapbetweenlike-
L
PHYSICALDIFFERENCES
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BASENJI(29)
iiiiiiiii024681012
F,(45)
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Fig.13.5.—Inheritanceofhairlength.Asingledominantgenewillaccountfor
Fig.13.5.—Inheritanceofhairlength.Asingledominantgenewillaccountformostoftheobservedvariation,althoughthereareprobablymodifyinggenespresentinthecockerbreed.Hairlengthwasmeasuredonthebackbetweentheshoulderblades.
individuals.Usingtheserelationshipsasaguide,weclassifiedtheanimalsintheotherhybridpopulations.Inthebackcrosstothecockerspanielstherewere14long-hairedand14short-haireddogs,correspondingexactlytotheexpected50-50ratio.IntheF2generationtherewere16long-haireddogsand57short-hairedones,correspondingquitecloselytotheexpectedratioof18.25to55.75.Weconcludedthatthedatastronglysupportedthefindingsofotherauthorsthattheinheritanceofhairlengthisdeterminedbyasingle
336DIFFERENTIALCAPACITIES
geneinwhichshorthairisdominantoverlonghair.Asindicatedabove,therecessivegenemayhavesomeeffectintheheterozygote,afewF*'sbeinglongerhairedthantheirbasenjiparents,andthereisalsoanindicationthatothergeneshavingaminoreffectonhairlengtharepresent,sincenoneofthelong-hairedcockerbackcrossesdevelopedcoatsaslongassomeofthepurebredcockers.
Thisgaveustheopportunitytoseewhethershorthairhadanyeffectonbehavior.Wehadstrongapriorireasonsforsupposingthatitwoulddoso,sinceashort-haireddogisobviouslymoreaffectedbycoldandlessprotectedagainstphysicalinjurythanalong-hairedone.Wethereforeexaminedtherecordsoflong-andshort-haireddogsinthebackcrossandF2generationsinrelationtothe10physicalmeasurementsand40behavioralmeasurementswhichBrace(1961)hadusedinhisfactoranalysis.
Inassessingsuchresults,onehastorememberthatdifferencescanoccursimplybychancewhenfinitenumbersareused.Wewouldexpectthatatleastonedifferenceoutof20wouldbestatisticallysignificantatthe.05levelsimplyasamatterofchance.In50variableschosenatrandom,weoughttogetontheaverage,2.5suchresultspurelybychance.Ontheotherhand,ifthereisarealandimportanteffectofthegene,weshouldgetmorethanthisnumberofsignificantdifferences,andthedifferencesshouldbeinthesamedirectioninthetwohybridpopulations.Afurthertestwouldbewhetherareasonablemechanismcouldbehypothesizedfortheobservedeffect.
Amongthebehaviorvariablestherewasonesignificantdifferenceinthe
Amongthebehaviorvariablestherewasonesignificantdifferenceinthebackcrosspopulation,intheobediencetest.However,thedifferenceinthesametestintheF2generationwasintheoppositedirectionandnotsignificant,andweconcludedthatthisapparentdifferencewasduetoanaccidentofsampling.AmongtheFYs,whichwehadinlargernumbers,thereweretwosignificantdifferences(Fig.13.6).Oneoftheseagainshowedanoppositedifferenceinthebackcrossgenerationandwasprobablyaccidental.However,therewasonehighlysignificantdifference,intheconfinementtest.Althoughthedifferencewasnotsignificantinthebackcross,itwasfairlylargeandinthesamedirection.Intheconfinementtest,thedogsinalitterwereconfinedoutdoorsinsmallwire-bottomedpensandgradedonallformsofactivitywhilealittermatewasremoved,handled,andfed.Theresultsindicatedthatshort-haireddogsweremoreactiveunderthesecircumstancesthanlong-haireddogs,whichisareasonableconclusion,becausetheshort-haireddogswould
PHYSICALDIFFERENCES337
havebeenconsiderablylesscomfortableincoldweather.Thisappearstobearealeffectofaphysicaltraitonbehavior.
Wealsocomparedthelong-andshort-haireddogsontheirphysicalmeasurements.Thelong-haireddogsaveragedlargerineverymeasurementinbothbackcrossandF2generations.Allthedifferenceswereinthesamedirection,butonlyoneofthesewasstatisticallysignificant.Sucharesultcouldbeeasilyexplainedbythefactthatallthemeasurementsweremadewithoutshavingthedogs,andthusthemeasurementsoflong-hairedanimalswouldbeslightlylarger,eveninthecaseofbodyweight.Anotherpossibilitymighthavebeenthattherewereaccidentallymoremalesinonegroupthananother,malesbeingbothlargerandhavinglongerhair.This
BACKCROSSTOCOCKER
-1.00-.60
Fig.13.6.—Distribution(instanines)ofdifferencesbetweenlong-andshort-coatedanimalsinrelationto34behavioralvariables(omittingthoseconfinedto2categories).Arrowsindicateapproximatestandarderrorofthedifferenceformostvariables.Longorshorthairhaslittleeffectonbehavior.
wasnotthecaseintheF2generation,inwhichmalesandfemaleswerealmostevenlydistributed.Wecanconcludethatlonghairmaypossiblyhaveaneffectonsizemeasurements,butifsoitisprobablyanartificialoneresultingfromslightlylessaccuratemeasurementofthelong-haireddogs.Inanycase,theeffectisnotanimportantone.
Despitethesenegativeresults,thereisnodoubtthatlonghairmayhaveaneffectonbehaviorinspecialsituations;e.g.,ashort-haireddogwillhesitatetositdownonsnoworice.Theexperimentdemonstratesthatthereisnoimportantgeneraleffectofthegeneforshorthairuponbehavior.Ifitistruethateverygeneaffectsallactivitiesofthebody,theeffectsofthisgenemustbesosmallastohavelittle,ifany,importanceandinfactbeunmeasurable.The
338DIFFERENTIALCAPACITIES
resultsupportsthesecondhypothesis,thatofspecificprimarygeneaction.
Theeffectofhaircoloronbehavior.—Whilewewereconductingourexperiments,Dr.C.C.Little(1957)wasmakingextensivebreedingteststodeterminetheinheritanceofcolorinalargenumberofbreeds,includingthoseusedinthebehavioralexperiments.Whilevariouscolorsarepermittedbythebasenjibreedstandards,theanimalsofourstrainwereallpureredasadults(exceptforwhitespotting),butthepuppieswerealwaysbornwithblackhairsmixedwiththered,theblackbeinglostatabout5or6weeksofage.
Crosseswithotherbreedsestablishedthefactthatthiscolorisproducedbythesamegeneasthatwhichproducesthecolorcommonlycalled"sable"incollies,whoselonghairisreddishoryellowishatthebaseandblackatthetips.Modifyinggenesinbasenjiscausetheblacktipstobelostinadults.
Thegeneavwhichproducestheredcolorinbasenjisisanintermediatememberofanallelomorphicseries,themostdominantgenebeingAs,agenewhichproducesasolidblackcolor,andtheleastdominantbeinga\producingblackwithreddishortanpoints.Whilesomeofthecockerswerered,thiswastheeffectofanotherrecessivegene,e,whichproducesaclearredcolorwithnoblackatanytimeinlife.
blackatanytimeinlife.
Consequently,thebasenjishadthegeneticconstitutionayay,thecockersA"A8,andtheFi's,A*av.BackcrossingtheFi'stobasenjisgavetwocolorsinapproximatelyequalnumbers:black(AW)andred(ayay).Thisgaveanopportunitytocomparethebehaviorandphysiqueoftwogroupsofanimals,onehavingthegeneA*andonewithoutit.
Thisanalysisgavenostatisticallysignificantdifferencesinanyofthephysicalvariables,althoughthegroupofredsaveragedslightlylargerthantheblacksonmostmeasurements.Thisresultwasprobablyaccidental.Therewasonesignificantdifferenceinthebehavioralvariables(P=.05),butthesametestintheF-populationshowedadifferenceintheoppositedirection,andnotsignificant.WemayconcludethatthereisnogeneralpleiotropiceffectproducedbythegeneA8.
Thisdocsnotmeanthatitisimpossibleforcolorgenestohaveeffectsonbehavior.Thereisacolormutationinthehousemousewhichitsdiscoverernamed"varitintwaddler"(CloudmanandBunker,1945).Thisanimalhasapeculiarmulticoloredspottingcombinedwithalimpinggaitresultingfromsomedefectinthenervoussystem.Likewise,the"merle"gene,foundinseveraldog
PHYSICALDIFFERENCES339
breeds,hastheeffectofchangingblackcolortoalightgraywithblackspots.Thiscolorismuchadmiredamongthefancy,particularlyinshelties,andisproducedbyadominantgene,M.Homozy-gotesareproducedwhicharealmostpurewhiteandoftenhavedefectiveeyesandears.Thesedefectivesenseorgans,ofcourse,causedifferencesofbehavior.Werearedonesuchanimalinourtestingprogram.Ithadsmalleyes,oneofthembeingalmostcompletelysightless,sothatitdidnotrespondtovisiononthatside.Itwasalsodeaf,butthisseemedtohavetheeffectofmakingitlesseasilydistracted,sothatinmanytestsitactuallydidbetterthannormalanimals.
Sincethepigmentcellsoriginateinembryonicdevelopmentfromthecrestoftheneuraltube,itislikelythattheprimaryeffectofthegeneistoalterthedevelopmentoftheneuraltubeandrelatedsenseorgans,thisinturnaffectingthedistributionoftheneuralcrestcellswhicheventuallyproducepigment.
Wecanconcludefromthesedatathatatleastsomecolorgeneshavenodemonstrableeffectonbehavior.Althoughcertainothercolorgenesmayhave
demonstrableeffectonbehavior.Althoughcertainothercolorgenesmayhaveeffectsonbehavior,theseeffectsareassociatedwithdefectsinthedevelopmentofthenervoussystem.
Theeffectsofbodysizeandproportionsonbehavior.—Physicalbuildandbehaviorhavelongbeensupposedtobeassociated.Accordingtotradition,fatpeoplearejolly,thinpeoplearesouranddyspeptic,andheavilymuscledmenarequicktoanger.ThemostambitiousattempttoinvestigatethistraditionwasundertakenbyW.H.Sheldon,whodevelopedatechniqueforestimatingbodyproportionswhichhasbeenwidelyusedinanthropologyandbydepartmentsofphysicaleducation.Sheldonmeasuredthebodyintermsofthreecomponents,eachmeasuredona7-pointscale.Thefirst,endomorphy,isbasedontheamountofbodyfat.Thesecond,ormesomorphy,isameasureofheavybonesandmuscles;andthethird,ectomorphy,isthetendencytohaveahighproportionofskin(actually,tobethin)withlightbonesandmuscles.Thetechniqueofmeasuringbodytypes,orsomatotypes,inthiswayistotakephotographsofthenudebodyinstandardpositions,blackingoutthefaceforreasonsofanonymity.Thebodytypeisthenestablishedona7-pointratingscaleforeachcharacteristic.
Sheldon'stechniquecanbecriticizedonthegroundsofbothsubjectivityandlogic(Hammond,1957).Theaccuracyofthescalesdependsagreatdealontheexperienceandskillofthepersonusingthem.Therearelogicallyonlytwoindependentcomponents,sinceectomorphyisessentiallyanabsenceoftheothertwo.Howells
340DIFFERENTIALCAPACITIES
(1952)hasshownbyafactorialanalysisofnumericalmeasurementsmadeofmendesignatedasextremesomatotypes,thatthereisactuallyonlyonescale,endomorphy-ectomorphy,andonecomponent,fat,thatcanberelatedtoSheldon'ssystem.However,thechiefinteresttousliesinthefactthatSheldonandStevens(1942),onthebasisofmanycasehistories,statedthattheyfoundacorrelationbetweensomatotypeandtemperament.Aswehavesaidbefore,physiqueobviouslyaffectsbehavior.Aboywithstrong,heavymuscles,forexample,ismorelikelytoenterasportlikefootballorboxingthanaboywithslightandwirybuild.SheldonandStevenswentbeyondthis,implyingthatthesamefactorswhichproducedphysicalbuildaffectedbehaviorindependently,producingtraitswhichhadnothingtododirectlywithphysicalbuild.Thisisessentiallythesametheoryofgeneralpleiotropywhichwehavediscussed
essentiallythesametheoryofgeneralpleiotropywhichwehavediscussedbefore.
Ourlong-termexperimentwithdogsseemedlikeanidealopportunitytotestSheldon'stheoryoftheeffectsofsomatotypesonbehavior.CharlesShade,oftheHarvardUniversityDepartmentofPhysicalAnthropology,spentasummerdevisingasystemformakingbodymeasurementsondogs.HefoundfirstofallthatSheldon'ssystemofphotographswasimpracticalwithdogs,sincethefurmakessomuchdifferenceinphysicalappearance.Everyanimalwouldhavetobeshavedforthissystemtowork.Furthermore,itseemeddesirabletotrytoimproveonSheldon'ssystemanddevisemoreobjectivemeasurements.Shadefinallydevelopedaseriesofsevengeneralmeasurementswhichcouldbedonewithreasonableaccuracy,andwelateraddedthreespecialmeasuresofboneandmusclesizetomakeatotaloften.
Thefirsttwoofthesewereover-allmeasurementsofbodysize:weight,andbodylengthfromtheanteriorendofthebreastbonetotheposteriorpointofthehips.Theaccuracyofthislastmeasuredependedonbeingabletogetthedogtostandwithitsbodyinastraightlineandinanaturalposition.Thentherewerethreemeasurementsofthechestregionofthebody:brisketdepth(measuringthechestfromtoptobottom),chestbreadth,andchestcircumference.Theabdominalregionwasmeasuredbywaistcircumference.Heavinessofbonewasmeasuredbytakingthediametersofthefemurandhumerus,thelargebonesofthehind-andforelimbs.Heavinessofmuscleswasmeasuredbytakingthecircumferencearoundthethigh,thusmeasuringoneofthelargestmusclegroupsinthebody.Finally,leglengthwastakenbymeasuringthestandingheightattheshoulder.Thus,ifthereweredogswithunusual
PHYSICALDIFFERENCES
341
70
6.5
6.0
iii
z
25.0m
4.54.03.5
humerusdiam.
waist
thighchestdepthfsmurdiam
bodylengttichestbreodth-humsrusdlam^'
tailr'
/Vheight/Awolstc.
thighc.bodylength
chestc.femurdiam.chestbreadth
height
height
f
BA
3.03.54.04.55.05.5
WEIGHT(STANINES)
6.0
6.5
Fig.13.7.—Relativeproportionsofcockerspanielsandbasenjis.Ifthetwobreedshadthesameproportions,allthelineswouldbeparalleltothatofweight.Actually,onlywaistcircumferenceandchestbreadthareapproximatelysimilar.
Ifthebasenjisweresimplythinnerdogs,alllineswouldbeparallelbutrunupwardwithrespecttoweight.Actuallythelinesrunindifferentdirectionsandthemeasurementsoccurindifferentordersinthetwobreeds(rankordercorrelation=—.17).Basenjisarerelativelytaller,andhaveathickerhumerus,deeperchests,andlongerbodiesthanspaniels.
amountsoffat,muscle,orbone,thesemeasurementsshouldreflectsuchtraits.
Webegantakingthefullsetofmeasurementsat17weeksofage,andrepeatedtheseat34and51weeks.Wetookthelastmeasurementstorepresentthefinalphysicalbuildoftheadultdog,andanalyzedtheminvariousways.
Whenwetaketheaverageofeachoneofthesemeasurementsforeachpurebreedandcompareittotheaverageweightofthebreed,wefindthatthereareindeeddifferencesinproportions(Table
DIFFERENTIA!CAPACITIES
13.2).Thesheltiesshowthegreatestnumberofextremedeviationsandcouldbedescribedashavinglargeanddeepchests,thinwaists,smallthighs,smallbones,longbodies,andlonglegs.InmanyrespectsthevcorrespondtotheectomorphsofSheldon'ssomatotvpes.
TABLE13.2
TABLE13.2
RankfromLargest(1)toSmallest(5)inBodyMeasurementsRelativetoWeight,intheFivePureBreeds
Xoneoftheotherbreedsshowssuchextremedeviations.Wire-hairedterriersarethickwaistedandhaveaheavythighandfemur,indicatingthatthevhavelargemusclesandthickboneswhichwouldbeusefultoabreedusedforattack.Theymightbelabeledmeso-morphs.thoughnotofanextremetvpe.Cockersarerelativelysmallchestedandshort-bodiedinproportiontoweight.Beaglesarerela-tivelvbroadchestedandshort-legged,butotherwiseundistin-guished.However,thismayhavebeencausedbyoneofthefoundationmaleshavingtheseproportions,ratherthanbeingcharacteristicofthebreedasawhole.Basenjis,althoughthevhaveadistinctiveappearance,areoutstandingonlvinhavingaheavyhumerus.
Tocomparethetwobreedsusedinthecross,basenjisarelargerinalmosteven-dimensionthancockers,bothinabsolutesizeandsizerelativetoweight.Thislastmeanschieflythatbasenjisarerelativelythinandcockersrelativelvfat.Thetwobreedsaremostdifferentinrespecttoheight;thenextmostimportantdifferencesareinthedepthandsizeofthechest,andbodylength.Thusbasenjisaretall,thin,deepchestedandlong-bodied,whilecockersarerelativelyshort,fat,shallowchestedandshort-bodied.Thediffer-sidproportionarenotextreme,andinSheldon'ssvstemthebasenjiwouldprobablybea'mescctomorph,"andthecockera"mesendomorph."
Aftermeasurementswerecollectedforallhvbridsaswellaspurebreeds,anotherphysicalanthropologist,LoringBrace(1961),began
PHYSICALDIFFERENCES343
hisdetailedstudybythemethodoffactorialanalysis.Hefirstconvertedallmeasurementsintostanines.Asdescribedinchapter7,thisisamethodoftenusedinpsychologytoconvertmeasurementsintoaforminwhichtheycanbeeasilyanalyzedbythemethodsofnormalcurvestatistics,includingstandarddeviationsandcorrelationcoefficients.
Bracechose40behavioralmeasurestocomparewiththe10measurementsofphysicalsize,selectingthosewhichseemedtoshowthemostclear-cutbreeddifferencesandindicationsofMendelianinheritance.Someofthesemeasurementscamefromthesametests,butthesewereoneswhichappearedto
measurementscamefromthesametests,butthesewereoneswhichappearedtobeatleastpartiallyindependentofeachother.Therewere13separatebehavioraltestsituationsrepresented.Bracethushad50measurementsoneachdoginfivedifferentpurebreeds,plussixhybridpopulationsbetweenthebasenjisandcockers,asbasicdata.
Factoranalysisisamathematicalmethodbasedoncorrelation.Thelogicbehinditsusewasthatiftherewereseveraldifferentbehaviortraitsorphysicalmeasurementsaffectedbythesamegenesorgroupofsimilargenes,theneachtraitshouldbecorrelatedwithalltheothers,appearingtogetherinthesameanimalandbeingmeasurablebycorrelationcoefficients.Themethoditselfisdesignedtosortoutgroupsofmeasurementswhichhaveacommoncorrelation,andthepresumedcausebehindsuchagroupiscalledafactor.IfthereisanytruthinSheldon'scontentionthatsomatotypeisrelatedtobehavior,weshouldgetfactorsincludingbothphysicalmeasurementsandbehavioralmeasurements.
Thefirstmathematicalstepwastocorrelateeachofthe50variableswitheachotherone.Thismeantcalculatingatotalof1,225correlationcoefficients,alongwiththemeansandstandarddeviationsforeachmeasurement.Bracedecidedtocalculatesuchtablesforeachbreedandhybridpopulation,andbyusingmoderncalculatingmachines,hewasabletocalculate50X50correlationtableson16differentpopulationsofanimalsinasinglenight'swork.Thismeantatotalof19,600correlationcoefficients.This,however,wasonlythebeginning.Thecommunalityofcorrelationstillhadtobedeterminedbytheprocessofrotation,whichisequallylaborious.This,however,couldbedonebyprogrammingcomputingmachines,andafterseveralmonths'work,Bracewasabletogetthemachinessetupsothattheywoulddothejobaccurately.Insodoing,hewasabletouseamathematicalmethod(thatofprincipalaxes)whichhadhithertobeenimpracticalbecauseofitslaboriousnature.
Wemaynowconsiderfactoranalysisinrelationtogenetics.The
344DIFFERENTIALCAPACITIES
methodisbasedoncorrelation,whichinturnisbasedontheassumptionofadditiveeffectsofcausalfactors.Studiesofgrowthandphysicalsizehavegenerallyindicatedthatgeneticfactorsaffectingsizeareadditive;thatis,eachgenemakestheanimalalittlebigger.Ontheotherhand,aswehaveshowninotherchaptersofthisbook,complicatedinteractionbetweengenesisaverycommonphenomenonaffectingtheexpressionofotherkindsofphysiologicalandbehavioraltraits.Themathematicallogicbehindtheuseofthecorrelation
andbehavioraltraits.Themathematicallogicbehindtheuseofthecorrelationcoefficientassumesthatthesamegenealwaysproducesthesameeffect,andthismaynotbetrueinthecaseofgenesaffectingbehavior.
Assuming,however,thatwecangetgoodadditiveeffects,therearetwowaysinwhichhereditycanproducecorrelationinadditiontothecaseofasinglegene'seffectondifferenttraits.Oneoftheseisthepresenceoftwogenesonthesamechromosome,producingthegeneticphenomenonoflinkage.Theotheristhesimultaneousselectionofseveraldifferenttraitsinasinglebreed.Wewouldexpectthatinanypurebreedtherewouldbeanumberofdifferentgenesbroughttogetherbyselection.Hence,inapopulationofseveralpurebreedswewouldexpecttogetgroupsofartificiallycorrelatedgeneswhichwouldappearinafactoranalysisasbreedfactors.
InsegregatingpopulationssuchasthebackcrossorF2generations,weshouldgetcorrelationsbetweenalloftheeffectsproducedbyeachsegregatinggene,orbyeachgroupofcloselylinkedgenes.TheF2populationwouldprovidethebestopportunityforsuchcorrelationstoshowup,becausetheeffectsofallsegregatinggeneswouldappear,astheymightnotinabackcrosstoadominantparentpopulation.
Wewouldalsoexpecttogetdifferentfactorsinthedifferentsegregatingpopulationsbecauseofdominance,whichwouldcompletelysuppresstheactionofarecessivegeneinabackcrosstoadominant.Thereshould,therefore,befewercommonfactorsbetweenbackcrossesthanbetweenbackcrossesandF2's.
Ontheotherhand,ifwearedealingwithnon-geneticcorrelations,thesamefactorsshouldappearinallpopulations.Wewouldexpectthatatleastsomeofthesenon-geneticfactorswouldturnupbecauseofthefactthatmorethanonemeasurementwastakenfromcertaintests.Somemeasurementscouldbecorrelatedsimplybecausetheycamefromthesametestsandweredoneontheanimalatthesametime.
Thecorrelationbetweenphysicalsizeandbehavior.—TheF2populationprovidesthebestchancefordetectingcorrelationsdue
PHYSICALDIFFERENCES
345
tocommongeneticfactors.Withoutgoingthroughtheentirefactoranalysis,we
tocommongeneticfactors.Withoutgoingthroughtheentirefactoranalysis,wecangetsomeideaoftheeffectofphysicalmeasurementsonbehaviorbysummarizingthecorrelationmatrix(Table13.3).Ininterpretingtheseresults,wemustrememberthatacertainnumberofcorrelationsmayoccursimplybyanaccidentofrandomsampling.Inourpopulationof72F-hybridsthereis1chancein20thatcorrelationslargerthan.23willappearsimplybyaccident.
TABLE13.3
SignificantCorrelationsbetweenPhysicalMeasurementsandBehavioralVariablesinPureBreedsandHybrids
•Correlatedtestsarenotidenticalinthesetwogroups.
ThephysicalmeasurementsintheF2'sareallhighlycorrelatedwitheachother.The45possiblecorrelationsrangefrom.90to.40,withmostofthemtowardthehigherend.Thereisnodoubtthatsizemeasurementsarecorrelatedwitheachother.
Ontheotherhand,thecorrelationsbetweenphysicalandbehavioralmeasurementsareallsmaller,thegreatestonebeing—.36.Eachofthephysicalmeasurementscouldbecorrelatedwiththe40behavioralmeasurementsmerelybychance1timeoutof20,oratotalof2times.The10measurementsshouldthereforeshow20significantcorrelationsmerelybychance,andtheobservednumberis24.Althoughthepossibilityexiststhatsomeofthesearerealcor-
DIFFERENTIALCAPACITIES
relations,thereisnoevidencethatthereisanystrongorimportanteffectofphysicalsizeonthe40behaviormeasurementschosenforanalysis.
Sincethephysicalmeasurementsarecorrelatedwitheachother,weshouldexpectthemtobecorrelatedwiththesamebehavioralmeasurementswhetherornotthiswasamatterofchance.Thiswasindeedthecase,and18ofthe25significantcorrelationsrelateto4behavioraltests:habit-formation,vocalizationinthereactivitytest,numberoferrorsinthebarriertest,andplayfulaggressivenessinthehandlingtest.Someofthese,likeplayfulaggressiveness,mightreasonablybeeffectsofsizedifferences.However,thelowcorrelationsandthesmallexcessofsignificantcorrelationsbeyondchanceexpectationsleadtotheconclusionthattheeffectsofphysicalsizeonthebehaviortestsareminorones,iftheyexistatall.Inshort,variationinphysicalsizehaslittleifanyeffect
ones,iftheyexistatall.Inshort,variationinphysicalsizehaslittleifanyeffectonthevariationofbehaviorintheF2population.
Whenwelookattheresultsofcorrelatingphysicalandbehavioralvariableswithinthepurebreeds,wegetasomewhatdifferentimpression.AsTable13.3shows,thebasenjisshowslightlymorethan
TABLE13.4
FactorLoadingsofPhysicalVariablesinCombinedFaPopulation,PrincipalAxisRotation*
Theloadingsindicatetherelativeefficiencyofeachvariablea?ameasureofgeneralsizeandfallinto4groups.
the
expectednumberofsignificantdefinitelyless.Theotherthree
correlationsandthebeaglesvbreedseachshowtwicetheexpectednumberofsignificantcorrelations.Withincertainofthepurebreeds,itlooksasifphysicalsizemighthavesomeeffectonbehavior.
PHYSICALDIFFERENCES347
Suchcorrelationsmightinpartbecausedbythefactthatthephysicalmeasurementsthemselvesarecorrelated.Wecantestthispossibilitybyexaminingthesampleofphysicalmeasurementsindependently.Actually,anyoneofthephysicalmeasurementsshowsmorethanthenumberofcorrelationsexpectedbychance.Thereisthusastrongpossibilitythatphysicalsizehasanimportanteffectonbehavioragainstthegeneticbackgroundspeculiartocertainbreeds.Adifferenceinsizemightbeexpectedtoproducearelativelyconsistenteffectonanimalsshowingsimilarbehaviorandthusshowupasacorrelation.However,analternateexplanationoftheresultsmightbethatthereareindividualsorstrainswithinapurebreedinwhichphysicalmeasurementsandbehavioralmeasurementsareaccidentallycorrelated,andthispossibilitycannotbeentirelyruledoutbythedata.
Relationshipsbetweenthephysicalvariables.—ThefactorloadingsintheF2populations(Table13.4)showhoweachmeasurementisrelatedtogeneralsize.Weighthasthehighestloading,followedbythethreemeasuresofcircumference,withalllinearmeasuresfallingbelowthese.Thisisareasonable
circumference,withalllinearmeasuresfallingbelowthese.Thisisareasonableresult,sinceweightcombinesalldimensionsofthebody,acircumferencecombinestwo,andalinearmeasurementonlyone.
Theloadingsthusfallintofourgroupsrelativetoeachother.Bodyweightandchestcircumferencehavethehighestloadingsonthegeneralsizefactor,formingthefirstgroup.Bodyweightmeasurestheentiresize,whereaschestcircumferencemeasuresthesizeofthethorax,thelargestpartofthedog'sbody,whichincludesmanyofhisinternalorganssuchastheheart,lungs,liver,etc.Inthenextgrouparethighcircumference,whichmeasuresthesizeofthehindlimb,andwaistcircumference,whichmeasuresthesizeoftheabdominalregion.Inthethirdgrouparefivemeasurementswhichhavealmostidenticalfactorloadings.Thetwochestmeasurementsarehighestandthetwobonemeasurementsthelowest.Finally,standingheight,whichmeasuresthelengthoftheforelimb,fallsintoagroupbyitself,withaverylowloadingcomparedtotherest.
Thefactoranalysisindicatesthatanymeasureofthebodyisstronglyrelatedtogeneralsize,andthusthatallthedogsintheFl»populationhavemuchthesameproportions.Theonlyexceptionisthemeasureofheight,whichmaybedisproportionatetotherest.Thereisnoindicationofdisproportioninanyspecialtissues,suchasfat,bone,ormuscle,inthispopulation.
Generalresultsofthefactoranalysis.—Braceusedtwomethodsoffactoranalysisoneachpopulation.Theprincipalaxismethodisthe
DIFFERENTIALCAPACITIES
idealmathematicalmethod(Thurstone,1947)andproducesagroupofmeasurementsrelatedbycommoncorrelationandweightedaccordingtotheimportanceofeach.Thisweighting,orfactorloading,canbeeitherpositiveornegative,andcanvaryfromzerotoone.Becausesomanymeasurementsappearineachfactor,theresultsaresometimeshardtointerpret.Thevarimaxmethod(Kaiser,1958)isusedtoemphasizethosemeasurementshavingthelargesteffectandtoeliminatetheunimportantones,andsoaidintheinterpretationofthefactors.Onlytheresultsoftheprincipalaxismethodareconsideredhere.
Aswestatedabove,theF2'sprovidethecriticaltestofthehypothesisthatphysicalmeasurementsareassociatedwithbehavior,sinceinthispopulationgeneticvariationshouldoccurfreelyinallrespects,withaminimumamountofcorrelationduetolinkageandaminimumeffectofdominance.Aswemight
correlationduetolinkageandaminimumeffectofdominance.Aswemightexpectfromthebasiccorrelationtable,onlyonebehavioralmeasurehasaloadingofanyappreciableimportanceonthegeneral-sizefactor.Goodperformanceonrunningtoagoalinthehabit-formationtestisweaklyassociatedwithlargesize(.29).Thisisareasonableeffect,butsosmallthatitmaywellbeaccidental.Furthermore,noneofthephysicalmeasurementshaveloadingsonanyoftheotherfourbehavioralfactors.Wecanonlyconcludethatthephysicalmeasurementshavenoimportantconnectionwithbehaviorinthecrossbetweenthesetwobreeds.
TABLE13.5
FactorLoadingsofFactor1(GeneralSize)inCombinedPureBreeds(N=100)
Variables
Physical:
Chestcircumference
Brisketdepth
Weight
Bodylength
Standingheight
Humerusdiameter
Waistcircumference
Thighcircumference
Chestbreadth
Femurdiameter
Behavioral:
Fewerrors,U-shapedbarrier
Fastspeed,longbarrier
Fewerrors,longbarrier
Fewnoises,U-shapedbarrier
Success,manipulation,stringpulling
Success,manipulation,movingbox..
Fastspeed,maze
Activewhileweighed
FactorLoading
.88.87.77.76.74.73.73.71.65.64
.48.44.43.37.36.36.35.30
PHYSICALDIFFERENCES
349
Whenwelookattheotherpopulations,wefindthatineveryonethephysicalvariablesarestronglycorrelatedandthatthefactoranalysisconsequentlyassignsthemhighloadingsonafactorofgeneralsize.Thesegregatingpopulationsareofparticularinterestindeterminingtherelationshipofthisfactortobehavior.Intheback-crosstothecocker,theheartrate—bothofpuppiesandadults—isassociatedwithsize,largedogshavingaslowerrate.Thesamethingistrueinthebackcrosstothebasenji,butthiseffectdoesnotappearintheF2S.Themostlogicalexplanationisthatitisaneffectoflinkageupontwotraits,neitherofwhichisaffectedbydominance.Inthebackcrosstothebasenji,therearethreeotherbehavioralvariablesassociatedwithsize,buttheloadingsarelowandlackalogicalexplanation.Theselastresultsarethereforeprobablyaccidental.
Incontrasttodiesegregatinghybrids,thepurebreeds,bothtogetherandseparately,showalargenumberofbehavioralvariablesassociatedwithsize(Tables13.5and13.6).Theseseemtobedifferentineverybreed,andthevarimaxrotationhaslittleeffectuponthem.Itlooksasifsizemayhaveaneffectonthebehaviorofanimalswhicharesimilartoeachotherotherwise,butthatthe
onthebehaviorofanimalswhicharesimilartoeachotherotherwise,butthattheeffectsarenotconsistent.Inotherwords,sizedoesnotproducethesameeffectonthebehaviorofasheltieasitdoesonthatofafoxterrier.
TABLE13.6
FactorLoadingsofFactor1(GeneralSize)inShetlandSheepDogsandFoxTerriers
Variables
Physical:
Chestcircumference
Femurdiameter
Brisketdepth
Weight
Chestbreadth
Humerusdiameter
Waistcircumference
Bodylength
Thighcircumference
Standingheight
Behavioral:
Manipulation,movingbox,success..
Manipulation,stringpulling,success
Littlevocalization,leashcontrol
Littlevocalization,reactivity
Muchvocalization,U-shapedbarrier
Fightingleash
Activeinconfinement
Obedience,littledocility
Fewerrors,longbarriertest
FoxTerriers
350DIFFERENTIALCAPACITIES
Ofcourse,itmaybethatthesecorrelationsareproducedbyaccidentalassociationofsizeandtemperamentamongtheoffspringofdifferentmatingswithinthesamebreed.Thispossibilitycanbetestedbycomparingtheresultsofreciprocalcrossesbetweenthetwobreeds,sincetheparentsinacrossbetweenmalebasenjisandfemalecockersarenecessarilydifferentindividualsfromthoseinthereversecross.InthetwoFipopulationsthereare13behaviortestswhichhavemoderatelyhighloadingsonfactor1.Ofthese,onlytwoarefoundinbothpopulations.Thiswouldmeanthatmostoftheapparenteffectsofphysiqueonbehaviorareprobablycausedbyaccidentalassociationbutthatsomeeffectsmaybereal.
TheseresultscorrespondtothoseofHumphreyandWarner(1934),whocorrelated42measuresofphysiquewith9measuresofbehaviorwithintheGermanshepherdbreed.Theyobtainedonly15correlationsoutofapossible378.Themostthatwecansayisthatthereisapossibilitythatsizehasvaryingeffectsonbehaviordependingonthegeneticconstitutionoftheindividualinvolved,butthatthisisatpresentonlyaninterestinghypothesis.
Withregardtotheotherresultsofthefactoranalysis,onebasichypothesistobetestedwasthattherewereafewbasicgenetictraitsofbehaviorwhichmightaffecttheresultsofmanydifferenttestsandsorunthroughthewholelifeofananimal.Ifsuchtraitsrepresentedtheactionofdifferentgenes,thenonewouldexpecttogetdifferentfactorsindifferentpopulations,dependingbothonthepresenceorabsenceofthesegenesandalsoupontheirmaskingbydominance.Insteadofthis,Bracegottheoppositeresult:muchthesamefactorsappearedineverypopulation.Therewasonefactoremphasizingphysicalmeasurements,anotheremphasizingphysiologicalmeasurements,andtwootherswhich
anotheremphasizingphysiologicalmeasurements,andtwootherswhichincludedbehaviormeasurements.Ofthelatter,oneincludedmostoftheperformancetests,andtheotherwasstronglyrelatedtotestsofemotionalreactivity.
Allthissuggeststhatsimilarkindsofbehaviorandphysiologicalactivityarecloselyrelatedonlytothemselves.Hereagainthedatadisagreewiththetypeconcept;thebehaviorofananimalinonesituationisnot"typical"forhisbehaviorinanothersituation.Amoredetailedstudyofthebehavioralaspectsofthefactoranalysiswillbegiveninanotherchapter.
Thustheresultsofthisexperimentarealmostcompletelynegativewithregardtothehypothesisthata"somatotvpe"isstronglycorrelatedwithtemperamentandbehavior.Itcan,ofcourse,bearguedthatsucheffectsmightappearinacrossbetweentwobreedscontrastingmoresharplyinphysicalbuildthandocockersandbasenjis.
PHYSICALDIFFERENCES351
However,therearegoodtheoreticalreasonsforbelievingthatgeneticfactorsaffectingbodybuildandbehaviorarelargelyindependentofeachother.
Evaluationofthesomatotypeconcept.—Wecanmakeabasictheoreticalcriticismofthesomatotypeapproachtobodybuildandbehavioronthegroundthatitrepresentsaprimitiveandnowalmostdiscardedmethodofbiologicalstudy.Thetypingmethodwasusedbytheearlynaturalistsintheirdescriptionofanimalspecies.Theyfirstselectedanindividualforverycarefuldescriptionandcalledthisthe"type"ofthespecies.Oftentheindividualwasselectedonthebasisofintuitionorsimplybecauseitwasavailable.Thentheyattemptedtodescribethespeciesasawholeascomparedtotheindividual"type."Thismethodhasobviousdrawbacks,anditresultedintheartificialcreationofmanyspecieswhichdidnotexistinnatureandwerelatershowntobepartofthesamepopulation.
Thetypingmethodcangiveaverymisleadingpictureofapopulation.Forexample,thetypespecimenselectedforNeanderthalmanturnedouttobeanoldmanprobablysufferingfromarthritis,withknobbybonesandstoopingposture.LatercollectionsofotherspecimensshowthatmanyNeanderthalskeletonsareindistinguishablefromthoseofmodern-dayEuropeans(Brace,1962).
Themodernapproachofnaturalistsistomeasureanddescribethepopulation
Themodernapproachofnaturalistsistomeasureanddescribethepopulationfirstandthentodescribetheindividualintermsofthepopulation.Thismeansthecollectionofmeasurementsonareasonablylargesampleofthepopulation,fromwhichestimatesoftheaverage,standarddeviationandvariancecanbemade.Inthisexperimentwehaveusedthepopulationmethod,butinsuchawaythattypescanberecognizediftheydoinfactexist.Ifapopulationisdividedintofourorfivetypesinsteadofshowingcontinuousvariation,weshouldgetclustersofcorrelatedtraitsbythefactor-analysismethod.Ifphysicaltypeisassociatedwithbehavioraltype,thensomephysicalmeasurementsshouldbeassociatedinonegroupbythemselves,withdifferentsetsofphysicalmeasurementsinothergroups.Thisdidnothappeninthefactoranalysis,andhencealltheevidencewhichwehavecollectedisagainsttheexistenceofsuchtypes.
Dogbreeders,inchangingandimprovingtheirbreeds,haveusedthetypemethod,selectinganindividualasagrandchampionandthenattemptingtobreedforthisparticulartype.Ifthecharacteristicsofanindividualareinfactproducedbyalargenumberofvariablegenes,producingauniformtypeshouldbeanextremelydifficulttask,asthedogbreedershaveindeedfound.Muchvari-
352DIFFERENTIALCAPACITIES
abilityremainsineverybreed.However,thebreedshavetosomeextentbeenstandardizedbyselection,andwhenthecombinedpurebreedsareanalyzedbythefactor-analysismethod,thereshouldconsequentlyappearcertainfactorswhichcorrespondtothegroupoftraitspeculiartothe"type"ofeachbreed.Asindicatedabove,thiswasnotthecase,andwemustconcludethattheassociationoftraitsproducedbyselectionforatypeisquiteweak.
Theearlygeneticistsalsousedthetypeconceptindescribingmutationsand,infact,didnotevenbothertostudyhereditaryvariationunlesstheyfoundagenewhichproducedaclear-cut"pheno-type."Aswithtaxonomists,themoderntendencyistousethepopulationapproach,butthetypeconceptmaystillbeusefulindescribingcertainextremetraitsorcombinationsoftraits.
Thisbringsusdowntotheunderlyingtheoryofgeneticeffectsonadultcharacteristics.Allourevidenceisconsistentwiththehypothesisofspecificprimaryeffectsofgenes.Whilepleiotropymayexist,itcertainlydoesnothaveuniversalimportance.Typingmaybeusedtodescribetheeffectsofasinglegenewhichhaseitherimportantpleiotropiceffectsoronemajoreffectwhich
genewhichhaseitherimportantpleiotropiceffectsoronemajoreffectwhichcarriesthephenotypeoutsidethenormalrangeofvariation.However,themajorityofevidencepresentedinthisandpreviouschaptersisonthesideoftheconclusionthatthedifferencesbetweenthedogbreedsareproducedbylargenumbersofindependentgenes,eachhavingahighlyspecificeffectonbehavior,physiology,orstructure.
CONCLUSIONSANDHUMANAPPLICATIONS
Bothbreedandsexdifferencesaffectthepatternsofgrowthofyoungpuppies.Thereislittledifferenceinsizeatbirth,butasthepuppiesgrowoldertheybegintodivergeanddifferentiatefromeachother,theamountofdifferencebeingproportionaltoage.Canthisdifferentiationbetakenasamodelforthedifferentiationofbehavior?Growthisanaccretionaryprocess,withalittleweightbeingaddedeaclidaytowhatwastherebefore.Toacertainextent,thisisalsotrueofthelearningprocess,aseachdaythepuppyhasnewexperiencesandpresumablylearnsalittlemore.Inthisway,thetwotypesofdifferentiationaresimilar.
However,insolvingaparticularnewproblemthepuppydoesnotinvariablymakeuseofallthathehaslearnedpreviously.Infact,iftheproblemisnewenough,hemayhavetostartfromthebeginningandwillbeabletouseverylittleofhisoldknowledge.Furthermore,
PHYSICALDIFFERENCES353
theprocessoflearningoftenproceedsbysuddenjumpsorsaltationratherthangradualaccretion(Hebb,1949).Whileonecanweighadogandmeasureallthathehasgrown,itisdifficulttodeviseanytestsituationwhichwillmeasureallthathehaslearned,oreventogivehimmanydifferenttestsandaddtheresultstogetherinanymeaningfulway.Ourconclusionisthatwherelearningistrulyac-cretionary,themodelofgrowthwillapply,butthattherearemanycasesoflearningwhichdonothavethispropertyandforwhichgrowthishenceapoormodel.
Physicaltraitshaveobviouseffectsonbehavior.Theshort-leggeddachshundcannotrunasfastasanormal-leggedbeagle,andtheheavymusclesofaterrierhaveobviousadvantagesinfighting.Thiskindofeffecthardlyneedsscientificproof.Afurtherproblemiswhetherornotphysicaltraitshavemoresubtleeffectsonbehavior,andthisisrelatedtothegenetictheoryofpleiotropy.Proponentsofitsmostextremeformhavearguedthateverygenemusthave
Proponentsofitsmostextremeformhavearguedthateverygenemusthavesomeeffectoneverybodyprocess.Opposedtothiswehavethetheoryofspecificprimaryeffectsofgenes—thatagenehasoneprimaryeffectwhichmayormaynotaffectotherprocesses.Underthislattertheorysomegenesmighthavepleiotropiceffectsandothersnot.Wehavetestedthesehypothesesbymeasuringthecorrelationbetweenknowninheritedphysicaltraitsandbehavior.Ifthegeneraltheoryofpleiotropyweretrue,suchgenesoughttoaffectalmosteverybehavioraltest.Asamatteroffact,thegenescontrollinghairlengthandtheredcoloringofbasenjishadnoappreciableeffectonawidevarietyofbehavioraltests,orevenuponmeasurementsofbodyproportions.Theevidenceisdefinitelyinfavorofthetheoryofonespecificprimaryeffectofagene.Thisdoesnotexcludepleiotropyinspecialcases,andweknowofatleastonedoggenehavingpleiotropiceffects,thatformerlespotting.Eveninthiscase,however,thereisevidenceforaspecificprimaryeffect.
Relatedtothetheoryofpleiotropyisthetheoryofbodyandbehavioraltypes;i.e.,thatallthemanifoldeffectsproducedbyapleiotropicgenecanbesummedupasatype.Braceconductedaveryextensivetestofthetypetheorythroughthemethodoffactoranalysis.Whilethedogbreedshavebeenselectedastypes,thecrucialgenetictestintheF2populationshowsthatthebreedtypesdonotreappearassuchintheF2,s,eitherinbodyconformationorinotherphysicalcharacteristicssuchashairlengthandcolor.Theevidenceisinfavorofalargenumberofindividuallysegregatinggenesratherthanafewmajorgeneshavingpleiotropiceffectsand
354DIFFERENTIALCAPACITIES
producingseparatetypes.Thetypeconcepthasonlylimiteduseinmodernbiologyandisbeingreplacedbythestudyofvariationaccordingtopopulations.
Theseconclusionsandideashaveanimportantrelationshiptohumanaffairs.Freshfromusingthetypemethodtoclassifyanimals,manybiologistsinpastgenerationsthoughtofthehumanracesintermsoftypes.Aswehavepointedoutabove,thetypeconceptisausefulonewhereverasinglemajorcauseconsistentlyproducesseveraleffects.Theearlierclassificationofhumanraceswasbasedontheideaofonemajorcauseproducingskincolorandallotherassociatedcharacteristics,notonlyphysicalbutculturaltraitsaswell.Themodernstudyofracesaspopulationsshowsthateachgroupisenormouslyvariableinitself,andthatpopulationsunlikeinmanyrespectsmayhavethesameskincolor.Inthosegeneticallydeterminedcharacteristicswhichcanbe
sameskincolor.Inthosegeneticallydeterminedcharacteristicswhichcanbemeasured,suchasbloodgroups,humanpopulationsdifferintheaveragedistributionofcertaingenes,butthedifferencesbetweenaveragesareusuallysmallcomparedtothedifferencesbetweenindividualswithinthesamepopulation.
Whatdoesthismeanintermsofinterpretinghumanbehavior?Itdoesnotmeanthatphysicaldifferenceshavenoeffectonbehavior,butsimplythatthesedifferencesareofasimpleandunderstandablenature.AmericanNegroeshaveontheaveragelongerlegsinproportiontothetrunkthandoAmericanwhites(McKusick,1960).Onewouldexpectthatontheaveragetheymightbebetterperformersinjumpingandrunning,asindeedtheirperformanceinrecentOlympiceventswouldindicate.Inthecaseofskincolor,thereisnoevidencethatithasanyeffectotherthanwhatmightobviouslybeexpected,namely,thatNegroesendureseverephysicalexertionbetterinahotmoistclimatethandowhitepeople,presumablybecausetheyareabletoradiatebodyheatmorerapidly(Baker,1958).Alltheevidenceisagainstanyassociationbetweenskinorhaircolorandbehavioraltraitsotherthantheabove.Wherevercomparableintelligencetestscanbegivenunderconditionsofequalopportunity,therehavebeennodifferencesbetweendifferentraces(Anastasi,1958).Thekindsofbehavioraldifferenceswhichwenowfindbetweenpopulationsreflectthecombinedeffectsofculturalandenvironmentaladvantages.WeshouldrememberthatcivilizationsofatypeatleastcomparabletothoseofBabylonandEgyptwereinexistenceintheNewWorldwhenColumbusdiscoveredit.Atwo-thousand-yearstartgaveatremendousadvantagetotheolderculturewhenthetwocameintocompetition,butallindicationsarethatanotheradvancedcivilizationwouldhavebeendeveloped
PHYSICALDIFFERENCES355
onthiscontinentifithadbeenleftaloneunderfavorableenvironmentalconditions.Thereislikewiseeveryevidencethathumanbeingswholiveunderextremelyunfavorableenvironmentalconditionssuchasthefarnorthorthetropicsarebasicallyjustascapableasthosecomingfrommoretemperateregions,butthatthesevereenvironmentprovidesastronghandicaptothedevelopmentofthesecapacities.
Inshort,alltheweightofmodernscientificevidence,bothfromdirectstudiesonhumanbeingsandfromanimalstudiessuchasthisone,isonthesideoftheconclusionthatthehumanraceisdividedintopopulationsratherthantypes.Thesepopulationsarebecominglargerandlargerastheyabsorbformersmall
Thesepopulationsarebecominglargerandlargerastheyabsorbformersmalllocalpopulations,andasevenlargecontinentalpopulationsbegintomergewitheachother.
Indealingwithindividuals,whethertheyaredogsormen,weneedtorememberthateachisauniquecollection(orpopulation)ofgenetictraits,notatyperepresentingarace.Likewise,indealingwithagroup,weneedtorememberthatwearedealingwithapopulation:agroupofvariableindividualsratherthanasingletype.
THEEFFECTSOFHEREDITYUPONTHEBEHAVIOROFDOGS
Sofarinthisbookwehavebeenconsideringtheresultsofindividualtests,manyofthemespeciallyselectedforanalysisbecausegeneticsappearedtobeimportantanditsmodeofactionreadilyexplainable.Inthischapterweshallconsideralltheteststogetherandsoobtainanover-allandreasonablyunbiasedviewpoint.Thiswillgiveusinformationonthreeprincipalpoints:generalevidencefortheexistenceofMendeliansegregation,evidencefortheextenttowhichheredityaffectsbehavior,and,finally,evidencefortheexistenceofspecificandgeneralbehavioraltraits.
GENERALEVIDENCEOFSEGREGATIONANDDOMINANCE
Thedetailedanalysesofindividualtestshaverevealednumerouswaysinwhichcomplexinteractionsonthebehaviorallevelcanmodifytheexpressionofhereditaryvariation.Nevertheless,onthebasisofMendeliantheory,onewouldexpectgreatervariationinthehybridpopulationsinwhichsegregationwouldoccur,thanintheFiandparentalpopulations.Inordertogetanover-allpicture,wecombinedtheresultsfromthecockerspanielandbasenjibreedsandthetwoFihybridsinonepopulation,andcombinedthosefromthetwobackcrossesandthetwoFi>generationsinanother.Eachofthetwopopulationswasthuscomposedoffoursubpopulationshavingapproximatelyequalnumbers.Oneofthemincludedallthesegregatinghybrids,andtheotherallthenon-segregatingpopulations(Table14.1).
356
EFFECTSOFHEREDITY
TABLE14.1CompositionofCombinedPopulations
357
Threestatisticaloperationswereperformed.Inthefirst,thesub-populationsweresimplycombinedandthetotalvariancecalculated.Inthesecond,onlythevariancewithinpopulationswascombined;andinthethird,onlythevariancewithinlitterswascombined.Thelastshould,ofcourse,giveusthebestpictureoftheeffectsofsegregation,sincewithinalittertheeffectsofrandomvariationinenvironmentalfactorsaregreatlyreducedandtheeffectsofaccidentalselectionofdifferentsortsofparentsareeliminated.Within-populationvarianceshouldincludemoreenvironmentaleffects,aswellaseffectsofdifferencesbetweenstrainswithinapopulation,whilethetotalcombinedvarianceofallthesubpopulationsincludesvariationfromallsources,includingthatfromdifferencesbetweenthesubpopulationsthemselves.
IfidealMendelianpopulationshavingequalnumbersarecombinedintheaboveways,thereshouldtheoreticallybenodifferenceinthemeansbetweenthesegregatingandnon-segregatingpopulations,whetherornotdominanceispresent.Actually,therewerealargenumber(26outof44)ofsignificantdifferencesbetweenthetwo.Thisresultmayinpartbeduetothefactthatthecomponentpopulationswerenotactuallyequalinnumbers,anditalsomayberelatedtoaccidentalselectionofdifferentindividualsfortheparentanimals.
Withregardtovariation,thetheoreticalgeneticvarianceofthecombinedparentandFipopulationsshouldbegreaterthanthatofthecombinedsegregatingpopulations,47percentlargerinthecaseofnodominanceand18percentinthecaseofdominance.Theactualfigures(Table14.2)indicatethatthevarianceofthenon-segregatingpopulationswasgreaterinslightlyoverhalfofthevariables.Thissmallexcesswouldarguethatdominanceisacommonphenomenoninthesevariables.
Ontheotherhand,thetheoreticalwithin-populationgeneticvarianceofthenon-segregatingpopulationsshouldbezero,while
DIFFERENTIALCAPACITIES
TABLE14.2
NumberofVariablesinWhichtheCombinedVarianceofSegregatingPopulationsExceedsthatofNon-segregatingPopulations
thatforthesegregatingpopulationsshould,onascaleof1.0,average.083inthe
thatforthesegregatingpopulationsshould,onascaleof1.0,average.083inthecaseofnodominanceand.146inthecaseofdominance.Eitherthevariancewithinpopulationsorthevariancewithinlittersshouldshowanimportantincreaseinthesegregatingpopulations.AglanceatTable14.2indicatesthatthisisindeedthecase.Asweprogressfromthecombinedtotalvariancetothewithin-littervariance,thereisanincreaseinthenumberofvariablesinwhichthesegregatingpopulationsaremorevariablethanthenon-segregatingones.Theratioof31to13issignificantlydifferentfromthatexpectedbychance(P=.005).Thisratioisapproximatelythesameinthevariableswhichshowsignificantdifferencesbetweenthebackcrossesandhenceshowimportantdifferencesbetweenthetwoparentbreeds.
Thustheover-allevidenceisconsistentwiththeassumptionthatMendeliansegregationincreasestheamountofvariationinhybrids,althoughthismaynotbetrueincertainindividualmeasurementssubjecttospecialbehavioralinteractions(seechap.12).Likewisethereissomeindirectevidencethatdominanceisprobablyacommonphenomenoninthisdata.
THEIMPORTANCEOFGENETICVARIATION:RESULTSOFANALYSISOFVARIANCE
Fromtheverystartwerealizedthatevenwithinpurebreedstherewasagreatdealofvariationbetweenindividuals,andouroriginalmatingplan,describedinchapter1,wasintendedtominimizeindividualgeneticdifferencesbyfirstdevelopingstrainsbasedontheoffspringofasinglematingand,second,bycrossbreedingbetweenindividualscomingfromasinglematingineachoftwopurebreedingstocksthusdeveloped.Thisplanshouldhavehadtheeffectofreducingvariationduetoindividualdifferencesrelativetovariationbetweenbreeds.Thisfactshouldbekeptinmindininterpretingtheresults.
EFFECTSOFHEREDITY359
WiththehelpofDr.GuntherSchlagerandtheJacksonLaboratoryBiometricService,wemadeanextensiveanalysisofvarianceofthe50variablesusedinBrace's(1961)factoranalysis.Foreachofthesevariables,thevariancewascomputed:(1)betweenbreedsorhybridpopulations,(2)betweenlitterswithinpopulations,and(3)withinlitters.Thefirstofthesecomponentscanbeassumedtobelargelygenetic,aseveryeffortwasmadetorearallbreedsunderuniformconditions.Likewise,thethirdcomponentofwithin-littervarianceshouldreflectalargeamountofgeneticvariation,thatbetweenindividuals.Sinceallmembers
alargeamountofgeneticvariation,thatbetweenindividuals.Sinceallmembersofalitterunderwenttestingatthesametimeandhadverysimilarenvironments,itcanbeassumedthatthispartofthevariancehasalargegeneticcomponent.Ontheotherhand,thebetween-littervarianceshouldincludealargepartoftheenvironmentaleffects,especiallywhererepeatedlittersfromthesamematingweretested.Wheredifferentmatingsareinvolved,italsoreflectsgeneticdifferencesbetweentheparents.
Thesecomputationsweremadeforallpurebreeds,thetwoparentbreeds(cockersandbasenjis),thetwoFi's,thetwobackcrosses,andthetwoF2's(Table14.3).Sixofthevariablesweredistributedinadichotomousfashionsothatvarianceestimatescouldnotbemade.Inthesecases,thechi-squareanalysiswasusedtomeasuretheimportanceofdifferencesbetweenpopulations.
Afurtherandmoredetailedanalysiswasdoneforselectedback-crossandF2populations.Intheseselectedgroupsthereweretwolittersfromeachoftwomatingsineachpopulation.Theparentsineachcasewerebrothersandsistersfromthereciprocalcrosses,sothatthewholegroupwasdescendedfromfoursiblingbasenjisandfoursiblingcockerspaniels.Inthesepopulations,thebetween-littervariancecouldbeseparatedintoabetween-matingcomponent(largelygenetic)andabetween-litter-within-matingcomponent(largelyenvironmental).
Sincelittersizeswerevariable,variancecomponentswerecomputedaccordingtothemethodofGower(1962).Inthismethod,thewithin-littervariancevalueisassumedtobecorrect,buttheremainingtwocomponentsarecalculatedwithsomedegreeofapproximation.Themethodtendsthereforetoslightlyreducetheestimatesofbetween-breedandbetween-littervariance;thatis,theseareconservativeestimates.
Thegeneralresultistogiveusestimatesoftherelativeimportanceoftwolargelygeneticcomponents,between-breedandbetween-mating,wherethelatterissomewhatminimized.Italsogivesusa
360DIFFERENTIALCAPACITIES
TABLE14.3ProfortionofVarianceAttributabletoPopulationDifferences
Variable
All
Pure•BreedsBA&CS
Fi's
Back-
F:'s
SelectedBack-SelectedcrossesFi's
PhysicalMeasurement:
Weight27**
Bodvlength59**
Shoulderheight52**
Chestcircumference.Waistcircumference.
Brisketdepth
Chestbreadth27**
Femurdiameter0*
Humerusdiameter21**
Thighcircumference16**
Mean
Physiological-Emotional(HeartRates):Averagerate,11-16weeks
Adultrate
Change,quieting
Change,bellringing
Arrhythmiaindex
Mean.
Emotional:
Distressvocalizationwhileweighed,1-4weeks
Activityinconfinement
Responsestostimulationduringreactivitychange,aloneandwithexperimenter
Activityduringbellringing....
Posture
Musculartremor
Vocalization*1
Investigativebehavior
Escapeattempts
Mean.
Socialrelationships:Withhumans:
Avoidanceandvocalization,
5weeks
Playfullighting,13-15weeks..Approachandfollowing,13-15
weeks
Withdogs:
Dominancescored
Mean
Trainability:
reedtraining:
Inactivitywhileweighed,5-weeks'1
16
27
39*46*27*10*66*
5^
26*
13*
134*14*44*
24*
28*
25
29**
15**
18**
21
42**76**82**37**21**65**27**4*58**19**
43
27*37*42*11*0
23
24*
8*11*43*
0
46*56*
25
59<
45
18*11*62*
2*48**11
0
315*
0
17
016*
29*
50
22*
11*
7
11
5*33**53**21**11**33**
0
0
021**
18
24**17**16**18**0
15
0
0
0
40*
13*29*
in
24**10
30**
:i
oo
30*
TABLE14.3—Continued
EFFECTSOFHEREDITY
361
d—dichotomousdistribution,variancecomponentsnotcalculated.
pictureofthechangeindistributionofthebetween-breedcomponentasaresultofhybridization.
ofhybridization.
Resultswithfivepurebreeds.—AsTable14.3shows,thereisonlyonevariableoutofthe50whichdoesnotshowsignificantdifferencesbetweenthebreeds,atleastonthe5percentlevel.Thegreatmajorityofthedifferencesaresignificanttofarbeyondaprobabilityof.01.Sincethesevariableswereselectedtorepresentallimportantbehavioraltests,itisobviousthatbreeddifferencesinbehaviorarebothrealandimportantinmagnitude.
Withrespecttotherelativeamountsofbreeddifferences,thesevaryfromzeroto66percentofthetotalvariance.Thelargestbe-
362DIFFERENTIALCAPACITIES
tween-breedcomponentoccursinthearrhythmiaindex,producedalmostentirelybythefoxterrierbreed,whichishighlydifferentfromalltheothers.Anearzeropercentageisfoundinthevariableofchangeinovertactivityduringthereactivitytest,butonlyinthepartinwhichthedogisleftaloneandlatercomforted.Thecomputationsalsoreduceasmallbutsignificantdifferenceinoneofthephysicalvariables(femurdiameter)tozero.
Asshownattheendofthesametable,theportionofvarianceattributabletobreeddifferences(comparabletotheintraclasscorrelationfiguresinpreviouschapters)averagesapproximately27percentforbothphysicalandbehavioralvariables.Evenifthephysiologicalmeasuresareomitted,theremainingbehavioralvariablesstillaverage25percent.Wecanconcludethatbehavioraldifferencesbetweenthefivepurebreedsareasimportantasdifferencesinphysique,eventhoughphysicalmeasurementsareusuallyconsideredtobemoreaccuratethanbehavioralones.
Resultswithbasenjisandcockerspaniels.—Asmightbeexpected,therearefewersignificantdifferencesbetweenthesetwoparentbreeds(Column2,Table14.3)thanwhenallfivebreedsareconsidered.Onenotableexampleisthatofthearrhythmiaindex,inwhichthereisnodifferencebetweencockersandbasenjisoranyoftheirhybrids.Nevertheless,therearestill35outof50variableswhicharesignificantlydifferentatthe.01levelorless.Thesetwobreedsareobviouslydifferentfromeachotherinmanyrespects.
Indeed,certainofthebetween-breedvariancesevenexceedthosecalculatedforallfivebreeds.Thoseforleashfightingandrunningtimeonthelongbarrierofthedetourtestare77and78percentrespectively.Almostallthephysical
thedetourtestare77and78percentrespectively.Almostallthephysicalvariablesarehigher,thatforheightbeing82percent.Nevertheless,thereisagreatdealofindividualoverlapbetweenthetwoparentstocksinmostofthevariables,eventhosewhichshowthegreatestdifferences.Thisoverlapmightbecausedeitherbyenvironmentalvariationorbygeneticvariationwithinthebreed,aquestionansweredbyfurthercomputationsdescribedlaterinthischapter.
ResultswiththeF\sandF/s.—Differencesbetweenthereciprocalcrossesinthesetwopopulationscouldbecausedbyaccidentalselectionofdifferentparents,Inmaternalinheritance,orbysex-linkedinheritance.Asshowninanearlierchapter,thereisnoevidencethatsex-linkedinheritanceaffectsanyofthevariables,and,indeed,thisisnotsurprising.Thereare39pairsofchromosomesinthedog,andthereforethechanceoffindingagenecarriedbytheXchromosome
EFFECTSOFHEREDITY363
isquitesmall.Maternalinheritanceisalikelypossibilityonlyinthecaseofapproachingandfollowingbehaviorexhibitedtowardahumanhandler,whereboththeFi'sandFu'sshowlargedifferencesandwherethereisalogicalmeansofpassingonatraitfromgenerationtogenerationbyfollowingthematernalexample.
TherearemanymoredifferencesbetweenthereciprocalFicrossesthanwouldbeexpectedpurelybychance.Outof50variables,2.5wouldbeexpectedbychanceatthe.05level.Actually,20variablesshoweddifferencessignificantatthe.05levelorless.Sincetwoofthethreealternativeexplanationslistedabovehavebeeneliminated,thereremainsthepossibilitythatthedifferencesbetweentheF/swerecausedbyaccidentalselectionoftheparents.ThisisespeciallylikelywherethedifferencesbetweentheFi'sareoppositefromthoseintheparents,asinallsixofthephysicalmeasuresandthreeofthebehavioralmeasures.Theresultsthereforeindicatethatindividualgeneticvariationwithinabreedisimportant.
However,thenumberofdifferencesbetweenthereciprocalcrossesisgreatlyreducedintheF2generation,therebeingonlysixdifferencessignificantat.05orless.SomeofthisreductionisundoubtedlyproducedbyselectionofasmallnumberofFiparentsfromtheoffspringoftheparentsselectedinthepreviousgeneration,whichwouldhavetheeffectofdecreasingvariation.Itisalsopossiblethatsomebreedcharacteristicsarefullydevelopedonlyinthematernal
possiblethatsomebreedcharacteristicsarefullydevelopedonlyinthematernalenvironmentofthepurebreeds;thatis,thedevelopmentofbreedcharacteristicsmayinpartdependuponanenvironmentproducedbyassociationwithmembersofthesamebreed.Forexample,foxterriermothersappeartobeconsiderablymoreaggressiveduringweaningthandoothermothers,andthismayaidinthedevelopmentofexcessiveaggressivenessamongtheirpups.Thisgeneralpossibilityisreinforcedbythefactthat11outofthe14significantdifferencesinbehaviorareinthesamedirectionasdifferencesbetweenthepurebredparents.
Resultsfromthebackcrosses.—Inthesepopulations,geneticsegregationtakesplace.Theresultisthatgeneticvariationisredistributed,beingdecreasedbetweenpopulationsandincreasedwithinpopulations.Onanytheoryofinheritanceinvolvingonesetofalleles,thereshouldbedifferencesbetweenreciprocalbackcrosses.Selectingthosevariableswhichshowhighlysignificantdifferencesshouldthereforegiveagroupofvariablesinwhichthebetween-breedcomponentisgreatest.Thenumberofvariablessignificantat.01isreducedfrom35intheparentstrainsto27inthebackcrosses,andfor
364DIFFERENTIALCAPACITIES
themostpartthevariablesshowingmostsignificantdifferencescorrespondtothosewhichshowedthemaximumdifferencesbetweentheparents.
Therearethreeexceptions.Oneoftheseistheaverageerrorscoreinthemazetest.InthisvariablethereisalargedifferencebetweenthetwoFi's,butnodifferencebetweenthetwopurebreeds.Thesignificantdifferencebetweenthebackcrossesprobablyresultsfromaccidentalselectionofparentswhicharedifferentfromthebreedaverages.Thesecondexception,tremorduringthereactivitytest,hasthesameexplanation.Finally,thereistheerrorscoreintheT-maze,forwhichthereisnoobviousexplanationexceptthattheoriginalsimilaritybetweentheparentstrainsmayhavebeenproducedbydifferentgeneswhichsegregatedseparatelyandthusproduceddifferencesbetweenthebackcrossgenerations.
ResultsfromselectedbackcrossesandF2S.—Intheabovecalculationsitisimpossibletodifferentiatebetweenthebetween-matingvarianceandthebetween-littervariancewithinmatings,asvariousaccidentspreventedourobtainingrepeatedlittersfromeverymating.Thefollowingcalculationsarebaseduponaselectedgroupofmatingsinwhichitwaspossibletoobtaintwolittersfromeach.Theoriginalparentswereallobtainedfrombasenjimating4andcockerspanielmating7,sothatdifferencesbetweenthematingsrepresent
andcockerspanielmating7,sothatdifferencesbetweenthematingsrepresentgeneticdifferencesbetweensiblings.
DescendantsfromthesefourmatingsproducedtwolitterseachinthebackcrossandF2generations,sothatforeachpopulationtherewerefourlittersand19to21animals.Itisthereforepossibletomeasurethevarianceproducedbydifferencesbetweenmatingsinadirectmanner.ItshouldberecalledthatinthebackcrossandF2generations,thevarianceduetosegregationismaximized,producingalargeamountofwithin-littervariance.Thedifferencesbetweenmatings,however,shouldnotbeaffectedbysegregationbutonlybyaccidentalselectionandsmallnumbers.
AsseeninTable14.3,thenumberofsignificantdifferencesbetweentheselectedpopulationsisstillfurtherreducedbecauseofthereductioninnumbersandtherestrictionofdifferencesbetweenmatings.Thevariableswhichstillshowsignificantdifferencesarethesameasthevariableswhichshowedthelargestdifferencesbetweenthebackcrosses,withthreeexceptions:theconfinementtest,thetrailingtest,andthespatial-orientation-persistencetest.Thesethreeshowsignificantdifferencesbetweenthepurebreedsbutnotbetweenthetotalbackcrosses.Thefactdiattheselectedbackcrossesaresignificantlydifferentprobablyresultsfromanaccidentalselec-
EFFECTSOFHEREDITY
365
tionofparentswhichshowedgreaterdifferencesthantheaverage.Thereshouldbeaslightlyhigherproportionofwithin-littervarianceintheF2'sthaninthebackcrosses,becauseofreductioninthelatterofageneticvariationduetodominance,andthisinfactistheresult.AsseeninTable14.4,thewithin-littervarianceineachF2populationisgreaterthaninthecorrespondingbackcrosspopulation.
TABLE14.4VarianceComponentsofEachSelectedBackcrossandF2Population
Population
BetweenMatings:BetweenLitters
WithinLitters
WithinLitters
MeanVarianceComponentsof10PhysicalMeasures,inPercentages
MeanVarianceComponentsof34BehavioralMeasures,inPercentages
Thebetween-matingvarianceaveragesapproximately12percentonbothphysicalandbehavioralvariables.Thebetween-litter-within-matingvarianceisveryclosetothesameamount.Itshouldberecalledthattheformerrepresentsgeneticdifferencesbetweenbrothersandsistersratherthanarandomsampleofthebreedandisthereforeaminimumestimate.Itmustbeconcludedthatgeneticdifferenceswithinbreedsareimportant.Ifwecomparetheseresultswiththosefromthepurebreeds,about75percentofthevarianceoccurswithinbreeds,includingabout21percentduetodifferencesbetweenlitters.Ifweassumethatone-halfofthelastfigure,or10.5percent,iscausedbydifferencesbetweenmatings,thefiguresarequitecomparable.
InTable14.5thevariancecomponentsofcertainselectedvariablesshowingthegreatestdifferencesbetweenthebackcrossesareshown.Ontheaverage,thereisnodifferenceintherelativesizeofthevariancecomponentsbetweentheseandthetotalofallvariables.Thereare,however,greatindividualvariationsbetweenthetests.Forexample,heightshowsalmostnobetween-matingvariance,
DIFFERENTIALCAPACITIES
TABLE14.5
MeanVarianceCo^iponentsemVariablesShowingDifferencesbetweenthebackcrosseswithap<.01
Variable
Bet'.veenMatings
BetweenWithin
Litters
Height
Ave.heartrate,11-16weeks
Adultheartrate
Heartratechange,quieting
Heartratechange,bellringing
Activityinconnneraent
Musculartremor
Approachandfollowing,13-15weeks.
Leashlighting
Finalrunningtime,longbarrier
Vocalization,U-shapedbarrier
Trailing
T-maze,motivation
T-maze,errors
Meantotal.
11
12
whereasinfantileheartrateshowsagreatdeal.Thiswouldmeanthatintheselectedsample,parentswereaccidentallychosenthatwereuniforminheightbutvariableinheartrate,althoughitwillberecalledthatinthetotalsampletherewasagreatdealofparentalvariationinheight.
Inthecaseofapproachandfollowing,thereisnobetween-littervariancewithinmatings.This,itwillberecalled,isavariableinwhichmaternalinheritanceisalikelvpossibilitv.IntheT-mazeerrorscore,whichisoneinwhichtheparentpurebreedsshowednodifferences,thereisalargebetween-matingvariance.Inthiscasetherewasprobablyaccidentalselectionofdifferentsortsofparentanimalsfromthetwobreeds,althoughthebreedsthemselvesaresimilarontheaverage.Finally,intheleash-fightingtestalargebetween-matingcomponent
average.Finally,intheleash-fightingtestalargebetween-matingcomponentconfirmsconclusionsfromthedetailedanalysisofthistestinchapter12.
Conclusions.—Reviewingthiscomplexmaterial,wecancometocertainfirmconclusions.Oneisthatthedifferencesbetweenbreedsareimportant,bothinphysicalmeasurementsandbehavioralmeasurements.Thevarianceaveragesbetween25and30percentofthetotalandrangesashighas66percent.Inonlvonebehavioraltestandonephysicaltestarebreeddifferencesestimatedasbeingclosetozero.
Atthesametimethereisagreatdealofoverlapbetweenthebreeds.Althoughthisoverlapisinpartcausedbyrandomenvironmentalfactors,itliasasubstantialgeneticcomponent.Thegeneral
EFFECTSOFHEREDITY367
picturewhichemergesfromthestudvisthatinmosttraitsthereareaveragebreeddifferences.Takinganytwobreedsatrandom,onewouldexpectalargenumberofsignificantdifferencesbetweenmeanscores.However,therearegenetieallvoverlappingindividualsineachoftiiesebreeds,sothatinmanytraitsonebreedcouldbemadeliketheotherwithinaveryshorttimebyselection.Thismeansthatthedogbreedshaveretainedagreatdealofgeneticflexibility.
Forexample,fightingtheleashischaracteristicofbasenjisandisshownbvnocockerspaniels.Nevertheless,thereareafewbasenjiswhichlackthistrait,anditwouldbepossiblebvselectiontoproduceastrainverymuchlikecockersinthisrespect.Thistypeofgeneticoverlapisnotnecessarilvreciprocal,asitwouldprobablybemuchmoredifficulttoselectcockersintheoppositedirection.
Inafewcasesselectionhasapparentlyproducedtraitsforwhichcertainbreedsarevervnearlygenetieallvhomozvgous,suchasthelowcapacityfordevelopingfightingbehaviorinthehoundbreedsandthehighcapacitvforthesametraitintheterrierbreeds.Suchinstancesare,however,relativelyrare.
Withinabreed,individualcapacitiesarelikelytobehighlyvariable;butmostindividualsmaybeabletoperformthetasksrequiredofthembvbringingdifferentcapacitiesintoplay.Outstandingperformerswithinabreedprobablyhavespecialcombinationsofcertaincapacitieswhicharelargelytheresultofaccidentalselection.
EVIDENCEFORTHEEXISTENCEOFGENERALTRAITS:RESULTSOFFACTORANALYSIS
Alternatetheoriesofinheritance.—Wehavenowconfirmedtherealityofalargenumberofdifferencesbetweenthebehaviorofbasenjisandcockerspaniels.Thebasenjishadatendencytofighttheleash,toshowagreatdealofplayfulaggressiveness,andtobehighlyfearfulasyoungpups.Incontrast,thecockersalmostneverfoughttheleash,hadlesstendencytoplayfullyfightandchewontheirhandlers,andshowedverylittlefearasyoungpuppies.Wemightsupposeeitherthatallofthesedifferencesarecausedbvonebasicbehaviortrait,orthateachoftheseisaspecialtraitandunrelatedtotherest.Ifthefirsttheoryistrue,thenthetestresultsshouldbecorrelatedeveninthesegregatinghybridgenerations.Ifthesecondtheoryiscorrect,thetestresultsshouldshowlittleifanycorrelation.
Thetraitsare,ofcourse,correlatedintheoriginalpurebreeds,nomatterwhatthegeneticsituationmightbe,andafewindependenttraitsmightbecorrelatedeveninthesegregatinggenerationsif
368DIFFERENTIALCAPACITIES
theywerecausedbytwogeneswhichareclosetogetheronthesamechromosomeandhencecloselylinked.However,sincethedoghas39differentpairsofchromosomes,thechancesofcloselinkagearenotverygreat.
Thetheoreticalresultisalsocomplicatedbythefactthataparticularbehaviortraitmightbecausedeitherbyasinglemajorgeneorbyseveralgeneswithminoreffects.Thefirstconditionwouldproduceverystrongcorrelationsbetweentests.Thesecondcouldproducesuchcorrelations,butonlyiftheeffectsofminorfactorswereadditive.Ifaparticulartraitisproducedonlybyaspecialcombinationofgenes,itwilldisappearduringsegregationandbefoundonlyinaverysmallnumberofindividuals,notenoughtoproduceanystrongcorrelation.Forexample,ifatraitwasproducedbyacombinationofthreerecessivegenes,thiscombinationwouldappearintheF2generationinonlyoneoutof64individuals.Inanycase,onewaytotestthesevarioustheoriesisthroughanalysisofcorrelations.
Thetheoryoffactoranalysis.—Dr.JosephRoyce,whowasatthetimewebegantheseexperimentsagraduatestudentworkingwiththelateProfessorThurstone,stronglyadvocatedtheuseoffactoranalysisonourdataandhas
Thurstone,stronglyadvocatedtheuseoffactoranalysisonourdataandhaspresentedthetheoryinvolvedinseveralpapers(1950,1957,1963).Ifthehypothesisofbasicgeneraltraitsiscorrect,factoranalysisshouldgiveaclear-cutindicationofthenatureofthesetraitsandofthesituationsinwhichtheyappear.Themethoddoeshaveonelimitation.Sinceitisbasedoncorrelations,itwillworkonlywherethebasicmathematicalassumptionsofcorrelationaremet.Theseassumptionsarethatcausalfactorsproducecertainspecificeffects,andthattheseeffectsareadditiveanddistributedinnormalcurves.
Thefactorialmethodhasprovedveryusefulinanalyzingtheresultsofhumanintelligencetests.Eachtestscoreistheresultofaddingtogetherseveraltestitems.Itthereforefulfillsthecriterionofadditiveeffects.Sincemanyintelligencetestsweredesignedbydevisinganumberofquestionsandproblems,andafterwardselectingthosetowhichstudentsgavedifferentanswers,theoriginalintelligencetestswereamixtureofmanydifferentsortsofquestions.Thefactorialmethodwassuccessfullyusedtosortoutthecommonfactorsinvariousquestionsandtoproducetestswhichcouldbeinterpretedintermsofspecialcapacities.ThurstoneandStrandskov(Strandskov,1953)testedthehypothesisthatthesepurifiedtestsrepresentedbasicgeneticdifferencesincapacitiesbygivingtheteststoidenticaltwinsanddeterminingthecorrespondencebetween
EFFECTSOFHEREDITY369
them.Inmostcasesthecorrelationswerelow,indicatingthathereditywasnothighlyimportantindeterminingthesecapacities,althoughsomeofthemorestrictlyphysiologicaltestsshowedhigherresemblances.Judgingfromtheevidenceontransferoftraining,whichindicatesthatpeopleareabletotransfermateriallearnedononesituationonlytocloselyrelatedsituations,itisprobablethatthefactorsobtainedbyThurstonerepresentproblemswithacommonrecognizablesimilarityratherthanproblemssolvablebyasinglecommoncapacity.Aswehaveseenfromtheresultsofperformancetestswithdogs,manycapacitiesmaybeinvolvedinthesimplestperformancetest,andanimalscanorganizethesecapacitiesinvariousways.
Afactoranalysisofemotionalandphysiologicaltests.—Rovce(1955)didafactoranalvsisoftestsmadeon53purebreddogsdistributedinsixdifferentbreeds.Thirty-twovariableswereincludedintheanalysis.Thesevariableswereobtainedfromonlyfivedifferenttestsituations,andsomeofthemwouldbeexpectedtobecorrelatedsimplybecausetheyoccurredinthesametest.Thebasiccorrelationtable,however,showsmanymorecorrelationsthanmightbe
basiccorrelationtable,however,showsmanymorecorrelationsthanmightbeexpectedfromthissourcealone.Ofthe396correlationsofunrelatedtests,85weresignificantatthe.05level,asopposedtothe19.8whichmightbeexpectedbychance.Realcorrelationsbetweenthedifferenttestsmustexist,althoughthesemaybecausedbythefactthattheanimalstestedbelongedtopurebreedsandhencehadcommontraitsproducedmerelybybreedselection.Rovcewasabletoidentifyseveralfactors,twoofwhichwerehighlyphysiological.Onewascharacterizedbyhighbloodpressureandarrhythmicheartbeatandmayhavebeenassociatedwithemotionalreactionsoftimidity.Thesecondshowedahighdegreeofchangeinheartratetosocialstimulation,associatedwithahighdegreeofexternalactivity.Fourfactorswerelargelybehavioral.Inoneofthese,therewerehighloadingsforbothplayfulaggressivenesstowardhumanhandlersandconfidencewhilebeingweighed.Asecondwascharacterizedbyahighdegreeoftimidityinreactiontopeople,alongwithsomeemotionalreactions.Athirdtestincludedahighdegreeofreactiontothenoiseofabellringing,andafourthwascalledgeneral-activitylevel.
Oneofthemostinterestingresultswastheindicationthattimidityandaggressivenesswerenotoppositeendsofthesamecontinuumbutwerefoundindifferentfactors.Theresultsalsoindicatethatthereareseveraldifferentkindsoftimidityandthusargueforthetheoryofhighlyspecificeffectsofgenes,butsinceanyofthefac-
torsmighthavebeencausedbyaccidentalbreedassociation,thislastconclusionisnotafinalone.
Rovce'sfactoranalvsisenabledustoselectcertainvariableswhichseemedtohaveimportantgeneraleffectsandtoeliminateotherswhichseemedtobeeitherinconsistentorspecific.Thusthetestingprogram,andparticularlythescoringofcertaintests,wascon-siderablvimproved.Anotherresultwasthedemonstrationthatthesametestscoresgivenatdifferentagescameoutindifferentfactors.Thetimiditv-confidenceratingonthefifthweek,orfirsttesting,appearedtobelargelvindependentoftheaverageratingsobtainedfrom5to10and11through16weeks.Thelasttwo,however,wereconsistentlvassociated.
Factoranalysisofperformancetests.—AnastasiandSchmidt1955),didasimilarpreliminaryanalvsisofperformancetests.Thedogstestedincludedallfivepurebreeds,totalingsome50animals,plus23oftheFihybridsbetweenthecockersandbasenjis.ThegrouptestedwasthereforesomewhatsimilartothatusedbvRoyce.Theresultsofeightdifferenttestsituationswereincluded,butseveraloftheseincludedmorethanonescore,makingatotalof17variablesto
severaloftheseincludedmorethanonescore,makingatotalof17variablestobeanalyzed.ThemethodwasthesameasthatusedbyRovce,thecentroidmethod.
Theanalysisproducedfivefactors.Oneofthesewasclearlva"test"factor,involvingtwoscoresfromonetest,andmeantlittleelsethanthatthesetwoscoresweresimilartoeachother.AnotherfactorchieflvincludedthreescoresindicatingpoorperformanceontheT-mazetest,plusscoresassociatedwithgoodperformanceonthesecondbarrier(maze)test.SincetheprincipalcauseoferrorintheT-mazeisatendencvtoalwaysruntothesamesideandthusshowpositionpreference,thisfactorwascalled"persistenceofpositionalhabits."Itisinterestingthatalaterdetailedanalysisofthesecondbarriertestrevealedbreeddifferencesinthetendencytoformsuchhabits,thebeaglesbeingquitedifferentfromtherestofthebreedsinbeingslowtoformfixedhabits.
Theotherfactorswereinterpretedaslargelvemotionalratherthanintellectualinnature.Factor1wascalled"impulsiveness*;Factor2,"docility":andFactor4,"visualobservation."
Someofthedifferentscoresonthesametestsituationappeared
indifferentfactors,particularlythoseonthebarriertest,butinmost
fromonetestappearedinthesamefactor.Onthis
swecouldselectthemostimportantscorefromeachtestfor
detailedanalysisandfuturework.
Whetherthesefactorsweretheresultofthecorrelationsarising
EFFECTSOFHEREDITY371
fromselectionofbreedtvpes,orwhetherthevrepresentedgeneralbehaviortraitsindogs,wasnotapparentfromtheresults.
Consideringthetwopreliminaryanalysestogether,itlookedasthoughitmightbepossibletoaccountformostofthedifferencesindogbehavioronthebasisofafewemotionalandtemperamentaltraitshavinganeffectonperformanceaswellasonemotionalexpression.Thetestofthistheorywastocombinebothemotionalandperformancetestsinasinglefactoranalysisandtofurther
emotionalandperformancetestsinasinglefactoranalysisandtofurtherdeterminewhetherornotthesecharacteristicswerereallybasictraitsbyapplyingfactoranalysistothesegregatinghybridsaswellastothepurebreedsandFihybrids|Brace,1961.
Ageneralfactoranalysis.—Brace'sextensivefactoranalyseshavealreadvbeendescribedinchapter13inconnectionwiththeeffectofphysiqueonbehavior.Braceusedthe40behavioraland10physicalvariableslistedinTable14.3asabasisforseparatefactorialanalysesoneachofthepurebreedsandeachhybridpopulation,aswellasonseveralcombinedgroups.Ofthese,resultsfromtheF?'sweremostimportant,sincethevwerebasedonthelargestnumbersandonthepopulationwheremaximumeffectsofsegregationmightbeexpected.
ItwillalsoberecalledthatallthephysicalmeasurementscameoutasasinglefactorofgeneralsizeintheF2generation,indicatingthattherewasnogeneticbasisforphysicaltypes.Inbothcockerspanielsandbasenjis,however,thephysicalmeasurementsdidappearintwofactors,indicatingthattherewerelong-andshort-bodiedtypesofanimalswithinthepurebreeds,probablvrelatingtostrainswithinabreed.Inthiscasetheremayhavebeenvariationinonerespectonly,namely,bodylength,producingtwotvpesofdogs.Thusthemethodiscapableofidentifyingtypesifthevdoexist.
Wecanagainaskthemostimportantquestion:isthereanyindicationoftheexistenceoftruebehavioraltypes?Anaffirmativeanswerwouldberelatedtothegeneraltheoryofpleiotropvdiscussedinthelastchapter:namely,theexistenceofmajorgenes,eachofwhichproduceseffectsinmanvdifferentsituations.TheF2populationgivesthemostclear-cuttestofanyhybridgroup,sincetheeffectofallgeneticfactorsshouldappear,andsincethereshouldbeaminimumeffectofgeneticlinkageuponcorrelation.
Inthefirstanalysis,wecanexamineacompletelynullhypothesis:thatnoneofthebehavioralvariablesarerelatedtoeachotherasidefromthosewhichareobviouslycorrelatedbecausethevwerederivedfromthesametestsituation.Thishypothesiscanbediscarded,becausethecorrelationsbetweenvariablesindifferentbehavioral
DIFFERENTIALCAPACITIES
TABLE14.6
Factor2,Activity-SuccessintheCombinedF2Generation(Brace)
Factor2,Activity-SuccessintheCombinedF2Generation(Brace)
testsfarexceedthenumberexpectedbychance.Thedifferenttestsaredefinitelyrelatedtoeachotherinsomeway.However,thecorrelationsbetweenthemintheF2generationareuniformlylow.IfthereweremajorgenesforbasictraitssegregatingintheF2>s,wewouldexpectgroupsoftestswithhighcorrelationsbetweenthem.Lookingatthefactorsthemselves,weseethatFactor2intheF2generationincludesalargenumberofperformancetestsandcertainmeasuresofhighactivity(Table14.6).Bracethereforelabeledit"activity-success."Factor3includesallofthemeasuresofheartrateandafewwhichmayindicatetimidity(Table14.7).Beyondthis,Factors4and5includeonlymiscellaneousvariableswithlow
TABLE14.7
Factor3,Heart-Rate,intheCombinedF2Generation(Brace)
Variable
Highadultheartrate
Lowarrhythmiarate
Manyerrors,U-shapedharrier
Littleplayfulfighting
Muchdistressvocalizationwhileweighed
Activeduringbellringing
Greatdocility,sittraining
SlowonT-maze
Muchtremor,reactivity
Fewerrors,longbarrier
Erectposture,reactivity
Highinfantileheartrate
Muchvocalization,U-shapedbarrier....
Loading
.68.56.43.43.41.37.34.33.32.32.31.31.30
EFFECTSOFHEREDITY
373
loadings.TherearethereforeonlytwoexplainablebehavioralfactorsintheF2hybrids.
Theothergroupsofsegregatinghybridsshowsimilarresults.InthebackcrosstothebasenjitherearetwofactorsverysimilartothoseintheF2,andpossiblyathirdwhichconsistsofagroupoftestsindicatingahighrateofvocalization.Inthebackcrosstothecockers,Factor2isagainmarkedbysuccessonavarietyofperformancetests,althoughtheseareadifferentgroupfromthoseemphasizedintheothertwohybrids.Likewise,thenextfactorisonewhichcanbelabeled"heartrate,"althoughnotasdefinitelyasintheothertwo.
Anotheranalysisinwhichgeneticdifferenceswouldbeexpectedtobehighlyimportantisthatofthecombinedpurebreeds,inwhichbreeddifferencesaremaximized.HereFactor2isagainoneofgoodperformanceonthesameseriesoftestsasintheF2andtheback-crosstothebasenji.Factor3isoncemorearecognizableheartratefactor.Thusthereappeartobeonlytworecognizablebehavioralfactorsderivedfromthepopulationsinwhichgeneticdifferencesshouldbeimportant.
ComparingthisresultwiththatintheFigeneration,inwhichgeneticdifferencesaretheoreticallylessimportant,wefindanentirelydifferentsituation.Herethereisonlyonerecognizablebehavioralfactor,whichincludesallofthe11measuresfromthereactivitytests,eachloadingindicatinganactiveanimalinovertbehaviororinheartrate(Table14.8).Thus,inapopulationinwhichgenetic
TABLE14.8Factor2,Reactivity,intheCombinedFxHybrids(Brace)
ReactivityTests
OtherTests
Loading
Activeinvestigation
Highadultheartrate
Erectposture
Littlechangeinheartrate.Activeduringbellringing.
Muchvocalization
Activeescape
Littlechangeinactivity..Littlecardiacarrhythmia.
Littlevocalization,leashtrainingLittlefearofhumanhandlersMuchinterference,leashtraining
Muchdistressvocalizationwhileweighed
Littlechangeinheartrate,bellringingLittletremor
ActivewhileweighedMuchplayfulfighting
FastonT-maze
Fewerrors,longbarrier
.71.63.61.59.57.51.50.49.46.45.42.40.40.39.38.38.33.31.30
DIFFERENTIALCAPACITIES
differencesarelessimportant,thegreatestamountofcorrelationappearstocomefromacommontestsituation.
Bracecametotheconclusionthathewasdealingwithfourmajorfactorsinallthedogs:bodysize,activity-success,heartrate,andgeneralactivity.Insteadofavarietyofgeneraltraits,theevidenceshowsthatthereareonlyalimitednumber.
Wemaynowtakeasecondlookatthemostimportantbehavioralfactor,activity-success(Table14.6).Itincludesaverylargenumberofsignificant
activity-success(Table14.6).Itincludesaverylargenumberofsignificantfactorloadings,noneveryhigh,butmostofthemindicatinggoodperformanceonavarietyofperformancetests.Infact,almostalloftheintelligencetestsareincluded.Alongwiththistherearehighloadingsoncertainreactivitytests,indicatinghighactivityandgeneralconfidence.Wecanthereforelabelthisfactor"Generalgoodperformanceandactive,confidentbehavior."
Asimilarfactorinvolvinggoodperformanceappearsintheback-crosstothebasenjis.Factorsinvolvingseveralperformancetestsarealsofoundinotherhybridpopulationsandinthepurebreeds,butthereislessconsistencyabouttheircomposition.LookingatthecorrelationtablesoftheF2'sandbasenjibackcross,weimmediatelynoticealargenumberofsignificantcorrelationswiththetrailingtest(Table14.9).
TABLE14.9
CorrelationsofPoorPerformanceontheTrailingTestwithPerformanceinOtherTestsinTwoHybridPopulations
TestPerformance
Manyerrors,T-maze
Slowonmotor-skilltest
Slow,spatial-orientationtest
Littleapproachandfollowingbehavior
Slowont-maze
Littleplayfulfightingwithhandler
Poorperformanceonstringpulling,manipulationtest
Littlepersistence,spatialorientation
Manyvocalizations,U-shapedbarrier
Fewescapeattempts,reactivitytest
Fast,goal-orientationtest
Fast,goal-orientationtest
Littleactivityduringbellringing
Littleinvestigation,reactivitytest
Manyerrors,U-shapedbarriertest
Slowonmazetest
BackcrosstoBasenji
33
Aswesawinchapter10,thetrailingtestshowsahighdegreeofvariationineverypopulation,butthedifferencesinvariancebetweenthesepopulationsarealmostentirelyaccountedforbyfearresponsestotheapparatus.Alargeamountofvarianceduetothis
EFFECTSOFHEREDITY375
sortoftimidityoccursinthebackcrosstothebasenjis,suggestingthatwemaybedealingwithabackcrosstoarecessive.
AssumingthatwehavesucharelativelysimpleMendelianmechanism,wewouldexpectcertainresultsinafactoranalysis.Thefactor-analyticmethodisbasedoncorrelation,andcorrelationispossibleonlywherethereisvariation.AccordingtoMendeliantheory,thereshouldbegeneticvariationonlyinthebackcrossandF2generations.Therefore,weshouldgetclear-cutgeneticfactorsfromonlythesepopulations.Thisexpectationisborneoutbytheresults,atleastinpart.Inthebackcrosstothebasenjis,thetrailingtesthasthehighestloadingonthegeneralfactormentionedabove.Wecouldthereforecallthisfactor"timidity,orfear,"particularlyofstrangeapparatusbutalsoinvolvingsomefearofhumanbeingsbecauseofthenegativecorrelationwithplayfulaggressivenessandattractiononthehandlingtest.Fearortimidityis,ofcourse,theoppositeendofthescalefromconfidence,whichwastheoriginallabelofthefactorandanequallyappropriateone.Wecannowspecifythekindofconfidence—thatevidentindealingwithstrangeobjects.
Wemayconcludethatthisisacaseofasimilareffectonperformanceinmanydifferentsituations.Thisfitstheconceptofageneralbehaviortraitproducedbyapleiotropicgene.However,withthepossibleexceptionoftheheartratefactor,
apleiotropicgene.However,withthepossibleexceptionoftheheartratefactor,whichmightitselfberelatedtoanothersortoftimidity,apparatus-fearistheonlycaseofthissortwhichturnedupinthefactoranalysis.Therearenootherwell-identifiedfactorsinvolvinglargenumbersoftests,andwemustconcludethatthevastmajorityofgeneticeffectsonbehaviorarehighlyspecificandrestrictedtooneortwosituations.
Re-examiningthecorrelationtables,wewouldexpectthatifgeneraltraitswerecommon,thereshouldbemanyhighcorrelationsinthebackcrossandF2generationasaresultofgeneticsegregation.Withtheexceptionofthetrailingtestscoresandcertainothersderivedfromcommontests,andhencedependentoneachotherforotherreasons,therearenosuchhighcorrelations.Therearemanymorecorrelationsbetweentheindependentteststhanmightbeexpectedbychance,butallofthemarelow.Thisindicatesthattheremaybetraitswhichhavemajoreffectsononetestandonlyminoreffectsonothers.Evaluatingthewholestudy,wecansaythatthemajorityofbehaviortraitsappeartobeofthislatterkind,specificintheireffectsandinheritedindependentlyofeachother,andthattheonlyverifiedgeneraltraitisanemotionalone.
Valueofthefactorialmethodforgeneticanalysis.—Thevalueofthefactorialmethodisthatitselects,onanentirelyobjectiveand
376DIFFERENTIALCAPACITIES
impersonalbasisindependentofthepreconceivedideasoftheexperimenter,thosemeasurementswhichhavecommoncorrelations.Thesameobjectivitycomprisesitschieflimitationforgeneticanalysis,becausethemethodmakesnodistinctionbetweenthosemeasurementswhicharecorrelatedbecauseofheredityandthosewhicharecorrelatedbecauseofvariousenvironmentalagents.Thedistinctionbetweenfactorswhichareprimarilygeneticandothersmustthereforebemadeonthejudgmentoftheexperimenter.
Theessentialcharacteristicofageneticallydeterminedfactoristhatitshouldappearonlyinpopulationsinwhichthereisimportantgeneticvariation.InaMendeliancross,itshouldappearinthesegregatingpopulations,i.e.,thebackcrossesandF2's.Ifthegeneticsysteminvolvesdominance,thefactorwillappearonlyintheback-crosstotherecessive.Aswehaveseenabove,onlyonefactorhadthischaracteristicinanyclear-cutway.
Factoranalysiswillalsoselectmeasurementsmadeinsituationswhichforsomereasonappeartobesimilartotheanimals,whetherornotthesimilarityhasa
reasonappeartobesimilartotheanimals,whetherornotthesimilarityhasageneticbasis.Forexample,boththemotor-skilltestandspatial-orientationtestrequiredclimbingonaramp.Correlationmayoccurbecausetestsareactuallysimilar,asinthiscase,orbecausemeasurementsaremadeatthesametimeandhencearenotcompletelyindependentofeachother.Stillanotherpossibilityistheeffectofprevioussuccess,whichmaycarryoverfromonetesttoanother,whetherornotthetestsaresimilar.Thesekindsofcorrelationsmayinpracticebedifficulttotellfromthoseproducedbygeneticcorrelation.Geneticallybasedcorrelationsshouldappearinonlythesegregatinggenerations,whilenon-geneticcorrelationsmightappearinnon-segregatingpopulationsaswell,inevitablyproducingsomeconfusionbetweenthetwosourcesofcorrelation.
Analyzinggeneticvariancebijcorrelationalmethods.—Analyzinggeneticresultsbythemethodoffactoranalysisisadifficultprocesswithoutadditionalcluesbasedonadirectknowledgeoftheteststhemselves.Thissuggestsanotherpossiblemethodofanalyzinginheritance—onebasedoncorrelation.Ifwetaketwotestswhichshowhighcorrelationinthesegregatinggenerationsandlowcorrelationsinotherpopulations,weshouldbeabletomakeanestimateoftheamountofvarianceduetogeneticfactors,usingtheprinciplethatthepercentageofvarianceduetocorrelationisgivenbythesquareofthecorrelationcoefficient.
AsshowninTable14.10,thismethodcanbeusedtotransform
EFFECTSOFHEREDITY
377
thevarianceofthetrailingtest,thekeyvariableinthe"activeconfidentsuccess"factor,bycomputingthecommonvariancewitherrorsintheT-maze,thetestwithwhichitismosthighlycorrelated.Theresultisadistributionofvariancewhichisconsistentwiththe
TABLE14.10
CommonVarianceinTrailingTestasIndicatedbyCorrelationwithPerformanceinT-Maze
hypothesisofarecessivegeneorgenesfortimidityinthebasenjibreed.Furthermore,theresultsareverydifferentfromtheoriginalrawdata,whichlookedasifthereweremanycomplicatedinteractionsinvolvedwiththe
lookedasifthereweremanycomplicatedinteractionsinvolvedwiththematernalenvironment,etc.Inotherwords,thecorrelationcoefficientcanbeusedto"strainout"thatportionofthevariancewhichconformstothemathematicalassumptionsofthecorrelationcoefficient;namely,thoseofsimplelineareffectsandanormaldistributionofvariation.
Themethodshouldworkwellonlyifthetwotestsormeasurementsusedaresituationallyindependentofeachother,sothattherearenocommonenvironmentalfactorsandcorrelationisduechieflytothehereditaryorganizationofeachindividual.Itshouldalsoworkbestwherenumberslargeenoughtoinsuretheaccuracyofestimatesofthecorrelationcoefficientareused.
Thisagainbringsuptheneedfornewmethodsofanalysis.Asindicatedinchapter12,presentlyavailablequantitativemethodsareinadequateforanalyzingtheeffectsofheredityuponintricateproblem-solvingbehavior,excepttoindicatethatcomplexinteractionisimportant.Progressinthefuturewillinpartdependonthedevelopmentofstatisticalmethodswhoseassumptionsmoreaccuratelymeetthefactsofbehaviorinheritance.However,thereis
378DIFFERENTIALCAPACITIES
alreadyabundantevidencefromourownandotherworkthatheredityhasaquantitativelyimportanteffectonbehavior,andfutureresearchshouldalsobedirectedtowardtheimportantquestionofhowheredityaffectsbehavior—aproblemwhichisstillalmostuntouchedwithrespecttothekindsofgeneticdifferencesinemotionalreactionsandsocialbehaviorwhicharesoimportantinthedog.
CONCLUSION
Inthischapterwehaveattemptedanunbiasedgeneralsurveyoftheeffectofheredityuponthebehaviorofdogs.Whilemanyofthetestsweresetupwithoutanypreviousknowledgeofbehavioraldifferences,manyothersweredevisedtomeasurethebreeddifferencesinbehaviorwhichwehadseenincasualobservations.Inshort,wetriedtodesignourexperimentssothattherewouldbeafavorablechanceofrevealinggeneticdifferences.Thedataarebiasedinthisdirection,butthestatisticalmethodsarenot.
Ingeneral,theresultsshowthatheredityisanimportantquantitativedeterminerofbehaviorindogsandthatgeneticdifferencesinbehaviorcanbeasreliablymeasuredandanalyzedascanhereditarydifferencesinphysicalsize.
measuredandanalyzedascanhereditarydifferencesinphysicalsize.
Consideredasagroup,theresultsofthevarioustestsareconsistentwiththeprincipleofMendeliansegregation,withsomeindicationthatdominanceisanimportantfactorinmostcases.Atthesametime,theresultsofindividualtestsarefrequentlydifficulttointerpretuponasimpleMendelianbasisbecauseofthecomplexinteractionswiththeenvironmentwhicharesoofteninvolvedintheprocessofbehavioraladaptation.
Therearerelativelyfewgeneralbehavioraltraits.Rather,eachbreedshowsacombinationofmanyspecialcharacteristicswhichareoftenrelatedtothespecialbehavioraltasksforwhichthebreedhasbeenselected.
Furthermore,therearerelativelyfewbehavioraltraitsforwhichanybreedisactuallyhomozygous.Evenwithintherestrictedsampleschosenforthisexperimenttherewasagreatdealofindividualgeneticvariability.
Thislargeamountofgeneticvariation,bothwithinandbetweenbreeds,Leadstotheconclusionthatitisimpossibletogeneralizeaboutanyonebreedfromexperiencewithonedogorevenonestrainofdogs,andthatitislikewiseimpossibletogeneralizeaboutalldogsfromexperiencewithonebreed.Furthermore,theirgreatrangeofgeneticvariabilitymakesdogshighlyreactivetoselection.
EFFECTSOFHEREDITY379
Selectionofcertainkindsofbehaviorcangreatlymodifyabreedwithinafewgenerations,andincreasingtherangeofvariabilitystillfurtherbybreedcrossingmakesitpossibletoreadilycreatenewanduniquecombinationsofbehavioraltraitstomeetthespecializedneedsofchanginghumansocieties.
GENERALIMPLICATIONS
IMPLICATIONSFORTHEARTOFDOGBREEDING
INTRODUCTION
Ourprimarypurposeinthisstudywastodiscoverasmuchaspossibleabouttheeffectofheredityuponbehavior,andwechosethedogasoneofthemostfavorablespeciesfordemonstratingthemagnitudeofsucheffects.Toachieveourobjectiveitwasnecessarytostudythegeneticbackgroundofdogs,theirbehavioraldevelopment,andtheirsocialorganization.Allthisinformation,togetherwiththefindingsfromourgeneticexperiments,hasimplicationsforthepracticaldogbreederaswellasthescientistandthestudentofhumanaffairs.
Wehaveusedtheword"Art"advisedlyinthetitleofthischapterbecauseanypracticalapplicationofscientificknowledgeinvolvesacertainamountofindividualjudgmentandadaptationtospecialcircumstances.Thescientificfindingsmustbeinterpreted,andwhenthisisdoneweareenteringtherealmofthearts.Applicationsmustbedesignedtoindividualcircumstances.OurownworkwasnecessarilylimitedtoonlyafewoutofthemorethanonehundredbreedsnowrecognizedbytheAmericanKennelClub.Inthefollowingpages,weshalloutlinethemajorfindingsofourstudyandindicatetheirgeneralimplications.
RESULTSANDTHEIRIMPLICATIONS
Basicdogbehavior.—Allpresentevidenceindicatesthatdogswerefirstdomesticatedfromwolvesandthatbothspeciespossessthesamebasicpatternsofbehavior.Muchdogbehaviorcanbe
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understoodintermsofthesociallifeofwolves,anddogbreedscanbethoughtofasmoreorlessspecializedpopulationsofwolves.Therawmaterialsofthedogbreederarethebehaviorpatternsofdogsandwolveswhicharelistedinchapter3.Hecanmodifythefrequencyofexpressionofthesepatternsinallsortsofcombinationsexceptthosewhichareincompatiblewithlifeandreproduction.Thisgeneralrepertoryofbehaviorlikewiseimposescertainlimitationsuponbreeding,inthatitisdifficult,ifnotimpossible,togobeyondthebasiccapacitiesofdogs.
Combinedactionofenvironmentalandhereditaryfactors.—Wefoundbreeddifferencesinbehaviorbeginningatbirthandextendingthroughoutthefirstyear.Duringthistime,particulardifferencesmightwaxandwaneandenvironmentalfactorscouldaffectbehavioratallstagesofdevelopment.The
environmentalfactorscouldaffectbehavioratallstagesofdevelopment.Theimportantfactisthatbehaviorisneverwhollyinheritedorwhollyacquiredbutalwaysdevelopedunderthecombinedinfluencesofhereditaryandenvironmentalfactors.Theconclusionforthepracticalbreederisthatitisalmostalwayspossibletomodifybehaviorbymodifyingenvironmentaswellasheredity.Sincetheformercanbedonesomuchmorerapidlythanthelatter,itisalwaysagoodideatosupplementabreedingprogramwithoneofimprovedtrainingandupbringing.
Thisbringsupthepracticalquestionofwhetheritisbettertoreardogsinapoorenvironment,withtheideathatonlythebestanimalswillovercomeitandwillbechosenforbreeding,orwhetheritisbettertosetupafavorableenvironmentandselectanimalswhichdobestundertheseconditions.This,ofcourse,isamatterofpracticaljudgment.Theformerplanobviouslyleadstoagreatdealofwaste,anddogsmaybeselectedwhichdowellinpoorenvironmentsbutinnoothers.Ingeneral,thebestplanwouldbetoraisetheanimalsunderthebestpossibleconditionsandbaseaselectionprogramonincreasinglyhigherstandards.
Periodsofdevelopment.—Designingagoodenvironmentforthedevelopmentofapuppydependsuponknowledgeoftheperiodsofdevelopment.Itis,ofcourse,importantatallagestoprovideadequatenutritionandtopreventdisease.Beyondtheserequirementsidealcarevariesfromperiodtoperiod.Intheneonatalperiodanormalmotherwillprovideoptimalcareforherpuppies,andattentionshouldbeconcentrateduponmakingsurethatthebitchiswellnourishedandallowedtocareforherpuppiesundisturbed.Themostthattheownerneedstodoistoinspectthepuppiesonceadaylorpossibleillnessoraccidents.Thisinspectionmayleadtosecondarybenefits.Althoughwehavenodirectevidence,experi-
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mentswithotherspecies(Levine,1962;Denenberg,1962)stronglyindicatethatvounganimalsbenefitfromthestimulationofhandling.
Asimilarregimecanbecontinuedthroughthetransitionperiod,anditisnotuntilthebeginningoftheperiodofsocializationthatadditionalcarebecomesimportant.Thefirstthingistoprovideadditionalfood,beginningat3weeksofageorpossiblyearlierifthemotherisshortofmilkorhasalargelitter.
Intheperiodofsocializationtherearetwobasicrulesforproducingawell-balancedandwell-adjusteddog.Thefirstoftheseisthattheidealtimetoproduceaclosesocialrelationshipbetweenapuppvandhismasteroccursbetween6and8weeksofage.Thisistheoptimaltimetoremoveapuppvfromthelitterandmakeitintoahousepet.Ifthisisdoneearlier,especiallyat4weeksorbefore,thepuppvhaslittleopportunitvtoformnormalsocialrelationshipswithotherdogs.Itwillformcloserelationshipswithpeoplebutmavhavedifficultvadjustingtoitsownkindeveninmatingorcaringforpuppies.Ontheotherhand,ifprimarysocializationwithpeopleisputofftoamuchlaterperiod(theoutsidelimitbeingabout12weeks),thesocialrelationshipsofthepuppywithotherdogsmavbeverygood,buthewilltendtobetimidandtolackconfidencewithpeople.Althoughalldogbreedshavethecapacitytodevelopaclosesocialrelationshipwithpeople,theimportanceofthisrelationshipvarieswiththedog'sfutureuse.Astrongrelationshipishighlyimportantwithpetdogs,workingdogs,andthosehuntingdogswhichworkunderclosedirection.Itisprobablynotsoimportantinmosthounds,withwhichthedog-humanrelationshipisnotsoessentialforsuccessfulhunting.
Thesecondgeneralruleisthatthevoungdogshouldbeintroduced,atleastinapreliminarvway,tothecircumstancesinwhichitwillliveasanadult,andthisshouldbedonebefore3or4monthsofage.Theyoungpuppyfrom8to12weeksisahighlymalleableandadaptableanimal,andthisisthetimetolaythefoundationforitsfuturelifework.Dogsleftinakenneluntil4monthsofageorolderarefrequentlypoorlvadaptedtoanvotherlife.ThisconclusionisstronglysupportedbytheworkofKrushinskii(1962)aswellasourown.Althoughanexceptionalanimalorbreedmaydofairlywellwhenthesetworulesarenotfollowed,theirobservancewillbringoutthefullgeneticcapacitiesofamaximumnumberofanimals.
Theimportanceofbreeddifferences.—Thereareimportantbreeddifferencesinalmosteveryaspectofbehaviorandphysique,andeveninthedevelopmentofsocialrelationships.Atthesametime,
thecapacitiesofeachbreedareagreatdealbroaderthanmostpeoplerealize.Abreedmayhaveonehighlyspecializedability,butinmostcasesitalsoretainsbroadandgeneralcapacitiesaswell.Forthepracticalbreederandevenforthepetownerthisfindinghasrelevancetothechoiceofabreedforanyparticularpurpose.Somebreedsarerathernarrowlyspecializedintheirbehavior,par-ticularlvtheworkingdogs,whichoftenmakepoorhouseholdpetsunlesstheyaregivenaratherhighdegreeoftrainingandregulartaskstoperform.Onthe
aregivenaratherhighdegreeoftrainingandregulartaskstoperform.Ontheotherhand,eventhesebreedsretainwiderabilities.Germanshepherdscanbetaughttracking,andcolliesretainanabilitytohuntdeer,asmanycollieownershavefoundtotheircost.
Ingeneral,huntingdogsdobetterinakennelthandotheworkingbreeds.Inourownexperiments,basenjis,beagles,cockers,andterriersalladjustedwelltothelaboratoryconditions.Thesamehuntingbreedsadaptthemselveswellashousepets.Beaglesareafavoriteforthispurposebecauseoftheirextremelackofaggressiveness.Withaminimumoftraining,abeaglewillbecomeabearablehousepet,andthechiefdifficultvwiththebreedundermodernconditionsisinattentivenesstocars,witharesultinghighdeathrate.Ontheotherhand,theydopoorlyastrainedperformers.Otherkindsofhuntingbreeds,suchasthebirddogsandretrievers,alsoadaptwelltohouseholdlivingandusuallyaremuchbetteratacceptinginhibitorytrainingthanthehounds.Thegeneralprincipleisthatmanybreedshaveawiderrangeofadaptabilitythanisordinarilyrecognized,andthatthescopeofadaptabilitymaybemuchnarrowerinsomebreedsthanothers.
Heterogeneitywithinpurebreeds.—Forourpurposesitwasdesirabletominimizevariationwithinbreedsbystartingwithoneortwofoundationpairsineachgroup.Theprocedurewassuccessfulindemonstratingsignificantvariationbetweenbreedsinalmosteverymeasure,buttheprecedingpagesalsodocumentthewiderangeofbehavioralandphysicalvariationwitiiineachbreed.WemayrecallsuchexamplesastheweightofShetlandsheepdogsatoneyear(mean=11.7kg.;range,4.2-31.6kg.)orleash-trainingdemeritsofbasenjis(mean=57;range,20-97).Obviouslyagreatdealofphenotvpicvariationisstillpresentinthepurebreedsofdogs,andthegeneticsourceofsomeofthisvariationisshownbythegeneralfindingthatmatingswithinabreedtendedtobeconsistentlydifferentfromeachodier.Thismeansthatthepracticalbreedercanusuallyeffectmajorchangesinabreedbvmeansofaselectionprogram.Whetherornothewillbesuccessfulinachieving
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thechangeshedesireswilldependuponthenatureofhisobjectivesandthedetailsofthebreedingprogram.
Importanceofemotionaldifferences.—Differencesinemotionalreactionsareverycommon,bothbetweenandwithinbreeds.Thishasseveralconsequencesofinteresttothepracticalbreeder.Mostoftheseemotionalreactionsarespecific
ofinteresttothepracticalbreeder.Mostoftheseemotionalreactionsarespecificinnature.Forexample,abasenjiisafraidofstrangeapparatusbutshowslittletimiditywithrespecttootherdogs.Thereappeartobeseveraldifferentkindsoffearfulnessindogs,andselectionforconfidenceinoneparticularsituationwillnotnecessarilyaffectconfidenceinanother.Theproblemofunwantedtimiditypresentsitselfinalmosteverybreed.Itsveryuniversalitysuggeststhatitmaybeatraitnecessaryforexistence.Ananimalwhichisafraidofnothingisnotlikelytolivelongorbeanamenablecompanionforman,andselectionshouldprobablybedirectedtowardadesirablebalancebetweentimidityandoverconfidenceratherthancompleteeliminationofeithertrait.
Emotionalreactionshaveimportanteffectsuponperformance,sothatselectionforabilitytolearnparticulartasksislikelytoaffectemotionsfirstandtruecognitiveabilitieslater.Itissometimesverydifficulttoseparatethetwoinapracticalsituation.
Motivationaldifferences.—Closelyrelatedtoemotionaldifferencesarevariationsindegreeofmotivation.Intermsofpsychologicallearningtheory,repeatedreinforcementofanactbyrewardorpunishmentleadstoincreasedmotivation.Ourfivebreedsdifferedintheirpreferredmodesofreinforcement.Beagles,forexample,werereliablymotivatedbyfood;Shetlandsheepdogsandbasenjiswouldsometimesmerelysniffatthefoodrewardsandweretypicallyhesitantabouteating.Anopportunitytoexplore,particularlyinanodor-richenvironment,appearedmorerewardingtobeaglesthantoShetlandsheepdogs.Differencesinreactiontounpleasantoraversivestimulationwerealsomanifested.Physicalrestraintevokedmorestrugglinganddistressvocalizationinbasenjisthaninwire-hairedterriers,althoughintheirpensbothbreedsappearedtobeactiveandaggressive.Sheltiesarehighlysensitivetopunishment.Hayes(1962)hasgonesofarastosuggestthattheeffectsofgenesuponintelligenceareexertedprimarilythroughmodificationsofthemotivatingpropertiesofparticularclassesofstimuli.
Forpracticaldogbreeders,themostimportantmotivationalcharacteristicofadogisitsresponsetopraiseandblamefromatrainer.Breedvariationsinattractiontohumansdevelopedearlyinourpuppies,asshownbythehandling-testresultsandwereobviouswhenthedogslivedinoutsideruns.Althoughallthedogshadthesame
amountofprevioushandling,spanielsandbeagleswouldtypicallyswarmoveranexperimenterduringtheweeklyexamination,whilebasenjiandShetland
anexperimenterduringtheweeklyexamination,whilebasenjiandShetlandsheepdogsstoodaside.Undoubtedlyselectionforsocialresponsestomanhasplayedanimportantpartindogbreeding.Whenananimalcanbereliablymotivated,ineitherapositiveornegativeway,itsbehaviorcanbemoldedbycontrollingreinforcement,sothatthisaspectofhereditaryvariationinbehaviorhasthegreatestsignificanceinchoosingabreedforaparticulartask.
Heredityandintelligence.—Theinheritanceofthetendencytoperformwellinaparticularsituation,insofarasitcanbeseparatedfromemotionalandmotivationalreactions,appearstobehighlycomplex.Thegeneralprinciplehereisthatproblemsolvingisaprocessofadaptation,andtheanimaluseswhatevercapacitiesithasinordertosolvetheproblem.Thiswasapparentinthedifferentsolutionsoftheproblemofboxclimbinginthemotor-skilltest,inwhichthecockerandbasenjibreedsusedverydifferentcapacitiestoachievethesameresult.Inapracticalprogramofselectionthismightmeanthattwodogshavingverydifferentbasiccapacitiesbutequalperformancemightbeselectedandmatedtogether,givingrisetooffspringwithstillothercombinationsofabilitieswhichmightbeinferiortoeitherparent.Anyrealprogressinsuchasituationwoulddependonanalysisofthebasiccapacitiesinvolvedandinde-dendentselectionforeach.
Indogswefoundnothinglikethegeneral-intelligencefactorsometimespostulatedforhumans.Thisfailuremighthavebeenduetoinadequatescopeoftesting,sincethedimensionsofintelligencewerenotthemajorgoalsofthestudy.Ourresultsare,however,compatiblewiththoseofSearle(1949),whofoundthatratsselectedforgoodperformanceononetypeofmazeperformednobetterthantheaverageonotherlearningtasks.Provisionally,wehaveadoptedtheviewthatgeneticeffectsinspecializedtasksaremediatedthroughnumerousindependentpathways,andthatselectionforgoodperformanceononetaskwillimproveonlyverycloselyrelatedtasks.Theunityormultiplicityofintelligence(fromthegeneticpointofview)wasnotcriticallytestedintheseexperiments,andmoreresearchisneededtosettletheissue.Itseemspossiblethatsincecertainpsychologicalprocesseshavebeenshowntobecriticallydependentupontheintegrityoflocalizedportionsofthebrain,theseorotherpsychologicalprocessesmightbecontrolledbyaparticulargroupofgenes.Itshouldeventuallybepossibletodescribeanyspecificproblem-solvingabilityinthedoginterms
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ofafewbasiccapacities,butatpresentwecanspecifyonlyafewofthese
ofafewbasiccapacities,butatpresentwecanspecifyonlyafewoftheserelatingtoemotionalandmotivationalresponses.
Traitindependence:lackofcorrelationbetweenphysicalandbehavioralmeasures.—Oneofourmajorfindingswasanegativeone,thefailuretofindcorrelationsbetweenphysicalandbehavioralmeasures.TheF2basenji-spanielhybridsdemonstratedthisbest.Theseanimalsshowedawiderangeofvariabilityinappearance,noneshowingexactlythesamecombinationsofcharacteristicsastheparentbreeds.Thephysicalphenotypeyieldednocluestotheresultsofthebehavioraltests.Thedogwithbasenjicoatandtailcarriageoftenwasdocileliketheaveragespaniel.Althoughsomeheritablevariationinbehaviorobviouslyrestsuponheritablestructuralcharacteristics,suchaslengthoflegsandlopears,mostifnotallbehaviorisunrelatedtothecolorandformcharacteristicswhichdefinethecommonimageofabasenjiorcockerspaniel.Therefore,attemptstocharacterizeabreedbiologicallyandpsychologicallywithrespecttoatypeembodiedinaparticularindividualareunsound.Thedefinitionofatypehassomevalueintheshowring,becauseitgivesjudgesanobjectivebasisforscoringacompetitiveevent,butitshouldberecognizedasanabstraction.Abreedisnotdefinedbyconformitytotype,butbycommonancestryandabsenceofoutbreeding.Ifconformitytotypeisestablishedasthegoalofaselectivebreedingprogram,certaindifficultiesareboundtoappearbecauseofthecomplexityofgeneticdeterminationofthemanytraitswhichenterintoatypedefinition.
Inheritanceofcoatcolorandbodystructure.—CloselyassociatedwiththebehaviorresearchprojectC.C.Little(1957),buildingonthepreviousworkofothers,workedoutthemajoroutlinesofcolorinheritanceinthedog.Inmostcasescolor,hairlength,andhairtexturearedeterminedbymajorgeneswithclear-cutdominanceandepistaticrelationshipsbetweenthem,withsomeminormodifyinggenes.Thismakestheselectionofadesiredcolorafairlyeasyprocess.Sizeandphysicalconformationareapparentlydeterminedbymultiplefactors,butsincethesecharacteristicscanbeeasilyquantified,thisdoesnotinterferewithselection.
Theinheritanceofstructuraldefectsislesswellknown.Thepurebreedsusuallycontaingeneswhichproducephysicaldefects.Cleftpalate,hipdysplasia,blindnessproducedbyprogressiveretinalatrophy,andhemophiliaareallknowntobeatleastpartiallycausedbyheredity.MoreextensivelistshavebeenmadebyBurns(1952)andFuller(1954,1956a,1960).Inourownparticularstrainswefoundcasesofundershotjawsandatendencytoinguinalherniain
thebasenji,otocephaly("pigjaw")inthebeagles,low-degreehydrocephalyincockers,obesityandmonorchidisminshelties,andclubfeetinwire-hairedterriers.Infertileindividualsproducedbyvariousphvsiologicaldefectsshowedupinallthestrains.
Someoftheseconditionsarerareandareseldomseenbytheordinarybreeder;othersarecommonenoughtocauseconcernamongbreedassociations.Theirgeneticmanagementdependsuponthemodeofinheritance,thefrequencyofthedefect,itseconomicimportance,anditseffectuponviabilityandfertility.Mostbreederswillfinditdesirabletoconsultageneticistforadviceonspecificproblems,butafewexampleswillillustratethedifficultiesinvolved.
OurShetlandsheepdogsillustrateasimpletypeofproblemanditsgeneticmanagement.SomeofthemcarriedthedominantMgene,whichchangesblackhairtograywithblackspots.Inthepropercombinationwithothergenes,itproducesthehighlyadmiredbluemerlecolor.Amerleisalwaysheterozygous(Mm),sinceMManimalsarenotbluebutalmostcompletelywhiteandpartiallyblindanddeaf.PreventionofthedefectiseasilyachievedbynotallowinganytwoanimalscarryingM,whethermerleorwhite,tomatewitheachother.Aslongasoneparentismm,nodefectivewhiteswillbeproduced.
Otherdeleteriousgenesarenotasreadilymanaged.Scatteredamongthedogbreedsaremanyrecessivegeneswhichproducenoobviousphenotypiceffectsexceptindoubledose.Manyofthesegenesarequiterareandthedefectscorrespondinglyinfrequent,butunderspecialcircumstancesaparticulargenemaybecomecommon.Progressiveretinalatrophvleadingtoblindnessissuchacondition.Incertainbreedsafewpopularstudmalesapparentlycarriedthegeneanddisseminateditsowidelvamongnumerousdescendantsthatblindnesshasbecomeaseriousproblemforthebreedassociations.Theonlywaytoeliminatethegeneisthroughbreedingtests.Withoutthem,itisimpossibletodistinguishbetweencarriersandnon-carriers.Testmatingstoablindanimalmustbemadeandtheproductionofsixorsevennormal-sightedpuppiestakenaspresumptiveevidenceofthegene'sabsence.Suchaprocedureisinevitablytimeconsumingandexpensive.
Somephysicaldefectsconsistentlyappearincertainstrainsbutfollownoregularpatternofinheritance.Thusoccasionalcasesofcleftpalateappearedinourbeaglesandclubfeetinourwire-hairedfoxterriers.Suchcasescanbeaccountedforbyageneticconstitutionsensitivetoharmfulenvironmentalinfluences;themoresensi-
influences;themoresensi-
tivethegenotype,thelessenvironmentaldisturbanceisneededtoproducetheanomalv.
Thepublisheddataonhipdysplasiaindicatethatitisanenvironmentallyinfluenceddefectwithimportanthereditarydeterminants(Fuller,1960).Vulnerabilityrunsinfamilies,butthedegreeofafflictionissovariablethatprecisegeneticpredictionscannotbemade.AsurveyofthreebreedsbeingrearedaspotentialguidesfortheblindshowedthatoffspringofparentswithgoodhipspracticallyneverhaddysplasiaasjudgedfromX-rayphotographs;ontheotherhand,parentswithpoorhipsmighthavesatisfactoryoffspringbutproducedmorethantheirshareofdefectivepups.Inaddition,itappearslikelythatmorethanonegeneisconcerned.
Thepracticalgeneticmanagementofsuchamultiple-factordefectofmoderateheritabilityis,however,reasonablysimple.Itconsistsofbreedingfromthebeststockavailable,selectingthoselinesinwhichthedefectappearsinfrequently,anddisregardingrarecasesofdefectswhichmayresultfromenvironmentalcauses.Themethodisnotinfallible,butitshouldproducedesirableresultsunlessalltheavailablebreedingstockarecarriersofthedeleteriousgenes.
Forthepracticalbreederthewidespreadoccurrenceofinheritedphysicaldefectsmeansthatanyprogramofselectionmustbebasedonmultiplecriteria.Itisofnousetoproduceahighlyintelligentdogifheisalsoinfertile.
BREEDANDSTRAINIMPROVEMENT
Selection.—Themajorresourceoftheanimalbreederisselection,whichimpliesbothadesiredobjectiveandtheprovisionofastandardizedrearingproceduretominimizeenvironmentalvariation.Selectionhasbeentreatedbyanumberofauthorsfrombothpracticalandtheoreticalpointsofview(Lush,1943;Lerner,1958;Falconer,1960).Basically,selectionisanattempttobringaboutthedifferentialreproductionofgenotypes,andsochangetherelativeproportionsofalternateallelesfromgenerationtogeneration.
Theresultsofselectiondependchieflyuponthedegreeofheritabilityandthemodeofinheritanceofthedesiredtrait.Asshowninchapters12and14,heritabilityestimatesbasedonthefivepurebreedsandcrossesbetweentwoofthemrangebetweenzeroand66percent,withanaverageof27percent.Heritabilityestimatesontraitsvaluableinlivestockproduction,suchaswool
Heritabilityestimatesontraitsvaluableinlivestockproduction,suchaswoollengthor
eggproduction,rarelyrunover60percentandoftenaremuchlower(Falconer,1960).Ontheaverage,therefore,behaviorindogsshouldbeasresponsivetoselectionasarephysicaltraits.
Ofcourse,theaveragebreederismorelikelytobeworkingwithapurebreedthanwithhybrids.Evenheretheindicationsarefavorable,sincethebetween-matingvarianceaveraged12percentinasampleinwhichthiskindofvariancehadbeendeliberatelyreduced.Theamountofvarianceavailableforselectioninanunrestrictedsampleofapurebreedmustbemuchgreater.
Theotherfactoronwhichthesuccessofselectiondependsisthemodeofinheritance.Ifinheritanceissimple,resultswillbeachievedveryrapidly.Forexample,selectionforaneffectproducedbyasinglerecessivegene,suchasthenon-merlecondition,canproducemaximumeffectsinonegeneration.Ontheotherhand,ifaneffectdependsuponacombinationofseveralgenes,whichmayinteractwitheachother,resultswillcomemuchmoreslowly.Ourevidenceindicatesthatthemodeofinheritanceofdifferencesinemotionalreactionsandrelatedsimplebehaviorpatternsisrelativelysimple,whereasthebehaviorinvolvedinproblemsolvingandothercomplextasks,whileequallyheritable,isgovernedbycomplexmodesofinheritance.Tothenumerouspossibilitiesofinteractioningenephysiologyareaddedtheenormouspossibilitiesofinteractiononthebehaviorallevel;theanimalorganizesitscapacitiesindifferentwaysdependingonthetaskathand.Selectioninsuchacasewillbebasedonthebestcombinationofgenespresentintheoriginalpopulation,andLush(1943)makesthesuggestion,basedontheearlierworkofWright(1935)thatitmaybeverydifficulttogetawayfromthiscombinationandmakefurtherprogress,withoutaddingnewcombinationsofgenesthroughoutcrossing.
Allinall,selectionforbehaviortraitsinthedogshouldgivemostrapidresultswhenappliedtoemotionalandmotivationaltraitsandsimplebehaviorpatterns.Thefinalproblemofselectionis,ofcourse,thatofselectingformanytraitsatthesametime,andthisisanimportantpracticalproblemforanybreeder.
Hybridization.—Thewell-knowneffectofhybridvigorcanbeutilizedindogsaswellascorn.Hybridizationisessentiallyatechniqueofreliablyproducingahighlydesirablecombinationofgenes.Itdependsuponmaintainingpurestrainsand,attheoutset,uponhavingalargenumberofparentstrainsfromwhichtochoose,sothatthebestcombinationofparentscanbeselected.Thetechniqueis
choose,sothatthebestcombinationofparentscanbeselected.Thetechniqueiscomparabletothatof"nicking,"aphenomenoninwhichacrossbetweentwospecificindividualsproducesunusuallydesirableoff-
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spring.Thehybrideffectcannotbemaintainedbeyondonegeneration,asisalsotruewithnickingbetweenindividuals.
ThepleasingqualityofFihybridsfromcockersandbasenjissuggeststhatbreedintercrossesmightbeusedtoproducesuperiorworkinganimals,justashybridcornisusedinagriculturetoproducesuperiorgrain.Ifthereareobjectionstocrossingbreeds,separatelineswithinalargebreedmightbedevelopedtoseryethesamepurpose.Themethodwouldprobablybemoreeffective,however,withthewiderdifferencebetweenparents,andweseenoreasonforthenon-acceptanceofplannedhybridmatingsoncetheirpurposeisunderstood.
Methodsfortheindividualbreeder.—Theuseoftheabovetoolswillofcoursedependagreatdealupontheobjectivesandresourcesofeachbreeder.Anindividualownerusuallyhasalimitednumberofanimalsathisdisposalandcannotaffordthe10or15yearsnecessarytoaccomplishaselectionprogram.Asstatedabove,mostofthebehaviorconcernedwithcomplexperformancedependsuponacombinationofalargenumberofgeneticcapacities.Theindividualbreederwillusuallyfindthatthebestchanceofgettingsuchcombinationswillbetotryoutvariousmatingswithinhisownstockandotherstocksaccessibletohim.Onceamatingisfoundwhichproducesahighproportionofdesirablepuppies,thebreedercanthenrepeatthismatingthroughoutthelivesoftheparentanimalsandobtainalargenumberofoffspring.Thisgeneralplan,basedon"nicking,"issuitableforthebreederwithlimitedresourcesandtime.
Methodsforbreedassociations.—Thebreedassociationswerefoundedinordertoovercomethelimitationsimposedupontheindividualbreeders,anditispossibleforthemtoaccomplishmuchmorethroughlong-continuedselectionprograms.Inthefuture,thebreedassociationscanaccomplishmorethantheyhaveinthepastbymodifyingtheirobjectivesandmakinguseofnewergenetictheoriesandtechniques.Firstofallitshouldberealizedthatabreedisapopulationofindividualsshowingalimitedbutstillimportantdegreeofgeneticvariability.Ifselectionisconfinedtoonenarrowlydefinedtype,theresultwillalmostinevitablybetheaccidentalselectionofvariousundesirablecharacteristics.Breedstandardsshouldincluderegulationsrelatingtohealth,
characteristics.Breedstandardsshouldincluderegulationsrelatingtohealth,behavior,vigor,andfertilityaswellasbodyform.Thesecanperhapsbestbeaccomplishedbyintroducingtestsofperformanceandemotionalreactionsaswellasappearance.Obediencetrialsandfieldtrialsareavaluablestepinthisdirection.
Thedesirabilityofmultiplestandardsmakesthepracticeofbreedingachampiontoalargenumberoffemaleswithinabreedaquestionableone.Almosteveryanimalcarriessomesortofinjuriousrecessivegenes,andthispracticeinsuresthattheywillbespreadthroughoutthewholebreed,withresultingdisappointmentasthedescendantsofthesechampionsareeventuallybredtogetherandtherecessivetraitsbegintoshowupinlargenumbers.Thebreedobjectivesshouldnotbethedevelopmentofasingle,fixedtype—somethingwhichisonlypossiblebystrictinbreeding—butratherforthedevelopmentofapopulationvaryingwithindesirablelimitsandwithinwhichnewandmorevaluablecombinationsofgeneswillalwaysbepossible.
Thebreedingofworkingdogs.—Dogsstillperformmajorservicesasstockherders,asguidedogs,andaspoliceandguarddogs.Breedingimprovedanimalsforsuchdutiesinvolvesselectionbasedonmultiplecriteria,includingbehavior,fertility,vigor,andspecialphysicalattributesofsizeandstrength.
Anotherimportantconsiderationisthemaintenanceofuniformrearingandtrainingconditions,whichshouldbethebestavailable.Otherwise,variationbetweenindividualsmaydependasmuchormoreupontheearlyenvironmentoftheanimalasuponitsheredity.Asafirstconsequenceofaselectionprogramforgoodperformance,wewouldpredictrapidchangesinemotionalreactions.Second,becauseselectionmustbemadeonthebasisofperformanceofacomplextask,andbecausesuchaperformanceislikelytorestonaparticularcombinationofgenes,onewouldexpectthatcontinuedselectiononthisbasiswouldsoonleadtoastandstillinprogress,andthattherewouldbegreatdifficultyinfixingthedesiredgeneticcombination.Progressshouldbemademostrapidlyiftheabilitytoperformcanbebrokendownintospecificcapacitieshavingareasonablysimplegeneticbasis.Otherwise,thebreedershouldcombineselectionwithoccasionaloutcrossesinordertobringinnewcombinations,repeatingthosematingswhichappearmostsuccessful.Alargenumberofanimalsmustbeavailabletocompensateforwastefromunsuccessfulmatings.
Dogsforresearch.—Themanyadvantagesofpurebreddogswhoseentirelifehistoryisknownareobvious,andtheuseofsuchanimalsisincreasingrapidly
historyisknownareobvious,andtheuseofsuchanimalsisincreasingrapidly(Scott,Ginsburg,etal.91962).Wehavealreadypointedoutthenecessityforthesocializationofkennel-raisedanimals.Laboratory-raisedpuppiesmustalsohavetheopportunityforsocializationatthepropertimeiftheyarenottobe-
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comefearfulanduntrainable.Inaddition,theyhavethesamerequirementsforfoundationtrainingandearlyintroductiontotheenvironmentinwhichtheyaretoliveasdootherdogs.Asaminimum,suchpuppiesshouldbegivenelementaryobediencetraining,includingleashandsittraining,andanintroductiontothelaboratoryrooms,beforetheageof3or4months.
Thechoiceofbreedsdependsupontheresearchobjectives.Beagleshavebeenwidelyused,andsomeworkershaveadvocatedthatthisbreedbeadoptedasthelaboratorydog,inthesamewaythatpsychologistsusedtouseWistaralbinoratsasthestandardlaboratorystrain.Therearegoodreasonsforthechoice.Ashuntingdogs,beaglesdowellinkennelconditions.Theyareofmediumsizeandinexpensivetofeed.Havingbeendevelopedprimarilyasahuntingratherthanashowbreed,theyretainagreatdealofvigor.Theyhaveshorthair,andthereforerequirelittlegrooming.Finally,theyareoneoftheleastaggressiveofdogbreeds,sothattheycanbehandledsafelywithaminimumoftraining.Atthesametimeitshouldberememberedthatbeaglesarenotauniversaldoganymorethananyotherbreed,beingspecializedinmanyways.Toadoptonebreedasastandardlaboratoryanimalwouldbetothrowawayoneofthemainscientificadvantagesthatdogspossess—theirenormousgeneticdiversity.Forpurposesofexperimentalsurgery,forexample,someofthelargerbreedsaremoreuseful,andforpurposesofstudiesofbehaviorthehighlytrainableworkingbreedsaremoreinteresting.Inlong-termexperimentswhichrequireahighdegreeofco-operationandcontrol,trainedworkingdogswouldhaveobviousadvantages,anditshouldberememberedwhenselectingabreedthatdogsingeneralarehighlyadjustableandadaptableanimals.Almostanybreedcandowellinalaboratoryenvironmentprovidedcertainadjustmentsincareandtrainingaremadeforthatparticularbreed.
ThevigorofFihybridsbetweenthepurebreedsrecommendstheiruseinmanylaboratorysituations,andtheirnatureneedstobeexplored.Eachnewhybridisessentiallyanewbreed,asitwillpossessnewcombinationsofcharacteristicsdependingonwhethertheparentaltraitsareinheritedasdominantsorrecessives.OurFicocker-basenjihybridswerelikebasenjisintheirabilitytoclimb,likecockersintheirresponsetofood,andintermediatewithrespecttobarking.New
cockersintheirresponsetofood,andintermediatewithrespecttobarking.Newcharacteristicsarealsopossiblethroughinteractionbetweennewcombinationsofgenes.
Finallythereisapossibilityofcreatingnewbreedsespecially
selectedforresearchpurposes.Inthiscaseitwouldbewelltostartwithhybridsbetweentwoormorebreedsinordertoobtainthemaximumadvantagesfromvariation.
SUMMARY
Thetoolsoftheanimalbreederareimprovementoftheenvironment,geneticvariation,selection,andhybridization.Theresultsoftheexperimentsdescribedinthesepageshavebeentosharpenthesetoolsratherthancreatenewones.Ourexperimentshaveledtoimportantwaysofimprovingtheearlysocialenvironment,particularlybytakingadvantageofcriticalperiodsindevelopment.Wehavefoundthatgeneticvariationishighlyimportantwithinbreedsaswellasbetweenthem,sothatitshouldbepossibletotransformastrainwithinabreedintoaverydifferentsortofanimalwithinafewgenerations.Themostimportantgeneticdifferencesinbehaviorappeartobeemotionalandmotivationalratherthanthoseofcognitionorbasicintelligence.Suchtraitshaveimportanteffectsuponanytypeofperformanceandshouldrespondrapidlytoselection,providedtheanimalsareraisedunderuniformconditionsminimizingenvironmentalvariations.Superficialappearanceisnoguidetobehavior,andtheuseof"markergenes"consequentlyhaslittlevalidity.Finally,anyselectionprogramleadingtotheimprovementofbehaviormustofnecessitybeonewhichinvolvesmultiplecriteriaincludinggeneralphysicalandreproductivefitness.
Ourtwomajorexperiments,breedcomparisonandbreedintercrossing,donotinthemselvesyieldablueprintfordogbreeding,buttheydofurnishguidesforpersonsinterestedinselectingforbehavioralcharacteristicsorinproducingworkingdogs.Theauthorshopethatthisby-productoftheirresearchwillbeofvaluetothelargegroupwhofindpleasureintryingtounderstandman'sfour-footedcompanion.Aswillbeseeninthenextchapter,anunderstandingofdogsalsohelpsthosewhosechiefinterestisunderstandingman.
THEEVOLUTIONOFDOGSANDMEN
INTRODUCTION
Whendogswerefirstdomesticated,someeighttotenthousandyearsago,theybecameapartofhumansociety,andtheyhavesinceundergonemostoftheculturalandenvironmentalchangesthathaveaffectedtheirmasters.Dogs,however,haveshorterlivesthanmen,andtheygothroughnewgenerationsattheapproximaterateofoneineverytwoyearsinsteadofman'soneintwenty.Wecanroughlyestimatethatdogshavegonethroughsomefourthousandgenerationssincetheirdomesticationwhilemanhasgonethroughonlyfourhundred.Thesefactssuggestahypothesis:thegeneticconsequencesofcivilizedlivingshouldbeintensifiedinthedog,andthereforethedogshouldgiveussomeideaofthegeneticfutureofmankind,alwaysassumingthattherearenoradicalnewchangesintheconditionsofhumanliving.Inshort,thedogmaybeageneticpilotexperimentforthehumanrace.
HISTORICALPERSPECTIVE
Wolvesandmenhadmuchincommonevenbeforedomesticationtookplace.Justasthelioninthesouthernhemisphereoccupiedtheecologicalpositionofthedominantcarnivorepreyingontheherdmammals,sodidthewolf,Canislupus,inthenorthernone.Onceearlymenhadinventedthespearandthebowandarrow,theytoocouldsuccessfullyattackandpreyuponthelargeungulatessuchasdeer,mountainsheep,andbison.StoneAgehuntingtribessoonfoundthemselvesindirectcompetitionwithwolvesforsimilarprey.
Furthermore,aswehavepointedout,bothwolvesandmenaresocialspecies,showingagreatdealofco-operationandmutually
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helpfulbehaviorwithintheirowngroups.Finally,asanecologicallydominantanimal,withnoothercompetitorsexceptman,thewolfshowssomepolymorphism,ashumansdo,inadditiontotheusualdivisionofsocialanimalsintomales,females,andyoung.Wildwolvesshowenoughvariationinform,color,andbehaviorthatMurie(1944)couldeasilyrecognizeeachmemberofawildwolfpack.
Adaptiveradiation.—Whenananimalspeciesmovesunopposedintoanewenvironment,thereisanopportunityforveryrapidgeneticchange,becauseeachsmallgrouppopulatesalargeareawithitsowndescendants,whichinturnreflecttheindividualgeneticpeculiaritiesoftheirparents.Atthesametime,thereisarapidselectionforthoseanimalsbestadaptedtothenewareas.The
thereisarapidselectionforthoseanimalsbestadaptedtothenewareas.Thewholeprocessiscalledadaptiveradiationandisthesortofthingwhichoncehappenedtothewholeclassofmammalsafterthereptileshadbeeneliminatedaspossiblerivals.
Adaptiveradiationonasmallerscaleseemstohavetakenplacesoonafterthedogbecamedomesticated.Withinthevarioushumansocieties,dogsfoundawholenewhabitat.Thedog,asoneofthefirstdomesticanimals,wasaremarkablesocialinvention,bothforprotectionandasanaidtohunting,andeverytribemusthavewantedtogetholdofone.Inthiswaydogsspreadrapidlyovertheworld,differentiatingastheymoved,andsoproducedthesouthernshort-hairedvarietieslikethedingoand,attheoppositeextremeoftheirrange,thenorthernEskimodogswhicharealmostlikewolves(seeFig.2.2).Afurthermultiplicationofhabitatswasprovidedwhentheherdanimalsweredomesticated.Nowdogswereneededtoprotecttheseherdsagainsttheirowncloserelatives,thewolves,whichfoundthedomesticbeastseasyprey.
Thedomesticationofanimalsandplantsproducedanothermajorenvironmentalchange.Huntingwasnolongeraprimaryoccupation,butasportandfrequentlyaluxuryoftherich.Underthesecircumstancesdogsbecamespecializedforthehuntingofmanydifferentanimals.Stillanotherexpansionofhabitatsoccurredaftertheindustrialrevolution,withtheuseofdogsaspetsandsocialcompanionsforcitydwellers.However,noneoftheselaterdevelopmentshadtheimportanceofthefirstmajorexpansionintothenewenvironmentprovidedbyhumansocieties.
Periodofisolation.—AsWright(1950)andothergeneticistshavepointedout,anidealsituationforrapidgeneticchangeisoneinwhichapopulationisdividedintosmallsubpopulationswithcontactspermittingoccasionalgeneexchangesbetweenthem.When
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dogswerefirstdomesticated,thiswasstillthesituationinthemajorityofhumansocieties,whichweredividedintosmallsemi-isolatedtribes,stillreflectingtheconditionswhichhadledtotheveryrapidbiologicalevolutionofmodernmaninthepreviousfiftythousandyears.
Dividedamongtribes,dogsweremaintainedinevensmallersocialgroupsthantheirmasters,withonlvoccasionalopportunitiesformixingwithanimalsfromadjacenttribes.Undertheseconditionswewouldexpectrapiddifferentiation
adjacenttribes.Undertheseconditionswewouldexpectrapiddifferentiationbetweensubpopulations,andthiswasprobablythefoundationofthemajorbreeddifferences.HistoricalrecordsofAmericanIndiantribesshowthateachonehaditsownparticularbreedofdog,perhapsnotverydifferentfromthatoftheneighboringtribebutgreatlydifferentfromthoseatlonggeographicaldistances(Allen,1920).UndersimilarconditionsinancientEurasiathereoriginatedthelargewardogsofonetribe,thelong-leggedgreyhoundsusedforhuntinggazellesonthedeserts,andtheshepherddogsusedtoguarddomesticflocks.
Periodofpanmixis.—Theperiodoflocalisolationwassucceededbyoneinwhichnewmethodsoftransportationbroughtexplorersandimmigrantstogetherfromallovertheworld.WherevertheEuropeanexplorerswent,whetherfortrade,discovery,orwar,theybroughttheirownbreedsofdogs,whichreadilyinterbredwiththenativevarieties.Sometimesthenativebreedsdisappeared,astheydidinAmericaandSouthAfrica.SometimestheEuropeansbroughtnewbreedsbacktotheirshores,asthecrusadersbroughtthegreyhoundsbackfromtheMiddleEast.Ineithercase,thiswasaperiodofmixingandcrossing.
Periodofgeneticcontrol.—Theideaofintensifyingandpreservingdesirablecharacteristicsindogsthroughscientificbreedingishardlymorethanacenturyold,thefirstdogshowhavingbeenheldinNewcastle,England,in1859(Ash,1924).Beforethistimedogsweremainlyproducedandbredonthebasisofresults,nomatterwhattheirancestorsmightbe.Inthelatterpartofthe19thcenturypeoplebegantoappreciatethepossibilitiesofartificialselectionandbegantryingtokeepdogpopulationscompletelyseparateinthemodernpurebreeds.Theseattemptsatgeneticchangeandimprovementwerenotalwaysscientificorcompletelyeffective,buttheyhaveresultedinanewdiversityofdogpopulations.Manyofthemodernbreedswereoriginatedwithinthepastcentury,havingbeenproducedbycrossingolderbreedsandthenselectingtheirdescendantsforspecialcharacteristics.
Geneticchangesinhumanpopulations.—Thefirstthreeofthe
aboveperiodscanalsobefoundinthehistoryofhumanpopulations,althoughextendedovergreaterlengthsoftime.Themodernhumanraces,withlighterskinnedpeopleconcentratedtowardthenorthernpolarregionandthedarkeronestowardtheequator,probablyrepresenttheresultofanancientperiodofadaptiveradiation.Theperiodofisolationintosmalltribeswasonewhichbegantodisappearwiththedawnofcivilizationsomeeightortenthousandyearsago.Aspeoplemovedintocities,theybegantoliveinlargerpopulations,andthesepopulationsbegantobecontinuouswithandmixwithadjacentones.Inmoderntimesthisprocessofpanmixisisstillaccelerating,withpeoplemovingrapidlyovercontinentsandtheentireworld,leavingtheirdescendantseverywhere.
Aperiodofscientificbreedingofhumanpopulationsisyettocome,butthebeginningsarealreadybeingmade(Hammond,1959;Reed,196-3).Asweaccumulateauthenticinformationabouttheinheritanceofgeneticdefectsandotherqualities,prospectiveparentsarebeinggivenadviceaffectingtheirdecisionstohavechildren.Moreover,whetheritisbasedonscientificinformationornot,theculturalhabitoffreechoiceinmarriageleadstoassortivemating.Thereisconsequentlyastrongcorrelationbetweenbodysize,appearance,andevenintelligencetestsbetweenhusbandsandwives.Whatdoesthefuturehaveinstore?Onepossibleanswerisgivenbythecaninepilotexperiment.
THERESULTSOFGENETICCHANGE
Diversityofformandbehavior.—Ourfirstproblemistoassesswhathashappenedtothedogasaresultoflongmembershipinhumansociety.Themostobviousthingisanextraordinarydiversityofformandbehavior.Wenowhavedwarfbreedswhichweighlessthanfourpoundsatmaturity,andgiantbreedsliketheGreatDanesandSaintBernardswhichweighatleastasmuchasthelargestnorthernwolves.Thereareallsortsofvariationsinhairstructureandcolor.DensityrangesfromnearabsenceintheMexicanhairlessbreedtoheavycurlsintheevergrowingcoatsofpoodles.Hairmaybewiryorsilkv,curlyorstraight,andappearinalmostanycolorofthevisiblespectrumwiththeexceptionofgreen.Earscanbeerectordroopingandallgradationsbetween.Tailscanlieshortorlongandvaryfromasickleshapetoatightcurl.Legsalsocanbeshortorlong,andtheskullcanbedeformedandshortenedasinbulldogs,orlongandnarrowasinthegreyhounds.Theonlythingwhichremainsrelativelyinvariableisgeneralbodvform.Asidefromocca-
sionalobeseindividuals,allbreedsretainthelargechestandthinwaistoftheirancestors.
Suchwidevariabilityisalsocharacteristicofhumanbeings,amongwhomthereiswidevariationofskinandhaircolor,shapeoffacialfeaturessuchasearsandnose,and,unlikedogs,ingeneralbodyproportions.Ifhumanbeingsaremorevariablethandogsinsomeways,theyarelesssoinothers.Forexample,aGreatDanemayweighfortytimesasmuchasaChihuahua.Nothinglikethisextremediversityisfoundinthehumanspecies,wherethelargestadultsmaybeonlyfourorEvetimesheavierthanthesmallest,exceptforcasesofextremeobesityanddwarfism.
Thisgeneticdiversityofmen,dogs,andotherdomesticanimalscontrastsgreatlywithwhatweseeinmostwildanimals.Itisalmostimpossibletotellonesquirrelfromanotherofthesamespeciesbyoutwardappearance.Infact,thisdifficultyoftellingindividualsapartisoneoftheperpetualproblemsofstudyinganimalsociologyundernaturalconditions.Weassumethatuniformityisaresultofnaturalselection;thatmutationswhichproducewhitespotting,forexample,makeasquirrelsoconspicuousthatheismuchmorelikelytobetakenbyapredatorthanarehisstandard-coloredrelatives.
Inaspeciesnotsubjectedtointensiveselectionbypredators,agreatervarietyofindividualscansurvivewithoutdifficulty.Furthermore,inahighlysocialanimalmanysortsofnewvariationswillbeprotectedbygroupaction.Inshort,theconditionofbeingahighlysuccessfulsocialspeciesautomaticallyresultsina
conditionofbeingahighlysuccessfulsocialspeciesautomaticallyresultsinarelaxationofnaturalselection,permittingagreatervarietyofindividualstoexist.
Wemaywonderwhythetendencytowarddiversityhasgonetogreaterlengthsinthedogthaninman.Therearetwopossiblereasons.Oneisthatthedoghashadmoregenetictime,intermsofgenerations,toshowtheeffectsofrelaxednaturalselection.Theotheris,ofcourse,thatpeoplehavedeliberatelypreservedandmultipliedharmfulcaninemutationsasobjectsofcuriosity,inawaywhichhasneverbeendonewithhumanmutants.Wemightthenconcludethatthedogisgeneticallyweakcomparedtotheancestralwolf,andthatweoughttoattempttorestorethemoreuniformappearanceandgreatervigorcharacteristicoftheseancestralanimals.Isthisconclusionreallyjustified?
Modificationoffertility.—Comparedwiththewolf,dogsaregenerallymorefertilethantheirwildancestors.Wolvesmatureattwoyearsofageandsometimeslater,andtheaveragelittersizeisfourorfive.Thisprobablyrepresentsthenumberofanimalswhichcanbesuccessfullyrearedtomaturityundernaturalconditions,
wherefoodmustbeprovidedbyhunting.Dogsofmostbreeds,ontheotherhand,becomesexuallymaturebeforeoneyearofageandhavedevelopedatwice-yearlybreedingcycleinsteadofanannualone.Thismeansthatapairofdogshasthepotentialityofproducingtwiceasmanyoffspringasapairofwolves.Medium-sizedbreedsusuallyproducelittersaboutthesamesizeasthoseofwolves,butthelargerbreedsexceedtheproductionofwolvesontheaverage.Againstthis,thedwarfbreedsproducesmalleraveragelittersthandowolves.Also,whilewehavenostatisticsonthis,thereareprobablymorecasesofcompleteinfertilityamongdogsthanamongwolves.
However,wecansayingeneralthatdomesticationandbecomingapartofhumansocietieshasnotonlyextendedtherangeoffertilityindogsbutactuallymadedogsmorefertilethantheirancestors.Suchhighfertilitywouldbeadisadvantageundernaturalconditionsbecauseofthedifficultyofraisingthepuppies,butinahumansociety,wherethepuppiesarepartiallyraisedbyhumanbeings,itisactuallymoreefficienttorearalargelitterthanasmallone,sincetheamountofworkrequiredisroughlythesame.
Reductionofwildness.—Ifawolfpuppyistakenfromitsparentsbeforeitseyesareopenandisadoptedintoahumansociety,itwilldevelopverymuchlikeadomesticdog.However,adoptionbecomesrapidlymoredifficultasthe
likeadomesticdog.However,adoptionbecomesrapidlymoredifficultasthewolfcubsgrowolder,becauseofthequickdevelopmentoffearreactionsandfightingbehavior.Anolderwolfcubbitesinfranticfearwhencaught.AlthoughGinsburg's(1963)recentworkhasshownthatevenadultwildwolvescanbesocializedeventually,thisisalonganddelicateprocess.Therehasevidentlybeenselectionindogstowardtheextensionofthecriticalperiodduringwhichsocializationiseasy.Theremayalsohavebeensomereductionofalertnessandwarinessofstrangesoundsandmovements,butthisisdoubtful,becauseoneoftheprincipalvaluesofdogsisjustthiscapacity—toalertthehouseholdertopossibledangers.Infact,aperennialprobleminmostbreedsisthedevelopmentofmoretimiditythanthebreedersconsiderdesirable.
Thespecializationofbehavior.—Inalmostanybehavioralcharacteristictherearebreedsofdogswhichsurpassthecapacitiesofwolvesineitherdirection.Theterrierbreeds,asevidencedbytheirincapacityforlivinginlargegroups,aremoreaggressivethanwolves,whereasthehoundbreedslikethebeaglesarefarlessaggressive.Greyhoundsarefasterrunnersthanwolves,butmanydogsarcmuchslower,especiallythosefromshort-leggedbreedssuchasthedachshund.Somebreedslikethetrailhoundsappearto
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bebettertrackersthanwolves,whereasothersliketheterriersappeartobepoorer.Thesheepdogsarebetterherdersthanwolvesand,ofcourse,manybreedsaremuchpoorer.Thesetters,pointers,spaniels,andotherbirddogsappeartohavemuchmoreinterestinbirdsthandowolves,aspecialcapacityusefulonlywithhumanco-operation.Wolvesthemselvesarepoorbirdhunterscomparedtofoxes.
Althoughmanvbreedsofdogsconsistentlyexceedwolvesintheircapacities,noneofthemcanbeconsideredsuper-wolves.Theirspecialcapacitieshavebeenachievedatthepriceofsacrificingothers.Thegreyhoundhasachievedspeedbysacrificingtheheavymusclesandjawswhichenableawolftoliveonbonesifneedbe.Itisinconceivablethatanyparticulardomesticbreedcouldcompetewithwolvesundernaturalconditions,withthepossibleexceptionoftheEskimodogs.Eventhesewouldbeatadisadvantagebecauseoftheirsmallerteethandjaws.Infact,dogshavesuccessfullygonewildagainonlywherethereisanabsenceofsuchcompetition,asonthecontinentofAustraliaoraroundtownsandcities.
Noneofthedogbreedsaresuper-wolves.Awolfisaruggedandpowerful
Noneofthedogbreedsaresuper-wolves.Awolfisaruggedandpowerfulanimaladaptedtolifeunderavarietyofadverseconditions.Consequently,nooneofhisbehavioralcapacitiescanbedevelopedtoahighdegree.Comparedwithwolves,dogsareagroupofspecialists.Butastheyareco-ordinatedandshelteredbyhumansocietytheycanperformtheirfunctionsmoreefficientlythananygroupofwolves.
Wecanconcludethatthedevelopmentofall-roundcapacitiestomeetavarietyofenvironmentalconditionsleadsnottoasuperbdevelopmentofthesecapacitiesbuttoabalancebetweenthem.Anall-rounddevelopmentmeansgreatadaptability,butnotsuperbperformance.
Thissuggeststhattheideathatnaturalselectionwillproduceasuper-manorsuper-animalofanysortisanunobtainablemyth.AsfarbackastheGreeks,andpossiblylongbefore,peoplehavedreamedofgodlikeorheroicfigureswhocombinedthephysicalstrengthofagorillawiththeintelligenceofanEinstein,themusicalgiftsofaBeethovenwiththebeautyofaGreekGod.Fromthehistoricalandgeneticevidenceaffordedbydogs,thisappearstobeanimpossibility,andwearenowbeginningtorealizewhy.Ontheotherhand,acomplexsocietycanuseallthesesuperbqualitiesintheformofspecializedindividuals,sothatthesocietyasawholehascapacitiesfarbeyondthoseenjoyedbyauniformlydevelopedgroup.Thesuper-manisnottobefoundasanindividualbutasawell-developedhumansociety.
THEACCUMULATIONOFMUTATIONS
AlmostassoonasDarwinputforwardhistheoryofnaturalselection,scientistsbegantoreasonthatifnaturalselectionwouldcausetheimprovementofaspecies,thentherelaxationofselectionwouldautomaticallycausedegeneration.Theargumentseemedplausibleenoughbecause,ifunfitindividualswerenoteliminated,thereoughttobemoreoftheminthenextgeneration,andifthisprocesscontinuedgenerationaftergeneration,theresultwouldeventuallybegeneticdisaster.However,thisideafirstbecamecurrentbeforethediscoveryofMendeliangeneticsandlongbeforewehadanyideaoftheprocessofmutation.Asweshallseebelow,therelaxationofnaturalselectiondoesnotnecessarilyleadtodegeneration.
TheHardy-Weinberglaw.—OncethemechanismofMendelianheredityhadbeendiscovered,itwaspossibletomathematicallycalculateitseffectuponfuturegenerations.Allchromosomesexistinpairs,andthereisanequalprobabilitythatoneortheotherofeachpairwillbepassedalongtoan
probabilitythatoneortheotherofeachpairwillbepassedalongtoanindividualinthenextgeneration.Inaninfinitelylargepopulationwithnoselectionandnoassortivemating,genescarriedonthesechromosomeswillthereforebepassedalonginexactlythesameproportionasthatexistingintheparentpopulation.TheMendelianmechanismhasthefunctionofrecom-biningthesegenesinallpossiblecombinationswithoutchangingtheirfrequency.Thisprinciple,knownastheHardy-WeinbergLaw,maybebrieflystatedasthatof"theconstancyofgenefrequency."
Therefore,thereisnothingintheordinarymechanismofinheritancetocausedegeneration.Ifnaturalselectionceasestoactuponalargepopulation,thehereditypresentinthegroupatthistimewillbepassedalongwithoutchangefromonegenerationtothenext,fromthattimeforward.Theresultisneitherdegenerationnorimprovement,butstability.
Thesituationisslightlydifferentinasmallpopulation.Heretheaccidentalselectionofonekindofparentsmayproduceashiftinheredityfromonegenerationtothenext,butthechangeisaslikelytobeinthedirectionofimprovementastowarddegeneration.InaLargepopulationcomposedofanumberofsmallsubgroups,wewouldexpectthatsomewouldbeimprovedandsomeworsened,willithewholepopulationremainingexactlyasbefore.
ThusneithertherelaxationofnaturalselectionnortheoperationoftheMendelianmechanismofhereditywillleadtoprogressive
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geneticdeterioration.Theoneremainingpossibilityofdegenerationliesintheprocessofmutation.
Theeffectofmutationonthedog.—Thedogprovidesanextremeexampleoftheunfavorableeffectsofmutation.Notonlyhasselectionbeenrelaxedbecausedogownersprotectandfeedtheirpetsfromthekenneltothegrave,butfanciershavepracticedbreedingsystemswhichactuallyincreaseandmultiplyinjuriousmutations.Inthefirstplace,theyhaveselectedcertainfreakishtraits,suchasthebulldoghead,whicharedefinitelyinferiortothenaturalconformation.Second,theyhaveselectedforneutraltraitssuchascoatcolorwithoutregardtoviabilityandfertility.Thebestlookingshowanimalinalittermayaccidentallybeapoorbreederorsubjecttovarioussortsofsickness.Third,inrecenttimesmostdogbreedershavedeliberatelyfollowedapolicyofoutbreeding,tryingvarioussorts
breedershavedeliberatelyfollowedapolicyofoutbreeding,tryingvarioussortsofmatingsbetweennon-relateddogsinthehopeofobtaininganunusualordesirabletype.Forpracticalpurposesthisisagoodwaytochangeorimproveabreed.However,continuousoutbreedingalsotakesawaythenaturalmethodofreducingthenumberofinjuriousrecessivegenes,i.e.,throughdeathorinfertilityofhomozygousindividuals.Underthesebreedingmethodssuchrecessivegeneswillnotevenberecognizedunlesstheybecomesofrequentinthepopulationthatcarriersbegintomatewitheachother.AccordingtotheHardy-WeinbergLaw,thereshouldbenospreadofsuchmutationsthroughthepopulation,butthedogbreedershaveprovidedamethodfordoingjustthis.Ifamalebecomesagreatchampion,everyonewantsoneofhispuppies,andhemaybebredtoseveralhundredfemales.Ifhecarriesevenonerecessivegene,itwillbespreadthroughoutthewholebreedinsuchnumbersthatitwillbealmostimpossibletoeliminatewhenhisdescendantseventuallybegintobematedwitheachotheranditisfinallyrecognizedasaseriousproblem.Thuscurrentdogbreedingpracticescanbedescribedasanidealsystemforthespreadandpreservationofinjuriousrecessivegenes.
TheseriousnessofthiseffectiswellillustratedinTable16.1.Inthepurebreeds,theneonataldeathrateaveragesabout15percent.Thisis,ifanything,anunderestimateofmortalityratesinthetotalbreedpopulations,sincefemaleswithunusuallygoodbreedingrecordswereselectedforourexperimentwheneverpossible.TheFihybridsshowedonlytwoneonataldeaths,bothstillbirths,andthemortalityrateinthesegregatinghybridsisintermediatebetweentheFi'sandthepurebreeds.AssumingthattheFideathswerecausedby
GENERALIMPLICATIONS
TABLE16.1MortalityRateper100BirthsenPureBreedsandHybrids
Excludingfiveanimalswhichdiedindistemperepidemic.
environmentalaccidents,wecanestimatethatthegeneticdeathrateis10to12percent.Estimatesfromothercoloniesgiveneonataldeathratesofanywherefrom10to30percent(Corbinetah,1962),dependinguponthestrainofanimalsinvolved,sothat15percentshouldbeagoodroughestimateofneonatalgeneticmortalityforpurebreedsingeneral.
Inadditiontotheselethaleffects,thereiswidespreadoccurrenceofcripplingdefectsanddeformitiesinpurebreddogs.Inourexperimentswebeganwith
defectsanddeformitiesinpurebreddogs.Inourexperimentswebeganwithwhatwereconsideredgoodbreedingstocks,withafairnumberofchampionsintheirancestry.Whenwebredtheseanimalstotheircloserelativesforevenoneortwogenerations,weuncoveredseriousdefectsineverybreed.Asmentionedinthelastchapter,ourAfricanbasenjisshowedahighfrequencyofundershotjawsinbothsexesandofinguinalherniainthemales.Beaglesshowedanoppositedefect—areductionofthelowerjaw.Untilcorrectedbvselection,wire-hairedfoxterriersproducedmanypuppieswithclubfeet.TheShetlandsheep-dogsproducedindividualswithhereditaryobesity.Allbreedsshowedatendencytodeclineinfertility.'
Inaddition,thecockerspanielsshowedanoutstandingdefectwhichhadapparentlybeenestablishedthroughoutthestrainbeforewereceivedit.Thisbreedhasbeenselectedforabroadforeheadwithprominenteyesandapronounced"stop,"oranglebetweenthenoseandforehead.Whenweexaminedthebrainsofsomeoftheseanimalsduringautopsy,wefoundthattheyshowedamilddegreeofhydrocephaly;thatis,inselectingforskullshape,thebreedershad
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accidentallyselectedforabraindefectinsomeindividuals.Besidesallthis,inmostofourstrainsonlyabout50percentofthefemaleswerecapableofrearingnormal,healthylitters,evenundernearlyidealconditionsofcare.
Amongotherdogbreeds,suchdefectsarequitecommon.Onewhichhasrecentlyreceivedagreatdealofattentionishipdysplasia,particularlyinGermanshepherds,butalsofairlycommonlyinotherbreeds.Inthisdefectthehipjointisnotproperlydeveloped,withtheresultthattheanimalsbecomelameandcrippled.IntheGermanshepherdbreeditisassociatedwiththefactthattheshowbreedershavepreferredasortof"downhill"carriage(associatedwith"angulation"ofthehindlegs)inwhichtheshouldersarehigherthanthehips.Inselectingforthistraittheymayhaveunwittinglyselectedforlamedogs.
Anotherexampleishereditarvhemophilia,whichhasbeendiscoveredinEnglishsetters.Indeed,almostanyimportantconstitutionaldiseaseofhumanbeingshasitscounterpartindogs,whichareconsequentlyhighlyusefulformedicalstudy.Alltheevidenceisinfavoroftheconclusionthatinjuriousrecessivemutationshaveaccumulatedinthedogandbecomeextremelvcommon.Atthesametimethereisnoindicationthatdogsarebecomingextinctasaresultofgeneticdeterioration.Ifanything,therearemoredogstodaythaneverbefore.
deterioration.Ifanything,therearemoredogstodaythaneverbefore.
Thetheoryofgeneticequilibrium.—Thehereditarycompositionofanywildspeciestendstoreachaconditionofbalance,insofarasthevariousfactorsproducinggeneticchangeworkagainsteachother.Forexample,theincreaseofinjuriousrecessivemutationsreachesastateofbalancewiththedeathrateofhomozygousindividuals,andthefrequencyofappearanceofhomozygotesdependsuponthedegreeofinbreedinginthepopulationaswellasonthemutationrate.
Inthecaseofthedomesticdogasimilarbalanceseemstohavebeenreached.Onereasonwhydogsarenotdisappearingisthat,althoughabout50percentofthefemalesareunabletoproducelivingyoung,reproductionbyafertileanimalisapproximatelydoublethatoftheancestralwolves.Thecaninereproductiveratefarexceedsthatforhumanbeings,asagoodbitchmayeasilyproduce50livingoffspringbythetimesheis6yearsold.Thisincreasedreproductivecapacitymorethancompensatesforthegeneticlossoffertility.
Inspiteoftheaccumulationofrecessivemutations,thereisstillselectionagainstabnormalindividuals.Extremelydefectiveindi-
victuals,suchasdogswithhereditaryobesity,areoftencompletelyinfertile.Thosewithminordefectssuchasundershotjawarefrequentlynotchosenforbreedingstock,anddogbreedersarebecomingmoreandmoreawareofthenecessityofselectingforgoodhealthandvitalityaswellasparticularshowpoints.Inshort,eveninahighlyprotectedspecies,naturalselectionisnotcompletelyinoperable,nordoesartificialselectionalwaysworkagainstit.
Wecouldmakeanotherpointinpassing.Adogwhichisinfertileorunsuitableforbreedingmaystillmakeahighlysatisfactoryhousepetorevenoccasionallybeanoutstandinglysuccessfulperformerasaguidedog,hunter,orherder.Inasocialanimal,orananimalsuchasthedogwhichisactuallypartofhumansociety,reproductivityisnotthesolecriterionofusefulness.
Wecanconcludethattherelaxationofnaturalselectioninthedoghasnotproducedacontinuingprocessofdegenerationbutratherhassetupanewconditionofgeneticbalancewhichpermitsawiderdegreeofvariation.
Thetheoreticaldangerfrommutations.—Fromthestudyoffruitfliesandmice,geneticistshavebeenabletocalculatemutationrates.Somegenesmutatefairlyfrequentlyandothersalmostnever.Theaveragerateseemstobeaboutone
frequentlyandothersalmostnever.Theaveragerateseemstobeaboutonemutationinaparticulargeneforeverymillionindividuals.Mutationscanalsobeinthereversedirection;anewmutationwilloccasionallyreverttotheoriginal.Theaveragerateispresumablythesameineitherdirection,andwecanhypothesizethatifamutationhadnoeffectonsurvivalandwasthereforenotremovedbynaturalselection,theprocessofmutationwouldgoonuntilthereversemutationratebalancedtheoriginalrate,whichshouldbeatthepointwheretherewouldbeequalnumbersofthenewmutationandtheoriginalgene(Wright,1955).
Thiskindofmutationmaybeverycommon,butusuallyescapesnoticebecauseamutationwhichhaslittleeffectonsurvivalis,ofcourse,onewhichhaslittleeffectofanykind.Themutationswhichwenoticearethosewhichproducelargeeffects,andthesearealmostuniversallyinjurious.Ifsuchaninjuriousgeneshouldoccurinashigharatioasinthehypotheticalexampleabove,inwhich50percentofthegenesinthepopulationwereofthemutantsort,therewouldbe25percentofdefectiveindividualsineverygeneration.Ifthesedefectiveindividualswereascapableofreproductionasnormalanimals,thesamehighproportionofdefectiveswouldbemaintainedinfuturegenerations.Theconsequencewouldbeacontinuingheavyburdenonthepopulation.
However,allourevidenceindicatesthatdefectiveindividuals,
EVOLUTION409
whiletheymayoccasionallybeabletoreproduce,arealwaysselectedagainstandfrequentlyarecompletelyinfertile.Ifthewhole25percentofdefectiveindividualsinapopulationwereincapableofreproductioninthenextgeneration,one-halfofthenormalgeneswouldhavetomutateineachgenerationinordertomaintainanequalratioofmutantandnon-mutantgenes.Thisisatremendouslyhighmutationratecomparedwithoneinamillionor,indeed,withanythingthathasbeenproducedartificiallybyradiation.
Manyscientistsareconcernedwiththegeneticeffectsuponhumanpopulationsofincreasedexposuretoradiation,eitherinmedicalpracticeorthroughtheuseofatomicweapons,orevenbyexposuretoradiationinouterspace.AccordingtoCrow(1961),anyincreaseinthemutationrateoverthenaturaloneisabadthing,asitwillinthelongrunincreasethenumberofseriouslydefectiveindividualsinourpopulation.Togivesomeideaofwhatthisincreasemightmean,Morton(1960)hascalculatedtheeffectofdoublingthemutationrateforcertaindefects,untilaconditionofequilibriumisreached.Themutationratecan
certaindefects,untilaconditionofequilibriumisreached.Themutationratecanbedoubledwiththesurprisinglylowradiationdoseof25roentgenspergeneration.Whenanirradiatedpopulationofonemillionpeoplehadreachedstability,therewouldbeanincreaseofatleast60casesoflimb-girdlemusculardystrophy(adiseaseinwhichthemuscleswasteaway),450casesofdeafmutism,and1,370casesoflow-gradementaldeficiency—anincreaseofsome1,880defectiveindividualsinjustthesethreecategories.
Anincreasedmutationratewould,ofcourse,greatlyincreasetheprenatalandpostnataldeathratesofhumaninfants.Wearestillagreatdealbetteroffthanpurebreddogs.In1960thecombineddeathsatbirthanduptooneyearofagewerelessthanoneineverytwentylivebirths,whilethecorrespondingfiguresinpurebreddogswereaboutoneinfive(Table16.1).Withincreasedmutationrates,wecouldexpecttheneonatalandinfantiledeathratestorisetoamuchhigherlevelthanatpresent.
Wehavebeenthinkingofthedogasbeingapilotexperimentforthegeneticfutureofthehumanrace.However,humanheredityneednotfollowthesamecourse,becausewecanatleastavoidthemistakeofspecialselectionofdefectiveindividualsforparents.Theexampleofthedogissomewhathopeful,inspiteofalltheunfavorablechangesthathavetakenplace,becausethespeciescontinuestoflourish.Byanalogy,wemaypredictthathumanhereditywilleventuallycomeintoanewconditionofbalance,dependingonthenatureoftheforcesforchange.
Withregardtofertility,oneofourmostimportantworldprob-
lemsisthatofincreasedhumanfertilityproducedbysuperiornutritionandmedicalcare.Thereisnoindicationthattherehasbeenanygeneticincreaseinfertility,asinthedog.Ontheotherhand,weknowthatatthepresenttimeabout10percentofmarriagesintheUnitedStatesareconfrontedwiththeproblemofsterility.Wemayexpectthatifmutationratesincrease,thepercentageofsterilitywillgraduallyriseandwillintimereachabalancewhichwouldcancelouttheincreasedsurvivalrate.However,itmighttakecenturiesbeforesuchbalanceisactuallyachieved.
Thechangesproducedbyincreasedmutatationratesmustbeslow,forevenifnaturalselectionisrelaxedinanypopulation,itiscertainlynoteliminatedandmayevenbeincreasedinsomerespectsthroughthespecialstressesofcivilizedliving(Dobzhansky,1962).Thereisalwaysselectionagainststerility.Morethanthis,theimprovementoftheenvironmentachievedbysocialandcivilizedliving
this,theimprovementoftheenvironmentachievedbysocialandcivilizedlivinghasmadeverylittlechangeintheprenatalenvironment.Theusualestimatesindicatethatthereisaprenatalmortalityrateofapproximately20percent,thatoneoutoffivepregnanciesnevercomestoterm.Therealratemaybeevenhigher,sincemanyembryosdiesosoonthattheirexistenceisordinarilyneverdetected.Figuresforsomeofthedomesticanimalsindicateaprenatalmortalityrateof30to40percent.Prenatallifeisthereforethemajorscreeninggroundforinjuriousmutationsandonewhichisnotlikelytobeseriouslyinterferedwithinthefuture.Theprenataldeathratealsoindicatesthatthereareactuallyalargenumberofinjuriousmutationsalreadypresentinhumanpopulations(Mortonestimates3to5perindividual),andthatthereisstrongselectionagainstthem.
Togetthewholematterintoperspective,therelaxationofselectionchieflyaffectspostnatallife,afterthemostimportantpartofselectionhasalreadytakenplace.Eveninpostnatallife,naturalselectionhasnotbeeneliminated.Parentswhohaveadefectivechilddonotrecklesslyhavemanymore,beingstronglydeterredbytheinevitabletragedyandexpense.Itusedtobethoughtthatwewereselectinginfavoroffeeblemindedindividuals,andthatmoronswouldbreedlikerabbits.AsReed(1963)hasshown,theactualfiguresindicatethatwhiletheremaybeafewexceptionalfeeblemindedpersonswithmanychildren,theaveragefeeblemindedindividualhasfarfewerchildrenthantherestofthepopulation.Furthermore,thenearrelativesofsuchpersonsalsohavefewerchildren.
Inshort,wemayconcludethattherelaxationofnaturalselectioninhumansocietiesliasnotsetintomotionacontinuingprocessof
degenerationbuthasrathersetupanewconditionofequilibriumwhichpermitsawiderdegreeofvariation.Inaddition,weshouldrememberthatsomeofthesevariantsmaywellhavespecialabilitiessuperiortotheidealofanall-roundman,insteadofbeinginvariablybelowtheaverage.
Wehavealreadyshownthatselectivebreedinghasnotproducedasuper-wolfamongdogs,andwemightpredictthatifanyoneshouldattempttoselectabreedofmenhavingall-roundability,health,andvigor,hewouldprobablyproducenotagroupofsupermen,butaveryaveragegroupofindividualswithnoexceptionalqualities.Inessence,suchpeoplemightindeedbeverysimilartoStoneAgemen,butwehavenoindicationthatprimitivemenwereanythingotherthanextremelytoughindividualswhocouldsurviveundermanyconditions.Bycontrast,ourpresentsituationwithitsrelaxationofselection
conditions.Bycontrast,ourpresentsituationwithitsrelaxationofselectionpermitsthetryingoutofalmostinfinitenumbersofgenecombinations,andsomemodernindividualsmaywellbesuperiorinall-aroundabilitiestothebestthatStoneAgemancouldoffer.However,underourpresentcircumstancesoflargepopulationsandpanmixis,thesegenerallysuperiorindividualsareunlikelytoproduceanewraceofmen.Iftheyappear,theywillmakeasocialratherthanageneticcontributiontothefuture.Eveninthisrespect,theirsocialvalueislikelytoberelativelysmallcomparedtothatofindividualswithmarkedlysuperiorspecialtalents.
Presentconditionspermitthesurvivalofsociallyvaluablebutgeneticallyspecializedindividuals,lackingtheall-roundsurvivalcapacitiesofStoneAgeman,butpossessingextremelysuperiorspecialqualitieswhichcanbeusedtogoodadvantageinahighlydevelopedcivilizedsociety.
Humansocietyisthusbasicallypolymorphic(Dobzhansky,1962).Aswithothersocietiesofmammals,wearebiologicallydifferentiatedintothreetypes:males,females,andyoung.Ahighdegreeofsocialorganizationencouragesthedevelopmentofafurtherdiversityofindividualswithinthesemainclasses.Eveninasocietyofwolves,itisanadvantagetohavebothextremelytimidandextremelycourageousanimals.Thetimidanimalmayscentdangerfromafarandwithdrawtowarntheothers,whiletheboldanimalmaypressforwardtoinvestigateandobtainfoodforthepackwhenthedangerprovestobesmall.Inahumansocietyadiversityofindividualsisevenmoreuseful.
Ahumansocietythusrestsonageneticbasisdifferentbothfromthatintheinsects,wherepolymorphismisexpressedinasmallnumberofgeneticallydeterminedcastes,andfromthatindogs,where
412GENERALIMPLICATIONS
geneticdiversityisorganizedintobreeds.Humansocietiesarefoundedonthegeneticbasisofmanyindividualdifferenceswithinthethreebiologicaltypesofmales,females,andyoung,andtheidealhumansocietyisconsequentlyonewhichrecognizes,respects,anduseshumanindividualityandvariation.
CHAPTER17
TOWARDASCIENCEOFSOCIALGENETICS
Thescienceofheredityisprimarilyconcernedwiththeactionofgenesorbasichereditaryunits.Atfirst,theprincipalproblemwastheirtransmissionfrom
hereditaryunits.Atfirst,theprincipalproblemwastheirtransmissionfromgenerationtogenerationbymeansofthechromosomes.Later,scientistsbecameinterestedinhowgeneswork,andthisproblemdevelopedintoasubscienceofphysiologicalgenetics.Anotherproblemwashowgenesaredistributedandpassedalonginnaturalpopulations,asopposedtothecontrolledexperimentsofthelaboratory.Inanswertothisquestionthesubscienceofpopulationgeneticswasborn.
Thescienceofheredityhasthusbeensubdividedaccordingtoitseffectsatdifferentlevelsofbiologicalorganization.Inordertocompletethetable,weneedtoaddtwomoredivisionsattheindividualandsociallevels.Oneconcernstheeffectofgenesontheactivityofanentireindividual.Thisdivision,whichwecall"behaviorgenetics,"istreatedinchapters7-14ofthisbook.Anotherinvolvestheeffectofgeneticsonsocialgroups,or"socialgenetics."Finally,thescienceofdevelopmentalgeneticscutsacrossalllevelsoforganization(Table17.1).
TABLE17.1TheSubdivisionsofGenetics
LevelofOrganization
Ecological
Societal
BehavioralorPsychological
Physiological
Cellular
Molecular
UnitofOrganization
Subdivision
Population
Society
Organism
Organs,tissues,etc.
Cells
Gene
PopulationgeneticsSocialgeneticsBehaviorgeneticsPhysiologicalgeneticsMendeliangeneticsChemicalgenetics
oa
GENERALIMPLICATIONS
Forthemostpartpopulationgeneticshasdealtwithtwounits:theindividualandthewholepopulation.Researchworkerssometimesassumefortheoreticalpurposesthatapopulationisunorganized,withitsmembersmovingaboutandmatingatrandom,justasagroupofgasmoleculesareunorganized.Thisassumptionmaybejustifiedinmanycases,particularlyinsomeoftheloweranimals,butthehigheranimalsarealwaysorganizedintosomesortofsocialgroupsinwhichtheyneithermovenormatecompletelyatrandom.Furthermore,insuchsocialanimalsthereisanewbasicunit,thesocialrelationship,whichmeansthattwoormoreindividualsformaunit.Anumberofrelationshipsinturnmakeupanorganizedgroup,whichmayrangeinsizefromasinglepairtoseveralhundredindividuals.Inmanyanimalseachgroupconstitutesanentiresocietyinitself,butinmanyothersthegroupshaveatleastsomeconnectionwitheachotherandareorganizedintoalargerwhole.Amonghumanbeings,suchgroupsofgroupsaremorecomplexlyorganizedandmakeupinstitutions,anditisagroupofinstitutionsthatbecomesasociety.Finally,apopulationmayconsistofasinglesocietyoragroupofsocieties,dependingonthesizeofthegeographicalunitonwhichitisbased.
Thesedifferencesbetweenvariouskindsofsocietiesmeanthatthefirstproblemofsocialgeneticsisoneofbasicinformation.Weneedtoknowtheanatomyoftheanimalsocietywithwhichwedeal:thecompositionofgroups,thenatureoftherelationshipswithinagroup,andtheimportanttypesofbasicrelationships.Withinthisframework,therearetwomajortheoreticalproblems.Oneishowgeneticsaffectsarelationshipandtheotheristhereciprocalquestionofhowthesocialenvironmentaffectsgeneticsandtheprocessofevolution.
THEANATOMYOFCANINESOCIETIES
AllmembersofthefamilyCanidaeshowthesamebasicpatternsofsocialbehavior,justastheyshowthesamebasictypeofstructure(Scott,1950).Evenfoxes(Tembrock,1957)gothroughmuchthesamepatternsofsexualandagonisticbehaviorasdogsandwolves.Suchdifferencesasexistarechieflymattersofdegreeratherthankind.Afox'sbarkcaneasilybetoldfromthatofadog,butitisstillrecognizablyabark.
Theprincipaldifferencesbetweenthesecaninesocieties,there-loir,lienotinbasicsocialbehaviorpatterns,butindiecomplexityofsocialgroups.Forfoxes,thematedpairisthelargestsocialgroupasidefromthetemporaryassociationofamotherandheryoung
SOCIALGENETICS415
litter,andfoxbreedershavegreatdifficultyingettingmalestomatewithmorethanonefemale.Likewise,thematedpairisthetypicalgroupincoyotesandjackals,althoughtheyareoccasionallyseeninsmallpacks.Attheoppositeextremearethedogsandwolves,whosetypicalorganizationisthepackofseveraladultmalesandfemales.Inwolves,agroupcomposedofasinglematedpairistheexceptionratherthantherule.
Thecomparativebehaviorofcanineindividualssuggeststhatbehaviorisaconservativetraitinevolutionjustastheircomparativeanatomysuggeststhatgeneralbodyformisresistanttochange.Inspiteofallthehumanselectiontowhichdogshavebeensubjected,westilldonothaveanytwo-leggedbreedsofdogsordogsthatemployhumanspeech.Conservatisminbothformandbehaviorprobablyresultsfromthefactthatitisdifficulttochangeanyhighlyorganizedsystemwithoutdisruptingit.
Incontrasttotheanatomyandbehaviorofindividuals,thestructureandfunctionofcaninesocietiesisrelativelylabileandchangeable,therebeingwidedifferencesinthecompositionofgroups.Thebasicreasonforthisliesinthetransitionfromoneleveloforganizationtoanother.Therearegreaterchangesonthesocialleveloforganizationthanonthebehaviorallevelbecauseanewtypeoforganizationonthehigherlevelcanbeconstructedwithoutgreatlymodifyingthatonthelower.ThebehaviorpatternsofwolvesaredifferentfromotherCanidaeinonlyminorways,butthesemakepossiblethedevelopmentoflargersocialgroupsandallthatalargegroupcandoincontrasttoasmallone.
largersocialgroupsandallthatalargegroupcandoincontrasttoasmallone.
Thetypicaldogorwolfsocietyisnotahighlyorganizedone.Thenumberofindividualsinapackisusuallysmall,andtherelationshipsbetweenthemembersaresimple.Foodisdividedthroughadominanceorganizationbutcanbeobtainedeitherbycombinedorindividualeffort.Asmightbeexpectedinagroupofanimalswhicharelikelytobeallthesameage,thereisnostrongsystemofleadership.
Whensocializedtopeople,bothdogsandwolvestransfertohumanbeingsthesocialrelationshipswhichtheywouldnormallydevelopwiththeirownkindinsofarasthisispermittedbytheirowners.Dogsdonotacquirehumanbehaviorthroughthisassociation,butcontinuetoshowthedog-likepatternsofbehaviorcommontoalltheCanidae.
Noveltydoesariseinthedevelopmentoftherelationshipbetweendogandhuman.Peopletransfertheirsocialrelationshipstodogsandattempttoteachthemhumansocialcustomsandnewskills.The
resultisarelationshipwhichisneithertypicallyhumannortypicallycanine.Thedogisnolongeranequalmemberofapack,althoughhewilldevelopalongtheselinesifallowed.Ratherhebecomesaperpetualfolloweranddependent.Norishelikeahumanchild,whoeventuallybecomesmoreindependentandcapableofcaringforothersofhiskind.Thedogbringsbonesbacktohisyardashewouldtoapack,butthesearenotsharedbyhismaster.
Inourexperimentswehaveprincipallystudiedtheeffectofgeneticsuponthesetwosimplesocialrelationships:thatbetweenthepuppyandhislittermatesandthatbetweendogandmaster.Thesimplicityoftheserelationshipshasmadethetasksomewhateasierthanitmightotherwisehavebeenandalsohashadtheadvantageofmakingcertaingeneralprinciplesmoreobvious.
Thedevelopmentanddifferentiationofsocialrelationships.—Oneofourmostimportantdiscoverieswasthatthedevelopmentofpuppiesisdividedintodefiniteperiods,eachcharacterizedbyanimportantprocess.Theneonatalperiodisdominatedbytheprocessofinfantilenutrition.Thetransitionperiodisoneofrapidacquisitionanddevelopmentofadultbehaviorpatterns.Theperiodofsocializationisoneofdevelopmentofprimarysocialrelationships.Thejuvenileperiodisoneofgrowthandtheacquisitionofskillswhicheventuallymakethepuppypotentiallyindependentofitsparentsorcaretakers.Finally,sexualmaturitymarksthedevelopmentofsexualrelationships,andtheconsequent
maturitymarksthedevelopmentofsexualrelationships,andtheconsequentbirthofyoungmakespossiblethedevelopmentoftheparentalrelationshipwithanewgeneration.
Socialdevelopmentcorrelatedwithsocialorganization.—Caninedevelopmentissoorganizedthattheperiodofsocializationisoneinwhichthemothernormallyleavespuppiesforlongperiodswhilethelitterstaystogetherandwaitstobefed.Consequently,thestrongestsocialrelationshipsareformednotwitholderanimalsbutwithlittermates,andthisappearstobethefoundationforpackformation.YVestilldonothavecompleteinformationonthenaturalformationofnewpacksinwolves,butMurie(1944)observedayounglittermovingaboutasaunitasitgrewup,alreadyactingasapack.Healsosawasingleadultattemptingtojoinanestablishedpackandbeingrejectedbyit.Itseemslikelythatmostwolfpacksareformedbylitterswhichstaytogetherasadults.
Thusthedevelopmentofsocialbehaviorindogsisdirectlyrelatedtothetypeofsocialorganizationtypicalofadultwolvesanddogsallowedtorunwildinpacks.Whenwecomparecaninedevelopmentwiththatinotherspecies,wecansecthatwehavegoodevidenceofagenerallaw.Insheep(Scott,1960and1962a),theyoungareborn
SOCIALGENETICS417
capableofmovingaroundactively;theprocessofsocializationbeginsimmediatelvafterbirth:andlambsbegintofollowtheirmotherswithinafewdavs.Thusthestageissetfortheformationofpermanentflocksledbvolderanimalsincontrasttothecaninepackofasimilaragegroup.
Humanbeings,thoughdifferentfromeithersheepordogs,followthesamegenerallaw.Thevaremorelikedogsinthatbabiesareborninanextremelyimmaturestate,butunliketheminthatphysicaldevelopmentismuchslower.Alongwiththis,theprocessofprimarysocializationbeginsbeforethetransitiontotheadultformoflocomotion,atatimewhentheinfantsstillrequireconstantcare.(Scott,1963a).Thismeansthatbabiesformtheirprimarysocialrelationshipswitholderpersons.Humansocieties,andindeedmostprimatesocieties,arecharacterizedbvlongassociationsbetweenyoungerandoldermembersofthegroupandinthiswayaremorelikeasheepsocietythanacanineonewherethemembersofapackmayallbethesameage.However,humanbeingsaresharplvdifferentfromsheepbecauseoftheirslowdevelopment,whichmeansthatthehumaninfantishelplessandmustbecarriedwhiletheprocessofsocializationisgoingon,whereasalambisimmediatelycapableof
processofsocializationisgoingon,whereasalambisimmediatelycapableofindependentlocomotionandatoncestartstoformahabitoffollowingitsmother.Theoreticallvthiswouldmakethehumaninfantdevelopsomewhatmoreindependently,sincetraininginfollowingbeginsrelativelvmuchlaterinlife.
Ifthisgeneralizationiscorrect—thatthedevelopmentofsocialbehaviorisdirectlyrelatedtothetypeofsocialorganizationtvpicalofadults—itshouldfollowthatthedisturbanceofsocialdevelopmentwouldcausethedisturbance(oratleastthemodification)ofsocialorganization.Thepointatwhichthemaximumchangeinsocialdevelopmentcanbemosteasilyproducedisduringtheprocessofsocialization.Thisisthereforeacriticalperiodforthedeterminationofadultbehaviorandsocialorganization.
Ourevidenceonthepuppyreinforcesthegeneralconclusionthatinanyhighlysocialspeciesofanimalthereisarelativelybriefperiod,usuallyearlyindevelopment,whenprimarysocialrelationsareestablished,normallytomembersofthesamespecies.Duringthisperiod,itiseasytotransfersocialrelationshipstoanotherspeciesbyexperimentalmeans.Thislawhasgreatsignificanceinexplainingthedomesticationandtamingofwildanimals.Italsohasmanyimplicationsforthemodificationofsocialorganizationinhumanbeingsandthedisruptionoforganizationbydisturbancesindevelopment.
418GENERALIMPLICATIONS
Geneticvariationindevelopment.—Now,howdoesgeneticsmodifythesegeneraldevelopmentalprocesses?Inthefirstplace,alldogbreedsgothroughthesamesequenceofdevelopmentalstagesandprocessesatapproximatelythesametime.Thevariationsduetoselectivebreedinghaveproducednofundamentaldisturbanceofdevelopment.However,therearevariationsinthespeedofdevelopmentofvariousbehavioralcapacities,andthesecanvaryindependentlyofeachother.Foxterriers,forexample,arequicktodevelopthecapacityforhearingbutat3weeksofageareslowerthantheotherbreedsinmostrespects.Thisperhapsforeshadowsthefuturebehavioroftheseanimals,asfoxterriersarehighlyresponsivetosound.Thereisnoindicationthatsuchincompatibilityofdevelopmentproducesabnormality.Instudiesofhumandevelopmentithasbeensuggestedthatanindividualwhohasslowphysicaldevelopmentbutrapidsocialdevelopment,orviceversa,maybemaladjusted.Ourworkwithdogssuggeststhatsuchvariationsmayberelatedtoindividualdifferencesbutthattheresultiseventuallyawell-integratedindividual.
Inhumandevelopment,Bayley(BayerandBayley,1959)hasshownthatvariationsinspeedofdevelopmentmayhaveimportanteffectsonchildreninoursociety.Earlysexualmaturityusuallyhasfavorableeffectsonboysandunfavorableeffectsongirlsinregardtosocialadjustmenttotheirclassmates.Wehavenotobservedanyimportanteffectofthissortindogsraisedunderourconditionsexceptpossiblythelatematurationofthesheepdogs,whichperformedrelativelypoorlyonmanytests.Thegeneraltraditionamongdogownersisthattheseanimalsdevelopconfidencemoreslowlythansomeotherbreeds.However,thereareotherpossibleexplanationsoftheirpoorperformance,andwecanonlysaythatgeneticdifferencesinthespeedofdevelopmentdonotseemtoproduceimportanteffectsintheearlylifeofdogs,althoughtheymaydosolateron.Onereasonforthisisthefactthatthepossiblerangeofsuchdifferencesintheperiodofearlydevelopmentisquitesmallcomparedwiththatinlaterlife.
Heredityandsocialrelationships.—Wemaynowconsidertheeffectofhereditarydifferencesuponthedevelopmentofasocialrelationship.Thiskindofdevelopmentgoesalongwiththebehavioraldevelopmentdescribedabove,butinvolvesinadditionthebehaviorofasecondindividual.Also,whilebehavioraldevelopmentistoalargeextentdependentongrowth,thedevelopmentofasocialrelationshipmaytakeplaceveryrapidlyandatanytimeindevelopment.
Ourbestexampleofasocialrelationshipisthedominance-sub-
SOCIALGENETICS419
ordinationrelationshipbetweenlittermates.Westudiedthedevelopmentofthisrelationshipindetailundercontrolledconditionsandfoundthatwithinitthebreedsdevelopedimportantdifferencesinagonisticbehavior.Infact,oneofthebiggestGeneticmodifica-tionsofbasicdogbehaviorpatternshasbeentheselectionofcertainbreedsforaggressivenessandothersforpeacefulness.Asdescribedinanearlierchapter,oneofthemostobviouseffectswasthelimitationofgroupsizeinfoxterriers.Foxterrierpuppieswereunabletoworkoutanvkindoflivablerelationshipinlitterslargerthanthreeindividuals.
Thesituationposesaninterestingtheoreticalquestion.Presumablythemembersofeachbreedarenearlyequalinaggressiveabilities,butthenatureoffightingmakesitimpossibleforbothanimalstowinandcontinuetobeequallyaggressive.Oneresultofthissituationmightbeafighttothedeathinthehighly
aggressive.Oneresultofthissituationmightbeafighttothedeathinthehighlyaggressivebreeds,andthisisexactlywhathappensiffoxterriersarelefttothemselves.Anotherpossibilityisthatthemoreaggressivebreedswouldworkoutsystemsofcompletedominancewhilethemorepeacefulbreedswouldshowlittleornodominanceamongthemselves.
Thebreedsdidindeedshowthiskindofdifference.Foxterriersandbasenjisshowmanymoreinstancesofcompletedominancethandobeaglesandcockerspaniels,whilesheltiesareintermediate.Examiningthesituationindetail,wefindineverybreedmorecompletelydominantmalesthanfemales,butthedifferencesbetweenthesexesinthisrespectarefargreaterinthetwomostaggressivebreeds.Thatis,inaggressivebreedsthegreatmajorityofrelationshipswithcompletedominancearecaseswheremalesaredominantoverfemales.
Hereweseetheresultofahereditarydifferencewithinbreeds—thatbetweenmalesandfemales.Whenwecomparedominancebetweenmalesinonebreedwiththatinanother,thedifferencesintheamountexpressedarenotgreat.Thebigdifferenceoccursinthemale-femalerelationships:thesearemorehighlydifferentiatedinthemoreaggressivebreedthaninthemorepeacefulone.Inadominance-subordinationrelationshiptheexpressionofageneticdifferenceinaggressivebehaviordependsuponthetwoindividualsalsobeingdifferentfromeachotherwithrespecttosex.Thiswouldnotnecessarilybetrueineverysocialrelationship,butitdoesillustratethecomplexityoftheproblemofhowadifferencebetweengenesisfinallyexpressedinasocialrelationshipbetweentwounlikeanimals.
"Personality"measuredbysocialrelationships.—Humanbeingsareoftenconcernedwiththeeffectorimpressionthatoneperson
producesonanotherandspeakofhis"personality."Oneofthedescriptivetermsappliedtohumanpersonalityisthatofdominance.Whatshallwesayaboutthe"personality"ofthedogsinthisexperiment?Obviouslywecannotsaythatallfoxterriersaredominantandallbeaglessubordinate.Thismightbetrueiftheydevelopedsocialrelationshipsbetweenthetwobreeds,butwithinitsowngroupthesamefoxterriermaybedominantinonerelationshipandsubordinateinanother,andthesamethingmaybetrueofabeagle.Neithercanwesaythatonebreedisaggressiveandtheothersubmissive.Againthisdependsuponthesocialrelationshipsconcerned.Allthatwecansayisthatafoxterrierhasagreatercapacitythansomeotherbreedstodevelopaggressivenessinarelationshipwherethecapacitiesofthetwoindividualsareunequal.Thatis,thedevelopment
wherethecapacitiesofthetwoindividualsareunequal.Thatis,thedevelopmentofthecapacitydependsnotonlyuponthepossessionoflatentabilitybutonthebehavioraldevelopmentoftheotherindividualconcerned.
Thisisanewconceptofpersonalityor,moreproperlyspeaking,amoreaccuratewaytomeasureit.Whatwearebasicallyinterestedinisthecharacteristicsocialbehaviorofanindividual.Sinceitvariesfromrelationshiptorelationship,wecanonlydescribeitintermsofthemostimportantrelationshipsinanindividual'slife.ForadogintheJacksonLaboratorySchoolforDogs,themostimportantrelationshipswerethosewithhislittermates,withthehumancaretakersandexperimenters,andwithoccasionalhumanstrangers.Thesamefoxterriermightbedominantwithallhislittermates,subordinatetothecaretakers,andfearfulwithstrangers.
Amonghumanbeingswecaneasilyobservethesamekindofcontradiction.Itisarareindividualwhoappearsthesametohiswifeastohisbusinessacquaintances.Thesmallboywhoattemptstotreathisplaygroundacquaintancesinthesamewaythathemanageslifewithhisparentsisquicklydisillusioned.Wehaveallseencasesofindividualswhoproduceawonderfulimpressionuponstrangersbutwhocannotgetalongwiththeireverydayacquaintances.Allthissuggeststhattheonlyrealisticwaytogetapracticalandmeasurablepictureofpersonalityisintermsoftheimportantsocialrelationshipsofeachindividual.Mostcurrent"personalitytests"arebasedoninformationregardingamixtureofmanyrelationshipsandoftendependupontheindividual'sviewofhimselfratherthanhisefleetonothers.Eventheclinicianseesanindividualonlyinonerelationship,thatofdoctorandpatient.Somerelationshipsarehighlyspecificandothersbroadandgeneral.Sometimestheymayresembleeachotherhut,asourexperimentalevidenceshows,somecanbehighlyindependentniothers.Attheveryleastwemustkeepinmindthe
SOCIALGENETICS
421
w
(I)
Fig.17.1.—Functionaldifferentiationofformduringgrowth.Hereditary(H)andenvironmental(E)factorsbothactonphysiologicalprocesseswithintheorganism(O),andtheseprocessesbytheirownfunctionmodifyfurther
organism(O),andtheseprocessesbytheirownfunctionmodifyfurtherprocesses.
distinctionbetweenthecapacitytodeveloparelationship,whichmaydependlargelyonheredity,andtheactualrelationship,whichdependsontheheredityoftheotherindividualaswell.
Thepredictionofsocialdevelopment.—Figures17.1to17.3graphicallyrepresenttheeffectofheredityuponthedevelopmentofasocialrelationship.Thediagramsaresomewhatartificialinthattheyareinevitablymoresimplethanreality,andbecauseitisdifficulttoexpressthefactthatseveralprocessesaregoingonsimultaneously.Thearrowsareintendedtoindicateactionofoneprocess
Fig.17.2.—Thefunctionaldifferentiationofbehaviorinrelationtothephysicalenvironment.Theorganismpreviouslydifferentiatedbygrowthprocessesat(1)isnowcapableofbehavior(B),whichmaychangethenatureoftheenvironment,aswellasthenatureoftheorganism(O)throughtheprocessoflearning.Heredity,ontheotherhand,remainsunchangedbutactsonacontinuallychangingorganism.Justasinthepreviousdiagram,theactivityoftheorganismmodifiesitself,butthistimethearrowsleadthroughbehaviorandthephysicalenvironmentbeforefeedbacktakesplace.
onanother,andthearrowsallpointinonegeneraldirection,indicatingthepassageoftime.
Thediagramsreflecttwofundamentaleffects.Oneisthatanorganismundergoescontinualchangeanddevelopment,sothatneitherbehaviornorphysiologyandstructurearethesameatonepointintimeasatanearlierone.Thesecondeffectisthatanorganismchangesitselfbyitsownactivity.Thisisthefundamentalconceptoffunctionaldifferentiation.Earlyinlifethesechangesoccurmostlythroughtheprocessofgrowth.Bydifferentialgrowthandother
occurmostlythroughtheprocessofgrowth.Bydifferentialgrowthandother
4fj$\s
\
/
(2)
N.
B.B:
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Fig.17.3.—Thefunctionaldifferentiationofasocialrelationship.Bothorganisms(01?02)stimulateeachotherat(2),resultinginanextremelycomplexdiagramoffeedbackandinteraction.Thebehaviorofanindividualinasocialrelationship(BxandB2atthebottomofthediagram)dependsupontheheredityandpastenvironmentoftheotherindividualaswellashisown.Further,hisownheredityandenvironmentaffecthimthroughtheotherorganismaswellasdirectly.Theeffectofadevelopingsocialrelationshipisthusamutualmodificationofbehaviorandthecreationofsomethingnew.
physiologicalprocesses,anembryochangesandmodifiesitsowncapacitytodevelopfurther(Fig.17.1).Laterindevelopmenttheorganismbeginstochangethroughtheprocessoflearningaswellasgrowth.ThetwoprocessesarecombinedinFigure17.2asifoneprecededtheother,butthevactuallyoverlap.Inthisdiagramwehaveindicatedthatheredityandtheenvironmentcontinuallyactuponanorganism,whichisalsoatanygiventimetheresultoftheirpastaction.Thereisanewcomplicationinthatbehaviormaychangethephysicalenvironment,aswellaschangingthenatureoftheorganismthroughtheprocessoflearning.Thischangeinenviron-
SOCIALGENETICS423
mentisreflectedinfuturebehavior.Justasinthepreviousdiagram,theactivityoftheorganismmodifiesitselfandhenceitsfutureactivity,butthistimethearrowsleadthroughbehaviorandthephysicalenvironment.
Figure17.3showstheresultofsubstitutinganotherindividualorganismforthe
Figure17.3showstheresultofsubstitutinganotherindividualorganismforthephysicalenvironment.Theresultisanenormouslycomplicateddiagram.Thebehaviorofanindividualinasocialrelationshipdependsnotonlyuponhisownheredityandpastenvironment(experience),butalsoonthoseoftheotherindividual.Furthermore,thearrowsfromhisownheredityandpastenvironmenteventuallyleadthroughhisbehaviortotheotherindividualandproducearesponse,whichinturnmodifieshisownbehavior.Theresultisthemutualmodificationofbehaviorandthecreationofsomethingwhichisimpossibleforeitherindividualtoachievebyhimself:asocialrelationship.
Doesthismakeitimpossibleeithertheoreticallyorpracticallytoanalyzetheeffectofheredity?Thediagramsindicatethatheredityisnot,asfarasweknow,modifiedbytheactivityoftheorganism.Theheredityofanindividualremainsaconstant,butthefactthatitactswithinacontinuouslychangingorganismmakesfordifficulties.
Aswefoundinthecaseofthedevelopmentofthedominancerelationshipinpuppies,wecanpredicttheactionofheredity,providedwehavereasonablypurebreedingstrainsdevelopingwithinauniformenvironment.Wecanpredictthatfoxterriersrearedinlargelitterswiththeirmotherswilldevelopseriousfightingabouttheageof7weeksandwilleventuallyworkoutdominanceordersinwhichthemalesarecompletelydominantoverthefemales.Wecanalsopredictsomeoftheotherpossibilitiesbasedonexperimentalevidence.
However,wherewedonothavepurebreedingstocksandwhereheredityisunknownexceptthroughitsexpressioninanindividual,thereisafarmoredifficultproblem,andthisistheonewhichwefaceinahumansociety.Inordertopredictthebehaviorofahumanindividualweneedtoknowhisbasiccapacitiesforthedevelopmentofsocialbehavior,irrespectiveofhowtheyhavebeenmodifiedbyenvironmentanduse.Forexample,weneedtestsofaggressivenesswhichwillmeasureaperson'scapacitytodevelopaggressivebehaviorwithoutreferencetotheamountthathehasactuallydeveloped.Sincesuchcapacitiesarebasicallyphysiological,ourhopeofsuccessliesinthedevelopmentofphysiologicaltests.Ifwecouldmeasurethedegreeofemotionalarousalinthecentralnervoussys-
ten3uldhaveameasurementofonetraitinvolvedinthe
.icitytodevelo::_.ss.Ourstudieswithdogshavenot
proceededfarinthisdirection,butwedohaveonesuchphysiological
proceededfarinthisdirection,butwedohaveonesuchphysiologicalmeasurementconnectedwiththearousalofemotion,name.
artratereaction,inwhichtheterrierswerequitedifferentfromallthe:
otherpracedisfortestsofdifferentsortswhichcan
gibdsoonenoughindevelopmentsothatenvironmentalopportunitiescould,ifneedful,beadjustedtobasiccapacities.Inthisdiesofthedogareonlymoderatelyencourag:gDifferencesinaggressivebehaviorarenotreadilvrecognizableuntilabc~_therdifferencesinbehavioroccurearlier,
buttheyarenotdirectlycorrelatedwithadulttraits.Infact,itlooksas::theearliestnofsocialbehaviorisquitevariable,indi-
catingforbehavioraldevelopmentareatE
quiteflexible.
_:basicinformationonearlydevelopment,wewouldeonlvalistofcapacities.Actualbehaviorwoulddependonwhetherornotthesecapacitieswereinfactdeveloped.Consequentlyif;uratepredictionofthebehaviorofanadultindividual,wemustworkintermsofthepotentialdevelopmentofcapacit:inimportantearlvsocialrelationships.Fortunately,thenumberofsuchrelationshipsislimited,orthetaskof:riptionwouldbeimpossiblvdifficult,complicatedasitisbythephenomenonofculturalchan^
illchancreisdeterminedbvthebiologicalmechanismfortransmittingbiologicalheredityfromonegenerationtoanother,soculturalchangedependsonthebasicmechanismfortransmittincrlearnedinformationfromonegenerationtothenext.:sthemechanismoflearninghasthesamefundamentalrelationshiptotheoriesofculturalchangethatthemechanismofMende-lianhereditvbearstothetheorvoforganicevolution.Aswehaveseeninpastchapters,thetwobasicmechanismsarenotentirelyindependentofeachother,andtheproblemofhowheredityaffectsthecapacity-tolearnconsequentlyhasgreattheoreticalimporta:
edityandthecapacitytolearn.—.Althoughtheseexperiments:lidedbythegeneralconceptofsocialbehavior,theproblemofindividualdifferencesinlearningandproblemsolvingseemedsoimportanttousthatwedevotedalargenumberofourteststoanattempttomeasurethedifferentiallearningcapacitiesofdogbreedsandindividuals.
ofdogbreedsandindividuals.
beganwiththeideathatthestudyofdevelopmentwouldbe
SOCIALGENETICS425
importantbecausethiswouldenableustoobservethebehaviorofyounganimalsbeforetheyhadbeenmoldedbytheenvironmentandwhiletheyweremorecompletelycontrolledbyheredity.Wethereforeexpectedtoseetheeffectsofgeneticspureandundefiledintheyoungpuppy.Thisideaturnedouttobesomewhatnaive,forwefoundthatmanyofthecharacteristicbreeddifferencesinbehaviordidnotappearinearlylife,andthiseventuallyledustotheconceptsofthedevelopmentanddifferentiationofbehavior,affectedbyboththeprocessesofheredityandthoseoflearning(Scott,1957).
Insteadofshowingstereotvpedbehavior,ayoungpuppyconfrontedbyanewsituationusuallytriesoutonepatternofbehaviorafteranother.Ifoneoftheseseemstowork,heislikelytorepeatitonsubsequentoccasions,withtheresultthathisbehavioreventuallybecomeslessvariableandmoreconsistent.Thustherearetwoopposingprocessesinanybehavioraladaptationwhichinvolveslearning.Oneoftheseisvariation,whichpermitsimprovementofperformance,andtheotherishabitformation,whichfixesperformance.Hereditymayalterthebalancebetweenthesetwoprocessesineitherdirection.Forexample,Shetlandsheepdogsformfixedhabitsveryreadily,particularlythoseinvolvinginhibitorytraining,whereasbeaglesformsuchhabitslessreadilythantheaveragedog.Althoughhereditythusdeterminesdifferencesbetweenthebreeds,thefinallimitsonbehavioraresetbytheprocessofhabitformation.
Effectoflearningonhereditarydifferences.—Oncehereachestheageof5or6weeks,apuppyhasawidechoiceofbehaviorpatternswhichcanbeusedinanygivensituation.Aswehavepointedoutinearlierchapters,therewereseveralkindsoflearningsituationsincludedinthosewegavethedogs.Oneofthesewasaproblemwithonlyonecorrectanswer,asolutionwhichweimposeduponthedog.Thisisthemethodof"forcedtraining,"well-knowntoprofessionaldogtrainers.Inasituationlikethis,hereditycanmodifythespeedwithwhichthedogacceptsthetraining,asintheleash-controltest,andalsothedegreeofperfectionwithwhichheperformsthespecifiedmovements,butithasrelativelylittleeffectontheendresult.Whenforcedtrainingisimposedontwobreedsofdogs,thefinaloutcomeisthattheybecomemorealikethantheywereinthebeginning.
Inanothertypeoftrainingthepuppyissubjectedtolessrigidcontrol.Whenweweretrainingpuppiestobeweighed,wedidlittlemorethanholdourhandsnearthepuppytokeephimfromfallingoffthescales.Fromthepuppy'spointofview,thegoalofhisbehaviorwastogetoffthescalesandbackonthefloor,andthiswas
achievedattheendofoneminute,nomatterhowheacted.Inthissituationthecockerspanielsusuallydevelopedthebehaviorpatternofsittingquietly,whileterriersandbasenjisdevelopedthatofconstantstruggling.Geneticdifferencesinfluencedthechoiceofthebehaviorpattern,andtheendresultwasthatthethreebreedsgotfurtherapartastheygrewolder.However,geneticsdidnotcontroltheanimal'sbehaviorsoexactlythateverycockerspanielalwayssatquietlyandeveryterrieralwaysstruggled.Whatitdiddowasinfluencetheprobabilitythatthesereactionswouldappear,ratherthancontroltheminanyironcladway.
Mostofourperformancetestsinvolvedfindingagoalwherefoodwasavailable.Therewasacorrectsolution,butthepuppyhadtofindithimselfinsteadofhavingitforceduponhim.Such"problem-solving"testsarenaturalonesforhuntinganimalswhomustfindtheirfoodunderavarietyofsituations.Althoughwetriedtodesignthetestssothatonlyonesolutionwaspossible,weusuallyfoundthatthepuppiesattemptedagreatvarietyofsolutionsandoftenperfectedoneswhichwedidnotconsiderthemosthighlyadaptive.Asthetheoryoftheadaptivefunctionofbehavioralvariabilitywouldpredict,thevshowedmuchmorevariationofbehaviorintheearlypartsofthetestthanlateron.However,insomeofthesetests(suchasthespatial-orientationproblem,inwhichthedogsweregivenaseriesofincreasinglydifficultproblemsonthesameapparatus),thedifferencesbetweenthebreedsremainedproportionallythesamefromfirsttolast.Behaviorbecameagreatdealmoreconsistentundertheprocessoflearning,buttherelativeamountofvariationproducedbyheredityremainedthesame.
Thustheeffectoflearningcanbetoeitherreducehereditarydifferences,magnifythem,orkeepthemthesame,dependinguponthekindoftrainingorproblem-solvingsituationinvolved.
Complexityofinteractionbetweenheredityandthelearningprocess.—Learningisonlvonemechanismbvwhichtheeffectsofheredityareexpressedinhighlycomplexways.Asourexperiencewiththeheredityofseasonalbreedingshows,itispossibletogetahighlycomplexexpressionofhereditvinthephysiologicalfactorswhichunderliebehavior,aswellasintheinteractionofhereditywith
factorswhichunderliebehavior,aswellasintheinteractionofhereditywithlearning
Furthermore,wefoundthathereditaryeffectsuponbehaviorwerehighlyspecificandthatwegotclear-cutindicationsofheredi-tarvdifferencesonlvwhenweworkedwithvervsimplebehaviorpatterns.Inmostproblem-solvingsituations,behaviorishighlvcomplexandmanybehaviorpatternsareused,combined,andrecom-
SOCIALGENETICS427
binedwitheachother.Theresultisthatwhilecomplexperformanceandintelligencetestsshowindicationsoftheeffectofheredityinbothpurebreedsandhybrids,neitherthekindsofsolutionsnorthedegreesofsuccessareinheritedinanysimpleMendelianfashion.
Atthispointwemightemphasizethefactthatourworkconflictswithseveralpopularnotionsoftheeffectofheredityonbehavior.Oneisthatthereareafewbasichereditarytraitswhichappearinallthebehayiorofanindividualandmakehisbehayiorpredictableandunderstandable.Perhapsthisiswhatisordinarilymeantbytheterms"character"and"personality."Althoughitmaybepossibleforhumanbeingstodeyelopsuchconsistentbehayiortraitsthroughlearning,thereisnoindicationinourresultsthatheredityactsinanysuchsimplefashion.
Anothermistakennotionisthatthereissuchathingas"generalintelligence."Asweshowedinanearlierchapter,adogbreedmayrateveryhighinonetestsituationandquitelowinanother,withlittleuniformity.Ourgeneralimpressionisthatanindiyidualfromanydogbreedwillperformwellinasituationinwhichhecanbehighlymotiyatedandforwhichhehasthenecessaryphysicalcapacities.Hereditymaylimitbothmotiyationandcapacity,butinhighlyspecificways.Ifwecomparetheseresultswiththehumansituation,welikewisefindnogeneralconfirmationoftheexistenceofafactorofgeneralintelligence(Anastasi,1958).Humanbeings,howeyer,havestillanothercapacity(orcapacities)whichisprobablyaffectedbyheredity,andthatistheabilitytolearnanduselanguage.Thismaychangethesituationfromthatwhichwefoundindogs,forinhumanbeingsthelackofonlyonespecificgroupofcapacities;i.e.,theabilitytouselanguage,wouldbeageneralhandicaptoalmostallaspectsoflearning.
Stillathirdpopularnotionisthatindiyidualsfallintobehavioral"types"andthatthesearesomehow7relatedtophysiqueorspecialphysicalcharacteristics.Our
thesearesomehow7relatedtophysiqueorspecialphysicalcharacteristics.Ourresultsindicatethatevenindogswearedealingwithpopulationsinvolvingcontinuousvariationandthat"types"haverelativelylittleimportance.
Wemustconcludethatanyattempttoimprovethecapacitiesforlearningandproblemsolvingbygeneticmethodsislikelytobemostsuccessfulwhendoneinahighlyspecificway,asithasbeendoneforthedogbreeds.Evenintheseanimals,thebreeddifferencesusuallyarenotgreat,providedallbreedsaregivenanequalamountoftrainingandopportunitytolearn.Thereisstillanenormousamountofgeneraladaptivecapacityinthespecializeddogbreeds,andapurebreddogcanlearnmanythingsbeyonditsownspecialty.
Thechiefdifferencesbetweenthebreedsseemtolieintheamountoflimitationproducedbythesespecialcapacities.Certainbreedsarequitelimitedwithregardtothesituationsintowhichtheycanadaptwell,andothersaremuchmoregeneralized.Forexample,withonlyaminimumamountoftraining,thebeagledoesquitewellasarabbithunterandalmostequallywellasahousepet.Mostoftheshepherddogscanbecomeindependenthuntersofbiggame(aswhencolliesrundeer),buttheyrequireagreatdealofspecialtraininginordertobecomeeithersuccessfulshepherddogsorhousepets.
Therehasneverbeenanydeliberateselectionofhumanbeingscorrespondingtothatindogs,althoughmodernhumansocialorganizationcanconceivablyhavethiseffectindirectlybyselectingcapableindividualsofbothsexesforcollegetrainingandthenbringingtheselectedindividualstogetheratthematingage.However,thecapacitiesusefulinhighereducationaresobroadandcomplexcomparedtotherelativelysimplecapacitieswhichcanbeeasilymodifiedbyageneticselection,thatitisunlikelythatevensuchassortivematingwilleverproduceahighlyspecializedanduniformpopulationhereditarilydifferentfromtherest.Mostindividualsarelikelytohavecertainspecialcapacitieshighlydevelopedandothersrelativelypoorlydeveloped.Becauseofthewidespectrumofadaptabilitypresentinmostindividuals,heredityshouldnotbethemostimportantlimitingfactorindeterminingtheirlivesandbehavior.Infact,aswehaveseenabove,themostimportantlimitingfactoronbehavior,andparticularlythatlimitingthedifferentiationofbehaviorbetweenindividuals,islearningandhabitformation,andourchiefpracticalproblemistodesignasocialenvironmentwhichwillprovideanopportunitytoexpressinusefulandpleasurablewaystheenormousamountofvariationinbehaviorofwhichhumanbeingsarecapable.
Howdoesheredityaffectthecapacitytolearn?—Oneoftheobviouswaysin
Howdoesheredityaffectthecapacitytolearn?—Oneoftheobviouswaysinwhichheredityaffectsthecapacitytolearnisbylimitingphysicalcapacities.Adachshund,forexample,willneverbeabletolearntocatcharabbitbychasingit.Suchlimitations,inturn,haveanimportanteffectonlearnedmotivation,whichissolargelydependentuponsuccess.Inaddition,thedogbreedsshowmoredirecthereditarydifferencesinmotivation,huntingdogsinourstrainsshowingmoreinterestinFoodthanrepresentativesoftheworkingbreeds.Differencesinemotionalresponsivenessareimportantandmaymakethelearningofcertaintaskseasierorharder.
SOCIALGENETICS429
Oneofthemostinterestingmodificationsoflearningisthatofhereditaryshiftingofthebalancebetweenvariabilityofbehaviorandfixationbvhabitformation.Thesedifferences,however,appeartobemodificationsoftheperipheralprocessesoflearning(i.e.,motivationtolearn)ratherthanofthecentralphenomenonofassociation.Alldogscanmakeassociations,anditispossiblethatthiskindofabilitvissofundamentalthattheanimalcannotexistwithoutit,thatlearningisasbasicallyimportanttoexistenceasismetabolism,andaslittlesubjecttochange.
CULTURALEVOLUTIONANDBIOLOGICALCHANGE
Thisbringsustoathirdbasicproblemofsocialgenetics:howdoessocialorganizationaffecttheprocessofbiologicalinheritanceandthusaffectbiologicalevolutionarychange?Theexistenceofsocialrelationshipsinananimalsocietyusuallyproducesamatingsystemofsomesort,sothatgenesarenotpassedfromonegenerationtothenextinarandomfashion,andthisfactinturnmayeitherspeeduporslowdownevolutionarychange.
Stabilizingeffectofsocialorganization.—Fromatheoreticalpointofview,thegeneraleffectofastablesocialorganizationonananimalpopulationshouldbetoslowdowngeneticchanges.Wehaveseenthattherearetwobasickindsofprocessesoffunctionaldifferentiationgoingon:physicalandanatomicaldifferentiationbasedontheprocessofgrowth,andbehavioraldifferentiationbasedontheprocessoflearningaswellasongrowth.Forachangeinhereditytosurvive,itmustproduceafavorableeffectonatleastoneoftheaboveprocesseswithoutproducinganoverridingunfavorableeffectontheother.Theadditionofstillanotherprocess,thedifferentiationofbehaviorinasocialrelationship,producesathirdformoforganizationinwhichthehereditarychangemustproduceafavorableoratleastneutraleffect.This,ofcourse,still
changemustproduceafavorableoratleastneutraleffect.This,ofcourse,stillfurtherreducesthelimitswithinwhichpermanenthereditarychangecantakeplace.Thesedevelopmentalprocessesareallpartiallydependentupononeanother,andsowefindthatthesocialbehaviorpatternsandthesocialdevelopmentofaspeciesaredirectlyrelatedtothenormalsocialorganizationofthespecies,andthatadisruptionofdevelopmentproducesadisruptioninsocialorganization.
Inaddition,anypopulationinaconstantenvironmenttendstoapproachastateofgeneticequilibrium,andthemoreconstantthesocialenvironment,themorestablethegeneticsystem.Evenifthe
stateofequilibriumistemporarilydisturbed,asbythechangeinenvironmentproducedbycivilizedliving,anewstateofgeneticbalanceiseventuallyreached.
Culturalevolutionandbiologicalevolutioncompared.—Inhumanpopulationstheseprocessesoperatingtoproducegeneticstabilityareopposedbyotherforcesmakingforsocialchange.Agreatmanyanimalsocietiesshowthebeginningsofculturalinheritance.Sometimesanimalsinheritstructuresbuiltbytheirancestors,asinthecaseofprairiedogburrows.Ortheymaylearnbehaviorfromolderanimals,asyoungdeerlearntobefearfulofhumanbeingsfromtheirelders.Totheseabilities,humanbeingshaveaddedthecapacityforspeech,whichenormouslymagnifiesthepossibilityoftransmittinglearningfromonegenerationtothenext.Furthermore,whatislearnedthroughspeechbecomesalmostcompletelyindependentofbiologicalheredity,withtheresultthatculturalchangeordinarilyproceedsmuchfasterthanbiologicalchange.
Anyonewhocomparesbiologicalandculturalevolutionbecomesfascinatedwiththeresemblancesbetweenthetwo.Languagesseemtoevolveinmuchthesamewayasspecies,andonecandrawaphylogenetictreeoflanguageswhichisnodifferentinformfromthephylogenetictreeofthespeciesoftheanimalkingdom.Yetthetwokindsofchangerestonentirelydifferentprocesses,onebeingMendelianinheritanceandtheothertheprocessoflearning.
InMendelianheredityaparentpassesalongtoeachchildonlvoneofeachpairofgenes,selectedpurelvbychance.Withtheusualnon-inbredhumanparent,theresultisanarrangementofgeneticfactorsinnewcombinationsinthenextgenerationwiththevirtualcertaintythatnoneofhischildrenwillhaveexactlythesamecombinationashisown.Similarly,thebasiccharacteristicofthe
thesamecombinationashisown.Similarly,thebasiccharacteristicoftheprocessoflearningisthateachchildmuststartalloveragainfromthebeginning.Itisimpossibleforhimtoacquireexactlywhathisparentshavelearned,becausepartofhisenvironment,asdistinctfromtheirs,iswhatthevattempttoteachhim.Theprocessoflearningisbothselectiveandorganizational;consequentlytheinformationlearnedbythepreviousgenerationisneverpassedalongcompletelvandneverorganizedinexactlythesameway.Biologicalandculturalheredityaresimilarinthattheyarebothfundamentallyunstablesystemswhichmakechangeinevitable.
Thereisonebigdifferencebetweenthetwosystems.Culturalheredityiscumulativeandhasbecomemuchmoresowiththeinventionofwrittensymbolsandrecords.Biologicalheredity,ontheotherhand,isnon-cumulative.Eachindividualhasonlvthesame
numberofchromosomesandgenesashisimmediateancestors.Thisisanotherwayofstatingthatlearnedbehaviorcanbeinheritedculturallybutnotbiologically.
Theresultisthathumansocietiesinevitablychange,andchangewithgreatrapidity—sofastthatbiologicalchangeisinevitablyleftfarbehind.Wehaveeveryindicationthatthehumanraceisphysicallyquitesimilartowhatitwastenthousandyearsago,yetthisisthetimeduringwhichwehaveprogressedfromprimitivehuntingtribestomodernindustrialcivilization.Ifanything,theprocessofculturalchangeseemstobespeedingupratherthanslowingdown.
Heredity,learning,andculturalevolution.—Evolutiontowardwidercapacitiesforadaptationisageneraltendencyintheanimalkingdom,althoughtherearemanyexceptionsinthecaseofspecieswhichhavebecomespecificallyandnarrowlyadaptedtoaparticularenvironment.Specializedspeciesarelikelytobecomeextinctwhentheenvironmentchanges,withthelongtermresultthatthosewhichsurviveusuallyhaveawiderangeofbehavioralandphysiologicaladaptability.
Thisgeneraltendencyinvolvesade-emphasisofbehaviororganizedonapurelyhereditarybasis,forsuchbehaviorcanonlybeadaptiveinacompletelystableenvironment.Alongwiththiswefindanincreasingemphasisonvariablebehaviororganizedbylearning.Moreover,theprocessesofculturalchangeandculturalevolutionautomaticallyproduceanunstableandchangingenvironment.Inhumansocietiessuchchangeshavealwaystakenplacebetweenonegenerationandthenext,andinthecurrentspeed-upofculturalchangetheyare
generationandthenext,andinthecurrentspeed-upofculturalchangetheyarebeginningtotakeplaceevenwithinasinglelifetime.Consequentlythereareandwillbeincreasingdemandsforpersonswhoareflexibleandadaptiveor,inshort,whohaveincreasedlearningcapacities.
Thekindsofeffectsofheredityuponlearningcapacitieswhichwehavedescribedindogschieflycontributetobreedandindividualdifferenceswithinthespecies,increasingtherangeofadaptabilityofthespeciesratherthanthatoftheindividual,whoseownbehaviormay,infact,belimitedbythem.
Therearenobreedsinthehumanspecies,butthereisanenormousamountofindividualgeneticvariability.Wehaveeveryindicationthatourspeciesasawholealreadyhasawiderangeofadaptability,inhabitingasitdoeseveryclimateontheglobeandtakingpartininnumerableproductiveanddestructiveoccupations.Individualhereditaryvariationhastheeffectofmakingthisrange
ofadaptabilityforthespeciesevenwider,andthisinturnhastheeffectoffacilitatingculturalchange.Thuswecanconcludethatthereisasynergisticrelationshipbetweenhereditaryvariationinbehavioralcapacitiesandthespeedofculturalevolution.Hereditaryvariationwidenstherangeofadaptability",permittingculturalchange;andculturalchange,inturn,permitssurvivaloflargerpopulations,withtheconsequentincreasedpossibilityofhereditarvvariation.
Now,whateffectdotheserapidchangesinhumansocialenvironmenthaveuponthedog?Dogsreflectthecultureinwhichtheylive.IntheMiddleEastthereareessentiallvonlvthreekindsofdogs:salukisusedforgazellehuntinginthedeserts,largeherdingdogsusedbvKurdishshepherdstoprotecttheirflocksfromwolves,andmongrelswhichchief!vactasscavengersinthecities.Bvcontrast,
OrJO
inmodernFrance,wheredogsarechieflvusedonfarms,therearesomeseventeenbreedsofshepherdandstockdogs.InEngland,wherehuntinghasbeenapopularsportinallclassesfromasfarbackastheMiddleAges,therewerein1959twenty-sixrecognizedbreedsofsportingdogs.
Wecanthinkofhumansocialchangeasprovidingtheopportunityforthephenomenonofcanineadaptiveradiation.Eachsocialchangeopensupawholenewenvironmentfordogs,andtheexpansionoftheirnumbersfromsmall
newenvironmentfordogs,andtheexpansionoftheirnumbersfromsmalloriginalgroupsprovidesanopportunityforrapidbiologicalchange.InmodernEuropeandtheUnitedStatesincreasedwealthandurbanlivinghasopenedupawholenewenvironmentfordogsassocialcompanions,andwemayexpecttoseethebreedschangedandmodifiedinthatdirection.Thusweseethegreatpopularityofthebeagleasachildren'spet,beaglesbeingextremelvnan-aggressivedogswhichadaptwelltofamilylifewithaminimumoftraining.AnotherbreedwhichisbecominghighlypopularistheChihuahua,whosesmallsizeandsturdyphysicalconstitutionmakeitanidealanimalforapartmentdwellers.Itwillbarkasvigorouslvasanywatchdog,butistoosmalltobitethepostman.
Moderndogsalsofillmoreserioussocialfunctions.Companiondogsprovideasolutionformanyofthepsychologicalstrainsimposedbyculturalchange.Theelderlycouplewhosechildrenhavemovedawaycanadoptapuppyasachildsubstitute,andthelonelybachelororspinstermaykeepadogasadependablecompanion.Wemayexpectthatinthefuturetherewillbedeliberateaswellasunconsciousattemptstodevelopbreedswhichwillsatisfythesesocialneeds.
SOCIALGENETICS433
Inthelongrun,theeffectofselectingdogsforfirstoneculturalenvironmentandthenanotherwillbetoproducerandomselection,eventuallyleadingtopermanentgeneticchange.Althoughwolflikecharacteristicsarestillpreservedinvariousdogbreeds,itwouldbeextremelydifficultatthispointtore-createanythinglikeawolffromasinglebreedlikethebeagle.Ingeneral,wecanpredictthataslongasbreedsaremaintainedasseparatepopulationstherewillbeacontinuousprocessofchangeindirectionsdeterminedbytheasyetunpredictablecourseofhumanculturalchange.Biologicalevolutionofthedogwillcometoastandstillonlyifbreedsandlocalvarietiesarenolongermaintainedseparatelyandallanimalsallowedtomateatrandom.
Thislastisessentiallywhatisnowhappeningtothehumanpopulationasaresultofculturalchange.Thekindofculturalchangepresentlycharacteristicofhumanpopulationsseemstohavehadtheneteffectofslowingdownhumanbiologicalchangewhilespeedingupthatofthedog.Itistruethathumanbeings,likedogs,continuallyhavenewculturalenvironmentsopeneduptotheminwhichonekindofindividualmaybemoresuccessfulthananother,buthumangenerationsaresolongandculturalchangeshavebecomesorapidthatthereisnotimefordifferentialselectiontohaveanyconsiderablebiologicaleffect.Eventhissmallpossibilityisnullifiedbytheenormousnumbersinhuman
thissmallpossibilityisnullifiedbytheenormousnumbersinhumanpopulations.
Toconclude,theeffectofculturalchangeuponhumansocietieshasbeentoreducedifferentiationbetweensmallhumansubpopu-lationsandtoincreasethedifferentiationbetweenindividualswithinapopulation.Indeed,thereisasynergisticrelationshipbetweenculturalevolutionandindividualbiologicalvariability.Theprincipaleffectofculturalchangehasbeentowidenthelimitswithinwhichvariouskindsofhumanbeingscanexistandcreateawidervarietyofsocialenvironmentswithintheselimits.Oneofoureffortstowardconscioussocialchangeshouldbeinthedirectionofrecognizingthisvarietyandprovidingsocialflexibilitywhichwouldpermittheusefulandhappydevelopmentofinevitablydifferentindividuals.Oneofourbasicproblemsinthistaskwillbetorecognizeindividualcapacitiesandassistpeopletofindfittingandcongenialsocialenvironments.Suchassessmentsarecrudelydoneatpresentandperhapscanneverbedoneperfectly.Infact,aperfectjobistheoreticallyunnecessary,sinceoneofthebasiccapacitiessharedbythemajorityofhumanbeingsisthatofadjustmentandadaptationtomanydifferentsortsofenvironments.
434GENERALIMPLICATIONS
Anotherfundamentalcontributionofascienceofhumannaturewillbethediscoveryofthelimitsofgeneraladaptation.Thiswillenableustorecognizeandavoidharmfulanddisappointingsocialchangeinadvance:tochooseinsteadmorebeneficialsocialchangesandtobringthemaboutinpeacefulandproductiveways.
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Baege,B.,435
Bahrs,A.M.,435
Baker,J.A.,15,435
Baker,P.T.,82,354,435
Banks,E.,97,226,439
Bayer,L.M.,418,435
Bayley,N.,418,435
Beach,F.A.,5,69,436,439,444
Beadle,G.W.,333,436
Berg,I.A,436
Bliss,E.L.,436,441
Bliss,J.Q,436
Blome,R.,47-48,436
Blume,D.,93,436
Bose,W.K.,148,442
Bowlby,T.,149,436
Boyden,A.,44,436
Brace,C.L.,323,336,342-43,347,350-
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Burgher,J.A.,435Burns,M.,4,389,436
Caius,J,45-47,51,436
Calvin,A.D.,146,441
Carpenter,C.R.,152,436
Castle,W.E.,263,266,436-37
Cattell,R.B.,443
Chambers,R.M.,437
Chapin,J.P.,48-49,437
Charles,M.S.,93,121,437,444
Chaucer,G.,45
Cherner,M.,443
Christake,A.,100,439
Clark,F.,93
Clark,L.D.,105,439
Cloudman,A.M.,338,437
Cohen,C,295,437
Coleman,C.E.,50,437
Collias,N.E,129,143,437
Corbin,J.E.,327,437
Cornwell,A.C,98,226,437,445
Crisler,L.,62-66,71,75,79,140,437
Crow,J.F.,409,437
Dahr,E.,35,37-38,437Darwin,C,29,51,274,404,437Dawson,W.M.,4,334,437Degerb0l,M.,34-35,437Denenberg,V.H.,385,437,443Deshaies,D.,444Dice,L.R.,437DiMascio,A.,437Dobzhansky,T.,333,410-11,437Dollard,J.,144,442Doughty,M.F.,435
449
AUTHORINDEX
AUTHORINDEX
Dubuis,E.,439Duerst,U.,45,438
Easier,C,97,226,314,439
Ellerman,J.R,438
Elliot,O.,73,102,105,109,124,128,
144-45,177,193,236,438,445Erlenmeyer-Kimling,L.,324,440Etkin,W.,81,438Eysenck,H.J.,436
Fabricius,E.,142-43,438Falconer,D.S.,297,298,391-92,438Feider,A.,144Fielde,A.M.,438
Fisher,A.E.,105,132,145,438,445Fredericson,E.,122,305,438,444Freedman,D.G.,105,124,128,438Fuller,J.L.,4,21-22,67,93,97-98,100,105,106,121-23,132,197,226,282,295,314,324,389,391,435-39,444,446Freud,S,3,144
George,W.C,323,439
Gessner,C.,45
Gibson,E.J.,93,446
Gillespie,J.H.,435
Gillum,0.,439
Gilmore,R.W.,69,436
Ginsburg,B.E.,62,67,74,76-77,131,
141,148,394,402,439,445Goldman,E.A,31,37,51,65,447Gordon,T.M.,Jr.,439Gower,J.C.,359,439Grant,D.A.,241,439Gray,A.P.,52,439Gray,P.H.,143,146-47,440Guilford,J.P.,186,440Guttman,L.,210,440
Haag,W.G.,35,440
Hafez,E.S.E.,437,439
Hafez,E.S.E.,437,439
Hall,C.S.,6,194,440
Hammond,W.H,339,440
Hammons,H.G.,400,440
Hansen,E.W.,440
Harlow,H.F.,143,145,226,440,442
Harlow,M.K.,440
Harman,P.J.,86,88,440
Harris,D.,444
Ilatt,R.T.,34,440
Hayes,C,143,440
Haves,K.J.,387,440
Hebb,D.O.,26,353,440
Ht-inroth,O.,142
Hess,E.H.,143,440Hildebrand,M,31,37,51,440Hilzheimer,M.,29,440Hirsch,J.,324,440Howells,W.W.,339,440Humphrey,E.,350,440Hunter,W.S.,242,441
Igel,G.J.,146,441Iljin,N.A.,52,441
Jackson,H.H.T.,31,37,447James,H.,146,441James,W.T.,86,441Jetter,W.,437Jinks,J.L.,324,436Jolicoeur,P.,43,51,83,441
Kaiser,H.F.,348,441
Keeler,C.E.,334,441
Kellogg,L.A.,143,441
Kellogg,W.N.,143,441
King,J.A.,62,73,105,124-28,144,167,
177,282,438,441,444-^5Klyavina,M.P.,98-99,441Kobakova,E.M.,441Koehler,W,226,441Krushinskii,L.V.,59,385,441Kulp,J.L.,33,441
Lacey,B.C.,204,441Lacey,J.I.,204,441Lawrence,B.,38,441Lerner,I.M.,391,441Levine,S„385,441Linnaeus,C.,29-30,56Little,C.C,6,338,389,441Lorenz,K.,142-44,441Lumer,H.,441Lush,J.L.,391-92,441
McCav,C.M,72,442McKusick,V.A.,354,442Marston,M.V.,445Martins,T.,109,442Mason,M.W.,435,442Mason,W.A.,226,442Mather,K.,187,264,324,442Matthew,W.D.,33,442Matthcy,R.,52-53,442Meeh,L.D.,74-75,435,442Menzel,R.,442Miller,N.E.,144,442Mohnnan,R.K.,437Morris,D.D.,444Morrison-Scott,T.C.S.,438
Morton,N.E..409-10.442Marie,A..51,61-65,75-76,140,39S,416,442
Nice,M.M.,143,442
Ogburn,W.F.,14S,442
Packard.A.S..29.442
Parrv.H.B..93.442
Paufv,L.K..45.442
Pavlov.I.P..97.144.195.442
Pawlowski.A.A..159.443
Pfaflenberger.C.J.,17,109,21S,443
Poggiani.C.445
Pribram,K.H.,439
Reed.C.A..34-35.436,443
Reed,S.C.400.410.443
Reed,S.C.400.410.443
Rheingold.H..171.440.443
RibbandsC.R..142.443
Robson.J.A..435
Ross,S..90-91,102,443.445
Rosvold.H.E..439
Royce,J.R.,323,36S-70,443
Sarris.E.G..6S.446
Schenkel.R.,62-65,79,443
Schlager.G..359
SchmFdt.J.R..370,435
Schwab.J.J..333.443
Scott.J.P..5.51.57.59.90.102,109.
113,116.119-20.122.129,143.153.
159.169.197.236.26.5-66.282,324,.394.414.416-17,425,435,438,
439.443-45Searle.L.V..6.194.256.388,445Seitz.A..53.445Seton.E.T..69.445Shade.C.341
Sheldon.W.H.,339,340-43,445Sherif.M..444Singh.J.A.L..147-4S.445Skinner.B.F..100,216.445Smith.A.C.50.314.445Smith,M.E.,439
AUTHORNDO451
Stanlev.W.C..87,100,144.445
Stelmakh.L.X..441
Stevens.S.S.,341.445
Stevens.S.S.,341.445
Stewart.P.B..436
Stockard.C.R..6.42.323.445
Strandskov.H.H..36S.445
Studer,T..35,445
Tembrock,G„62-65.414,445Terhune.A.P..163Thompson,W.R..324.439Thurstone,L.L..34S.36S-69,445Tinbergen,X.,109,446Trattner.A..445Trevelvan,G.M.,45,446Troshikhin.V.A.;86.441,446Trvon.R.C.,5,6,446Tudor-Williams,V.,48,446
VanderMerwe,X.J.,50.446Vogd,H.H..445Volokhov,A.A..446VonUexkiill,J.,68,446
Waddington,C.H.,446--41.446Walk.R.D..93.446Waller.M.B..105.439,446Wamer,L.,350,440Waters,R.H.,444Watson,J.B.,3Welker.W.I.,87,446Werth.E.,32,38.54-55.446White.G.,50,446Wilcke.H.L.,437Wilson,M.O..444Wolfe.H.R.,45,442Wright.S..5.263,266,297,314,392,398,408,446
Yokes,R.M..4
Young,S.P.,31,36-37,51,63-65,447
Zahn,T.,167
Zingg,R.M.,147-48,445
"Acquireddrive,"doesnotexplainsocialization,144,146Activity-successfactor,inperformance
tests,372-73Adaptation,limitedbyspecialization,
427-28Adaptiveradiation
dog,36,55-56,398,432
human,400Adoption,inrelationtosocializationprocess,149Africa
human,400Adoption,inrelationtosocializationprocess,149Africa
disappearanceofaboriginalbreeds,399
distributionofbasenjiin,49
distributionofjackalsin,31Africanhuntingdog,30
fossils,33Age
changesinheritabilitywith,201
effectonemotionalreactivity,198-200,201,312-13,315Aggression;seeAgonisticbehaviorAggressivebehavior,breedcomparisons,
136-37Aggressiveness
independentoftimidity,369-70
measuredbydominancetest,137
problemofmeasurementinearlydevelopment,423-24Agonisticbehavior
basenji,261
cockerspaniel,261
dog,6X),84,757s
inemotionalreactivitytest,202
inheritanceofpatterns,267-68
injuvenileperiod,109452
limitssocializationindog,131-32
insocializationperiod,104-6
intransitionperiod,91-92
wolf,64,75-78Agriculturalrevolution,anddog,34Airedale,history,51Allelomimeticbehavior
Allelomimeticbehavior
dog,63,74-75
effectonsocializationindog,131
injuvenileperiod,110
insocializationperiod,106
wolf,63,74-75America,aboriginaldogbreedsin,399Analysisofvariance
appliedtomatings,298
methods,189-93,298
simplifiedschema,192
seealsoVarianceAnatomy,comparative,evidenceofdog
origin,36-44Ants,socializationin,141-42Arrhythmia;seeHeartrateAssortivemating,effectonhumanbehavior,428Attractionscore,obediencetest,212,214Australia,dingoin,32
Barkingandbarklessness,inheritanceof,
^273-78Barriertests;seeDetourtest;MazetestBasenji
agonisticbehavior,261behavior
inleashtest,306
inmotivationtest,307
inspatialorientationtest,319
SUBJECTINDEX
453
bodvproportions,341
breedingcycle,49,50.67,27
climbingabilityof,219
fearofapparatusin,247
growthcurves,328,330-31
history,48-50
inguinalherniain,389-90
inheritanceofbarkingandbarkless-ness,273-78
manipulativeabilityof,229
origin,296
posturalresponses,288-91
problem-solvingabilityof,258,322
reactiontopassivehandlertest,145
skullmeasurements,40-41,43-44
variationinbodylength,371
seealsoBreedcomparisonsBassethound,skullshape,42Beagle
adaptivecapacities,428
comparedtowolf,402
history,47
otocephalyin,390
asresearchsubject.395
skullmeasurements,40-41,43-44
slowhabitformationin,237-38,425
useaschildren'spet,432
useofsenses,79,80
usedincriticalperiodexperiment,122
vocalizationinstrangeroom,122
weightgain,327
seealsoBreedcomparisonsBees,socializationin,142Behavior,3-7Behaviorgenetics
biometricalgoalsfor,323-25
fieldof,413Behaviorpatterns
inCanidae,63-65,414-15
definition,59
ofdogsandwolves,383-84
inheritance,261-94
methodsofobservation,57-58
inrelationtoinstinct,60
singlefactorandpolygenicinheritance,292-93
asunitsofstudy,58-61Behavioralsystems
definition,59-60
ofdogandwolf,61-80
inrelationtoinstinct,60
relationshipsbetween,61Biometricalgenetics,goalsof,323-25Birds,process
relationshipsbetween,61Biometricalgenetics,goalsof,323-25Birds,processofsocializationin,115,
142-43Biting,inreactivitytest,313-14
Blindness,inheritanceindog,389-90
Bloodhound,history,46-47
Bodyposition,inemotionalreactivity
test,313Bodvproportions,breedcomparisons.
341-42Bodysize,inheritance,286-87Bolognese,skullmeasurements,40-41Borzoi
headshape,29
skullmeasurements,40-42
useofsenses,79Bostonterrier,skullshape,42Boxer,skullmeasurements,40-42Brain,sizeindwarfbreeds,42Breed,proportionofvarianceassociated
with,360-67Breedassociations,objectivesfor,393-94Breedcomparisons
aggressivebehavior,136-37
barkingindominancetest,274-75
bodyproportions,341-42
coefficientsofinbreeding,48^19
congenita]defects,406-7
cue-responsetest,241-42
delaved-responsetest,243
detourtest,228-29
developmentofallelomimeticbehavior,106
developmentofheartrate,121-22
developmentofstartleresponse,94
distressvocalization,92
dominance-subordinationrelationship,156-63,419
emotionalreactivitytest,198-203
eruptionofteeth,96
fearresponses,134-36
followingtest,174-75,177
forcedtraining,215-16
goal-orientationtest,217-18
growthcurves,329-31
handlingtest,134-38
investigatorybehavior,137-38
leash-trainingtest,208-9
manipulationtest,230-31
maternalnursingbehavior,171
maternalretrievingtest,172-73
mazetest,234-35,237-38
inmodeofmotivation,387
mortalityrates,405-6
motivationtest,240
motordevelopment,96
motor-skilltest,220-21
obediencetest,213-14
physiqueandbehavior,345-47
problem-solvingbehavior,257-58
SUBJECTINDEX
quietingtest,206-7
retrievingtest,2IS-19
size,329
ikullshape,37-44
spatial-orientationtest,250-52
statisticalmethodsfor,185-93
summarytable,36061
tail-wagging,137-40
timeofopeningofeye,8990
trailingtest,246-47
variancecomponents,30067
seealsoInheritanceBreeddifferences
inendocrineglands,6
andrearingpractices,385-86
seealsoBreedcomparisonsBreedsymbols,key,10Breeding,scientific,indogs,399Breedingcycle
399Breedingcycle
basenji,49-50,67
dingo,67
dog,67
inheritance,278-83
inwolf,dog,andcoyote,278-79Breedingplan,7-11Breeds
aboriginal,inAmericaandEurasia,399
effectofpanmixison,399
factoranalysisappliedto,371-75
geneticheterogeneityin,29,185,295,378,386-87
history,45-51
notequivalenttoraces,82
aspopulations,393-94
useinresearch,394-95
seealsoundernameofbreedBrusselsgriffon,skullshape,42Bulldog
bull-baiting,77
headshape,29
jawshape,38
short-leggednessin,42
skullshape,40-43,400Bulldocr,French,skullmeasurements40
42Bulldoghead,probablvamutation.42Bush-dog,SouthAmerican.30
fossils,33
fossils,33
Canidae
chromosomenumb,ification,30-31fossils,33geographicalOriginanddistribution
32
serologicalrelationships,44-45Canis
ecologyof,31
geneticsof,51-53
interspecifichybrids,52-53Care-dependencyrelationship
development,176-78
dog,153,174Care-solicitingbehavior;seeEt-epimeletic
behaviorCarnivora,classification,30Castle-Wrightformula,foranalysisof
quantitativeinheritance,263-64Catchingtime,testresults,168Chick,criticalperiodforsocializationin.
143Chihuahua
popularityincities,432
size,56
skulls,43
weight,29China,homeofchow,50Chow,history,50
Chromosomes,infamilyCanidae,52-53Classification,biological,seeTaxonomy
ornameofanimalClassification,ofsocialrelationships,152-
53Cleftpalate,inheritance,389Clubfoot,infoxterriers,390Cockerspaniel
agonisticbehavior,261
behavior
inleashtest,306
inmotivationtest,307
bodyproportions,341
breedingcycle,278-79
earlylearningin,97
growthcurves,330-31
history,48
hydrocephalyin,390
origin,296
posturalresponses,288-91
problem-solvingabilityof,322
skullmeasurements,40—41.43-44
variationinbodylength,371alsoBreedcomparisonsCollie,adaptivecapacities.428Comfort-seekingbehavior
effectonsocializationprocess.14^
secalsoShelter-seekingbehaviorConditionedresponse,experimentsin
transitionperiod,97-100Conditioning
rel.ttionshiptosocializationprocess,144,146
SUBJECTINDEX
455
455
seealsoLearningConfidence,effectonmazeperformance,
237Confidencescore,obediencetest,212,
214Confinementtest
affectedbyhairlength,336-37
variancecomponents,360Co-ordinatedattackrelationship,dog,
154Correlationalmethods,appliedtogenetic-variance,376-78Covariance,methodofanalysis,236Coyote
appearanceandproportions,37
behaviorpatterns,63-65
classification,31
distributioninNorthAmerica,31
fossils,33
interspecifichybrids,52-53
skullmeasurements,40-41,44
socialbehaviorpatterns,62-65
socialgroups,415Criticalperiodconcept,117-18Criticalperiodhypothesis,testsof,122-
29Criticalperiodforlearning
inretrievingtest,22Criticalperiodforprimarysocialization
inbirds,142-43
boundariesof,118-29
dog,108,111,117-50
dog,108,111,117-50
generalphenomenon,417
inguineapig,143
inhumaninfants,115,147-50
inrhesusmonkey,143
insheep,143Criticalperiods,indevelopment,110-12Cross-fostering,resultsof,186,191Cue-responsetest
breedcomparisons,241-42
hybridcomparisons,308-9
methods,238-42Culturalchange,basedonprocessof
learning,424Culturalevolution;seeEvolution,cultural
Dachshund
comparedtowolf,402
leglength,29,42
skullmeasurements,40-41Defects,structural
indogbreedingmanagement,389-90Delayed-responsetest
breedcomparisons,243^44
hybridcomparisons,309-10
methods,242Denmark
domesticationofdogsin,54
possibleoriginofdogin,35
stoneagedogin,34-35Dependency;secCare-dependencyrelationshipDetourtest
test
behaviorduring,227-28
breedcomparisons,228-29
correlationwithtrailingtest,374
effectofmaternalenvironment,284-85
factorloadings
foractivity-successandheart-rate,
372forreactivity,374
methods,19-20,226-27
intestschedule,24
variancecomponents,361-62,366Developmentofbehavior
care-dependencyrelationship,176-78
changesinhandlingtest,176-77
conceptof,16-17
differentiationofbehaviorin,287-92
dog,84-116
dog-humanrelationship,175-80
normalvariationin,119-20
observationalmethods,15-17
problem-solvingbehavior,225-26
processesof,111-12Developmentalgenetics,413Dhole,30
fossils,33Differentiation,growthcurves,332Differentiationofbehavior
fossils,33Differentiation,growthcurves,332Differentiationofbehavior
duringdevelopment,287-92,425
functional,421-22
andgenetics,165-69,181
insocialrelationships,152Differentiationofsocialrelationships,law,
168-69,181-82Dingo
breedingcycle,67
classification,31
origin,32
resultofadaptiveradiation,398
skullmeasurements,40-41Diseasecontrol,methodsof,13-15Distemper,canine,controlof,13-15Dobermanpinscher
history,51
skullmeasurements,40-41Dog
adaptiveradiationof,36,55-56,398.432
SUBJECTINDEX
agonisticbehavior,60,64,75-78
andagriculturalrevolution,34
allelomimeticbehavior,63,74-75
behaviorpatterns,63-65,383-84
behavioralsystems,61-80
comparisonwithhuman,80-83
comparisonwithhuman,80-83
breedingcycle,67,279
caredependencyrelationship,174
chromosomenumber,53
classification,29-31
criticalperiodforprimarysocialization,
117-50developmentofbehavior,84-116developmentofsocialrelationshipsin,
151-82domesticationfromwolf,54-56dominance-subordinationrelationship
in,77effectofhumanculturalchangeupon,
432-33effectofisolationupongeneticchange,
398-99inEgypt,34
eliminativebehavior,65,68-70epimeleticbehavior,63,70-71,169-
75et-epimeleticbehavior,63,72evolution,81-82,397-411,433geneticvariation,4,400-401
indevelopment,418
magnitude,358-66geographicaldistribution,31-32growthandgrowthcurves,326-32humansocialneedsfor,432huntingbehavior,75-76,78-80hybridswithothercanids,52-53ingcstivebehavior,60,65,72-73investigativebehavior,63,78-80inIraq,34inJanno,34inJericho,34-35leader-followerrelationship,175maternalbehavior,169-75inMesopotamia,34-35mother-offspringrelationship,169-75mutationsin,51origin,29-56
evidencefrompre-history,33-36
evidencefromtaxonomy,30-33
fossil(\idence,33
inPalestine,performancetestscomparedwithhuman[Qtests,257periodsof
inPalestine,performancetestscomparedwithhuman[Qtests,257periodsofdevelopment,84112aspilotexperimentforhumanrace,397
polymorphismin,83
serologicalrelationshipwithothercanids,44-45
sex-linkedinheritancenotfound,283
sexualbehavior,62-68
shelter-seekingbehavior,65.73-74
skullshape,38-44
socialbehavior,57-83
socialgroups,61-62,414—15
socialorganizationin,414-29
socialrelationships,153
socializationin,118-41
somatotyping,339^3
specializationin,402-3
stoneage,34-35
territory,62,69,110
useinbehaviorgenetics,325
variationintoothsize,39,41
"wild,"30Dogbreeding,383-96
environmentalcontrolin,384
geneticmanagement,390-91
history,399
hybridizationin,392-93
methodsforassociations,393-91
methodsforkennelowners,393
forphysicaltype,389
forresearch,394-96
selectionmethods,391-92
strainimprovement,391-96
andstructuraldefects,389-90
seealsoRearingpracticesDog-humancomparison,ofheritabilities,
324Dog-humansocialrelationship
development,175-80
noveltyin,415-16
optimumtimeforinitiating,385Domestication
estimateddateandlocation,54-56
effectsondog,400-3Dominance,genetic,effectsonbehavior.
35&-5SDominanceorganizationofgroup,genetic
effectsupon,163-64Dominance-subordinationrelationship
breedcomparisons,156-63
development,155-69
dog,77,154,415
<ffectofgeneticsegregationupon,165-66
effectofheredityon,418-19
effectofsexon,16I
effectofsi/eon,164-65
effectonexpressionof"jealousy,"167
effectonfighting,156-59
injuvenileperiod,109-10betweenmothersandoffspring,175wolf,77,415
Dominancetest
breedcomparisonsofbarking,274-75breedandhybridcomparisons,360measureofaggressiveness,137methods,155-56intestschedule,18-19,24
Drinking;secIngestivebehavior
Duck,socializationin,143
Dwarfbreeds,brainsize,42
Dwarfpinscher,skullmeasurements,4041
EEG,development,93,107Ear,firstfunctionof,94Earlyexperience
dogdevelopmentsuitableforexperiments,112-13EastIndies,dogsin,54Eating;secIngestivebehaviorEcologicalniche,wolfandhuman,397Ecology,Canis,31Egypt,dogsin,34,54Eliminativebehavior
inemotionalreactivitytest,202
injuvenileperiod,109
inneonatalperiod,85
patternsindog,65,68-70
patternsinwolf,65,68-70
patternsinwolf,65,68-70
insocializationperiod,101-2
intransitionperiod,91Emotionalbehavior
effectofgeneticson,6
effectonmazeperformanceinrats,6
effectonperformance,246-47,256,387
effectsontrainability,222
importanceinselectionforperformance,387,394Emotionalreactivity
definition,194
heritabilityof,204
Pavloviantypesof,195
sexdifferencesin,202
unitarynatureof,203,315-16EmotionalreactivityfactorinFihybrids,
374Emotionalreactivitytest
agechangesin,198-201,312-13,315
bitingin,313-14
bodypositionin,313
breedcomparisons,198-203
correlationwithtrailingtest,374
SUBJECTINDEX457
effectofheredityatdifferentages,201
effectofmaternalenvironment,285
effectofmaternalenvironment,285
heartrate,199,313-14
hybridcomparisons,inheritance,312-17
loadingsinactivity-successandheat-ratefactors,372
loadinginreactivityfactor,374
matingdifferences,316-17
methods,194-97
observerreliability,196
responsecategories,196-97
resultsinhome-reareddogs,180
resultsin"wilddogexperiment,"128
tail-waggingin,313-15
intestschedule,21-22,24
variancecomponents,360,366Emotionalresponse,effectofconditioning
upon,100Emotionaltests
factoranalysisof,369-70
variancecomponents,360Endocrineglands,differencesamong
breeds,6England
developmentofdogbreedsin,4548
dogsof,432
firstdogshow,399Englishsetter,hemophiliain,407Environment
effectofvariationonbehavior,236,256
effectofvariationonbehavior,236,256
enrichedeffectsondogsandrats,26-27
physical,25-28
variancecomponents,190Environmentalimprovement,useindog
breeding,384Epimeleticbehavior
dog,63,70-71
selfgrooming,107
wolf,63,71Eskimodog
comparedtowolf,403
resultofadaptiveradiation,398Et-epimeleticbehavior
dog,63,72
inneonatalperiod,85
insocializationperiod,102-4
intransitionperiod,91-92
wolf,63,72Eurasia
aboriginaldogbreedsin,399
distributionofjackalin,31
wolfin,31Europe,dogsof,432
SUBJECTINDEX
involution
behavioraconservativetraitin,415dog,397-411human,399-400,409-12Evolution,cultural
comparedtobiologicalevolution,430-
31effectonbiologicalchange,429-33synergisticrelationshipwithbiologicalvariation,431-33Evolutionofbehavior,dogandhuman,
81-82Experimentaldesign;seeMethodsEye
developmentinsocializationperiod,
107developmentintransitionperiod,93-
94inheritanceofdefects,389-90timeofopening;inbreedsandhvbrids,89-90
Factoranalysis
breedandhybridpopulations,371-75
emotionalandphysiologicaltests,369-70
evidenceofgeneraltraits,367-68
andgenetics,343-44,368-99,376
performancetests,370-71
physique,340,343^4,347-51Failure,effectonmotivation,230-31,256Fearofapparatus
inspatialorientationtest,320
intrailingtest,246-47,256Fearresponses
breedcomparisons,134-36
development,104-5
seealsoAgonisticbehaviorFeeblemindedness,correlatedwithlow
fecundity,410Fennec,chromosomenumber,53Fertility
declinewithage,110
increaseunderdomestication,401-2
probleminhumanpopulations,410Fighting
effectofdominancerelationshipupon,156-59
seealsoAgonisticbehavior;Dominance-subordinationrelationshipFighting,playful
developmentof,105-6
effectonsocializationindog,130
inheritance,269-73Followingtest
breedcomparisons,174-75,177
methods,173-74Foodandfeeding,11-12,14Foodrewards,effectondog-humanrelationship,177-78Forcedtraining,205-16
breedcomparisons,215-16
non-unitarynatureofreactions,215-16Fossils,fromCanidae,33Fox
chromosomenumbers,53
comparedtowolf,403
fossils,33
serologicalrelationshipwithothercan-ids,4^-45
socialbehaviorpatterns,62-65
socialgroups,414-15Foxterrier
clubfootin,390
earlylearningin,97-9S
groupattacksby,106
history,50
rateofdevelopment,418
reactiontopunishment,145
sizefactorin,349
skullmeasurements,40-41,43-44
useofsenses,80
weightgain,327
seealsoBreedcomparisonsFrance,dogsof,432
Geneaction,theoryofspecific,333-34Geneticeffectsonbehavior,3-7Geneticequilibrium,theoryof,407-8Geneticvariation,indevelopmentofdog
andhuman,418Genetics
anddifferentiationofbehavior,165-69.181
andfactoranalysis,367-69.376
ofgenusCanis,51-53
sub-divisions,413Geographicaldistribution,dogandother
Canidae,31^32Germanshepherd
fewcorrelationsofphysiqueandbehavior,350
hipdysplasiain,407
jawshape,39
skullmeasurements,40-42Goal-orientationtest
breedcomparisons,217-18
correlationwithtrailingtest,374
correlationwithtrailingtest,374
methods.217
variancecomponents,361(loldenretriever,history,50
Goose,primarysocializationin,142Greatdane
agonisticbehavior,7S
jawshape,39
size,56,400-401
skullmeasurements,40-42Greyhound
comparedtowolf,402
history,45-47,51
jawshape,38
leglength,29
origin,399
skull,400
skullmeasurements,40—43Growth
dog,326-32
injuvenileperiod,108
modelforlearningprocess,332,352-53
relationtoperiodsofdevelopment,326-29Growthcurves,dog,328-31Guarddog,Kurdish,34Guineapig
criticalperiodin,143
polydactylousmonster,333
Habitformation
effectofheredity,425limitsvariabilityofbehavior,151weaktendencyinbeagle,237-38Habit-formationtest;seeGoal-orientation
testHaircolor,inheritanceandrelationto
behavior,338-39Ilairlength
inheritance,262,334-36inrelationtosizeandbehavior,336-37Handlingtest
breedcomparisons,134-38correlationwithtrailingtest,374developmentalchanges,176-77effectsofhandfeedingupon,177-78effectofmaternalenvironment,284-85ofhome-reareddogs,179-80inheritance
offearreactions,267-68ofplayfulaggressiveness,269-73loadingin
activity-successandheart-ratefactors,372reactivityfactor,374methodsresultsin"wilddogexperiment,"125
SUBJECTINDEX459
intestschedule,18,24variancecomponents,360,366Handler,effectonobediencetest,212.
214Hardy-Weinberglaw,404-5Heartrate
changeswithage,199effectofmaternalenvironment,285inheritance,287inreactivitytest,199,313-14relationtoarrhythmia,203responsetoquieting,199variancecomponents,360,366Heart-ratedevelopment,breedcomparisons,121-22Heart-ratefactor,ofphysiologicaltests,
372-73Hepatitis,infectiouscanine,controlof,
15Hemophilia
inEnglishsetter,407inheritance,389Heredity
actionthroughdevelopmentalprocesses,113culturalandbiologicalcompared,430-
31effects
31effects
ofculturalevolutionupon.431-33ondevelopmentofsocialrelationships,421-24ondifferentiationofbehavior,152ondominanceorganizationofgroup.
163-64onlearningcapacities,424-25,428-
29onsocialrelationships,113,418-10onsocializationprocess,133-41ontrainability,222-23onvariationandhabitformation,425magnitudeofeffectonbehaviorand
physique,358-66synergisticrelationshipwithcultural
evolution,431-33variancecomponents,190,321Heritability
ofbehavior,andselection,391-92effectofpracticeon,254-56emotionalreactivitytest,201,316leashtrainingtest,299,301,305limitationsandusefulness,324-25measuredbyintraclasscorrelation,192methodsofestimation,185-86motivationtest,308obediencetest,311
460SUBJECTINDEX
problemsolvingbehavior,321,388
jrcssionanalysis,297-98specificityofestimates,323-25summarytable,360-61Hernia,inguinal,inbasenji,389,406Heterogeneitv,inpurebreeds,185,295,
7,386-87Heterosis;seeHybridsuperiorityHipdysplasia
inGermanshepherds,407inheritance,359,391History,dogbreeds,45-51Home-reareddogs,socialrelationships,
17&-82Homozygosity,rareinpurebreeds,378Hostility,towardsimilarandunlikedogs,
167-68Hounds,agonisticbehavior,77Housebreaking,behaviorpatternsuseful
in,102Housing
designofnurseryroomandruns.25-
"26planforall-weatherkennel,27Humanbehavioralsystems,80-83critical
"26planforall-weatherkennel,27Humanbehavioralsystems,80-83criticalperiodininfant,147-50dangerfrommutations,408-9developmentofsocialorganization,
417ecologicalniche,397effectof
assortivematinson,428isolationupondevelopmentof.147-48ivolution,81-82,399-400,409-12fertility-andsterilityproblems,410geneticchangein,399^00
triationindevelopment,41BIQtestscomparedwithdogtests,257periodsofdevelopmentin,113-16ymorphism,usefulnessof,83,411-'12prenatalmirtalityrate,410sociali.(■•dsfordoes,432somatotyping,339-40variation.401Hunting,behaviorpatternsindogand
wolf"
Huntingdiicalrecords,45-4S
Hybridcomparis
08-9n\la\t.309-10
tartlcresp•'tfvity,315lotionoft
leashtraining,299-306
mortalityrates,405-6
motivationtest,307-8
motordevelopment,96
motor-skilltest,221-22
obediencetest,311
physiqueandbehavior,345-46
spatial-orientationtest,318-20
statisticalmethods,297-98
summary,360-61
timeofopeningofeye,89-90
variancecomponents,360-66
seealsoInheritanceHvbridization,indogbreeding,392-93.
396Hybridsuperiority
inbasenji-cockerci
inmotivationtest,307
inmotivationtest,307
inspatialorientation.31vHybrids
behaviorof,295-325
factoranalysisof,371-75
reactivityfactorinFi,374
forresearch,395
betweenspeciesingenusCants,52-53Hydrocephaly,incockerspaniel,390
Icelandicdog,skullmeasurements,40-41Imprinting
equivalenttoprimarysocialization,142ohoSocialization,primary;Socialization,period;Socialization,processInbreeding,infoundationstock,48-49Individualvariation
indelaved-re^:.243-4I
310inemotionalreactivity,202inmazetest,237inspatial-orientationtest,251variancecomponentswithinlitters,190-91.321,364-67[ngestrvebehaviordog.60.85,72effectonm131,
144-46insocializationperiod,101intransitionperiodswolf,65,72-7Inheritance,modeof
ianccandvocalizationpatl267-6S
ingandbarkl<aviorpatterns.261-94bod)
SUBJECTINDEX
461
emotionalreactivitytestscores,312-
17haircolor,338hairlength,262,334-36heartrate,287leashfighting,268-69multiple-andsingle-factortheories,
367-68noclearpatternsinperformancetests,
367-68noclearpatternsinperformancetests,
285-86patternsofagonisticbehavior,267-78playfulfighting,269-73posturalresponses,288-92quietingtest,287-88selectionand,392structuraldefects,389-90wildnessandtameness,266-69seealso,Single-factorinheritance;PolygenicinheritanceInsightlearning,developmentindetour
test,228-29,256Instinct,inrelationtobehaviorpatterns
andsystems,60"Intelligence"concept
noevidenceofgeneralfactor,256,388,
427seealsoProblem-solvingbehaviorIntelligencetests;seeTest;Performance
testInteraction,genotype-lifehistory,325Intraclasscorrelation,measureofherit-
ability,definition,192Investigativebehavior
breedcomparisons,137-38indogandwolf,63,78-80effectonsocializationindog,130inemotionalreactivitytest,200inneonatalperiod,85insocializationperiod,104intransitionperiod,91Iraq,dogin,34Irishwolfhound,skullmeasurements,40-
41Isolation
effectsonsocializationprocessandhumandevelopment,145-48andgeneticchangeindogs,398-99
Jackal
appearanceandsize,37
chromosomenumber,53
classification,31
distributioninAfrica,Eurasia,31
fossils,33
hybrids,52-53
serologicalrelationshipswithothercanids,45
skullmeasurements40-41,44
socialgroups,415
vocalization,50Jackdaw,socializationin,142Jarmo,dogin,34
Jawshape,ofdogsandwolves,38-41"Jealousy,"inrelationtodominance-subordinationrelationships,167Jericho,dogin,34-35,54Juvenileperiod,dog,108-10
KasperHauser,caseofpartialisolation,
147-48KingCharlesspaniel,history,46
Labradorretriever,history,50
Laplanddog,skullmeasurements,40-41
Leader-followerrelationship,dog,154
indogandwolf,175,415Learning
analogywithgrowth,332,352-53
basicprocessofculturalchange,424,430
complexinteractionwithheredity,426-28
effectofheredityupon,424-25,428-29
effectsonexpressionofgeneticvariation,425-26
effectsonsocializationprocess,144
limitingfactoronbehavioralvariation,428
seealso;Training;PerformanceLearningcapacities
injuvenileperiod,109
inneonatalperiod,87-88,98
insocializationperiod,107-8
intransitionperiod,97-100Learningcurves,mazetest,235Leash-controltest;seeLeash-trainingtestLeashfighting
inheritanceof,268-69
inleash-trainingtest,301-5Leash-trainingtest
breedcomparisons,208-9
demeritscoresinhybrids,299-300
effectofmaternalenvironment,285
heritability,299,301,305
hybridcomparisons,298-306
inheritanceofleashfighting,268-69
intercorrelationsofdemerits,210
loadingsonreactivityfactor,374
methods,207
SUBJECTINDEX
resultsin"wilddogexperiment,"127-2fl
intestschedule,22.24
variancecomponents,361-62,366Legs,mutationforshortness,42Levelsoforganization,inrelationtobehavior,5Lip-licking,inemotionalreactivitytest.
199Litterdifferences
incue-responsetest,242,309
inemotionalreactivity,203
inleash-controltest,301-2
proportionofvarianceassociatedwith,190-91,364-67
inspatial-orientationtest,319Localization,processof,102—4,112
Mammals,socializationin,143-44
Man;seeHuman
Manchesterterrier,chromosomenumber,
53Manipulationtest
breedcomparisons,230-31,361correlationwithtrailingtest,374hybridcomparisons,361loadinginactivitv-successfactor,372method,229-30Mastiff
agonisticbehavior."9history,46Masterlistofexperimentalanimals,10Maternalbehaviordog,169-75.151limitsperiodofsocializationinsheep,
L30weaningtest,173seealsoEpimeleticbehaviorMaternalenvironment
effectsontests.283-85,363onleashtraining,300-301onreactivitytest.317Matings,differencesbetweenanalysisofvariance,29Sincue-responsetest,309inleash-controltest.302-5inreactivityte>t.316-17
inceassociatedwith,190-91,364-66Maturation,interactswithgeneticdiffer-
er.Mazeperformance,rats,effectofemotionalbehavior,6Maz-
behaviordur
Icomparison,234-3"_
correlationwithtrailingtest.374
loadinginactivity-successfactor.172
methods,232-34'
and"positionalhabit"factor,370
variancecomponents,236-37,361Mendeliangenetics,413Merlegene,geneticmanagement,390Mesopotamia,dogin,34,35
domesticationofdogsin,54Methods
analvsis
of'qualitativeinheritance,264-66ofsingle-factorinheritance.262-66ofvariance,159-93,236
breedingplans,7-11
correlational,appliedtogeneticvariance,376-78
cue-responsetest,238-42
delaved-responsetest.242
detourtest,19-20,226-17
diseasecontrol,13-15
dominancetest,155-56
emotionalreactivitvtest,194-97
followingtest,173^74
genetic,7-11,296-97
goal-orientationtest216-17
handlingtest,133-34
leash-trainingtest.207
manipulationtest.229-30
maternalretrievingtest,171
mazetest.232-34
motivationtest.240
motor-skilltest,219-20
nutrition,11-12
obediencetest.211-12
observationofbehaviorpatterns.r"58
observationofdevelopment,15-17
performancetests.19-25
physiquemeasures,340-41
quietingtest.206
retrievingtest.2IS
sanitation.13-14
ofscalinc
socialbehaviortests.17-19
spatialorientation,248-50
statistical
breedcomparisons.1^5-93hvbridcomparisons,297-98
trailingtest,244-45
variancecomponentcomputation,359
weaningtest,173Mexicanhairless.29.400MiddleEast,d\
mentonbreeddifferences,191Moleculargenetics,413
SUBJECTINDEX
463
Molossianhound,56
Monorchidism,inShetlandsheepdog,390
Mortalityrates
breedandhybridcomparisons,405-6
humanprenatal,410Mother-offspringrelationship,dog,169-
75Motivation
breedcomparisons,3S7
effect
offailureon,230-31,256onperformance,3S7-SS,428-29onproblem-solving,230-31methodusedinperformancetests,20-21Motivationtest
breedcomparisons,240
effectofmaternalenvironment,2S5
hybridcomparisons,307-8
method,240
staninescaling,188-S9Motorcapacities
injuvenileperiod,108-9
inneonatalperiod,87
insocializationperiod,107Motordevelopment
breedandhybridcomparisons,96
breedandhybridcomparisons,96
Intransitionperiod,94-96Motor-skilltest
breedcomparisons,220-21
correlationwithtrailingtest,374
hybridperformanceon,221-22
loadinginactivity-successfactor,372
methods,219-20
intestschedule,22,24
variancecomponents,361Multiple-factorinheritance;seePolygenic
inheritanceMutations
accumulationindogs,405-8
basisofvariationindog,51-52
dangerinhumanpopulations,408-9Mutualcarerelationship,indog,154Mutualdefencerelationship,dog,154Myelination,inneonatalperiod,88
Naturalselection
anddegeneration,404,408
roleinhumanpopulations,403,410Neonatalperiod
characterizedbyneonatalnutrition,416
declineofnursingin,170-71
dog,84-89
rearingpracticesfor,384
Newfoundlandbreed,skullmeasurements,40-41"Nicking,"useindogbreeding,392-93NorthAmerica
breeding,392-93NorthAmerica
distributionofcoyotein,31
dogsin,55
stoneagedogsin,35
wolvesin,31Norwegianharehound,skullmeasurements,40-41Nursingbehavior,170-71Nutrition,methodsof,11-12
Obediencetest
breedcomparisons,213-14hybridcomparison,311loadingsinactivity-successandheart-ratefactors,372methods,211-12intestschedule,22,24variancecomponents,361Obesity,inShetlandsheepdog,390,406Observerreliability,inemotionalreactivitytest,196Olfaction,inneonatalperiod,86"One-mandog,"lackofevidencefor,
213-14;223Organizationofbasiccapacities,intraining,222Otocephaly,inbeagle,390Outbreeding,protectsrecessivegenes,405
Palestine,dogin,34Panmixis
effectondogbreeds,399
human,400Parent-offspringcorrelation;seeRegressionanalysisPassive-handlertest
reactionofbasenjis,145
resultsin"wilddogexperiment,"125-26Pekingese,skullmeasurements,40-42Performance,effectsofemotionaland
motivationaldifferences,387-88Performancetests
correlationwithtrailingtest,374
factoranalysisof,370-71
ofhome-reareddogs,180
loadingsinactivity-successfactor,372-73
methodsof,19-25
motivationin,20-21
noclearpatternsofinheritance,285-86
SUBJECTINDEX
relationshipsbetween,21
scheduleoftesting,22-24Periodsofdevelopment
dog,84-116
andgrowth,326-29
human,113-16
andproblem-solving,224
processesof,416Persistencetest;seeSpatial-orientation
test"Personality"
andbehavioralorganization,80
expressedassocialrelationships,166-67,419-20Physiology,comparative,evidenceondog
origin,44^45Physiologicalgenetics,413Physiologicaltests
factoranalysisof,369-70
heart-ratefactor,372-73Physique
andbehavior,breedandhybridcomparisons,344-47
factoranalysis,346-51
generalsizefactor,348-49,371
generalsizefactor,348-49,371
magnitudeofgeneticeffectson,358-66
methodsofmeasurement,340-41
relationtobehavior,326,333-55,389
variancecomponents,360,362,366Pleiotropy
inbehavior,375
hypothesesconcerning,333,371
limitedoccurrenceof,352
andtypeconcept,353-54Pointers
agonisticbehavior,78
comparedtowolf,403
history,48
skullmeasurements,40-41Polydactyly,guineapig,333Polygenicinheritance
ofbehaviorpatterns,293
expressionof,262-63
theory,367-68Polymorphism
indogs,wolves,humans,83
usefulinhumansocieties,411-12
wolf,398Poodle
hairlength,29
hairstructure,400
skullmeasurements,40-41Populationconcept
skullmeasurements,40-41Populationconcept
appliedtodogbreeds,393
appliedtodogskeletons,37-44
appliedtohumanpopulations,354-55
ofspecies,30
useintaxonomyandgenetics,351-52Populationgenetics,413-14Populations,wolf,variationin,43Posturalresponses,inheritance,288-92Practice,effectonheritability,254-56Predation;seeHuntingPrehistory,evidenceofdogorigin,33-36Problem-solvingbehavior,224-58
asadaptation,388
breedcomparisons,257-58
dog-humancomparison,257
dualprocesstheoryof,322-23
heritabilityof,321,361,388
motivationand,255,320-21
unitarynatureof,256-57,388-89Problem-solvingtests
scheduleoftesting,22-24
varianceofcomponents,361Processes,ofdevelopment,111-12Psychologicalprocesses,insocialrelationships,151-52Pug
headshape,29
skullmeasurements,40^2Punishment,effectonsocializationprocess,145-46
Qualitativeinheritance,methodofanalysis,264-66Quantitativeinheritance,methodofanalysis,263-64Quietingtest
breedcomparisons,206-7,360
differentiationofbehaviorin,425-26
hybridcomparisons,360
inheritance,287-88
loadinginactivity-successfactor,372
loadinginreactivityfactor,374
method,206
Raccoondog,chromosomenumber,53Raceconcept,inrelationtotypeand
populationconcepts,354-55Races,notequivalenttodogbreeds,82Radiation,effectsonmutation,409Rat
effectofenrichedenvironment,26-27
cflcctsofgeneticsonbehaviorof,5-6
Rattlepinscher,skullmeasurements,40-
41Reactivitytest;secEmotionalreactivity
testRearingpractices,384-87Regressionanalysis
SUBJECTINDEX
465
ofheritability,297-98
ofleash-controlscores,305
ofmotivationtest,30S
ofobediencetest,311Reliability
leash-trainingtest,207
obediencetest.213
obediencetest.213
tial-orientationtest,254-55rch,useofpurebreedsandhvbridsin.394-96Retric-
agonisticbehavior,7S
useofsenses,79Retrievingtest
breedcomparisons,219
criticalperiod.II
methods.218
intestschedule,22.24Retrievingtest(maternal)
breedcomparisons.172-73
method,171Rewardtraining,216-23
asmethodofsocialcontrol,155Rhesusmonkey
criticalperiodin,143
effectofrearinginisolation,145Russia,stoneagedogin,35
SaintBernard
jawshape,38,39
size,400
skullmeasurements,40-42
weight,29Saluki
gazellehuntin:
history,51
leglength,29
skullshape.42
useinMiddleEast.
useofsenses,79Sanitation,methodsof,13-14Scaling
methodsof,324
staninesystem,186-89Scheduleoftesting,24Schnauzer,skullmeasurements,40—41Scottishterriers,useofsenses,80Sealvhamterriers,chromosomenumber,
53Segregation,genetic
effectonvariance,357-58
evidencefor,355-58Selection,effectlimitedbyheritability,
391Selectionprocedures,indogbreeding,391-92,396
Sensorycapacities
inneonatalperiod,S6-S7
useinhunting.79Separation,effectsuponsocialization
process,149-50Serologicalrelationships,betweencanidae,
"44-A5Setters
agonisticbehavior.
comparedtowolf,403
history,46
skullmeasurements,40-41Sexdifferences
effectondominance-subordinationrelationship,164-65,419
growthcurves,329-32
noneinemotionalreactivity,202-3Sex-linkedinheritance,2S3
notfoundindata,362Sexualbehavior
dog,62-6S
effectonsocializationindog,130-31
effectonsocializationinsheep,129
home-reareddogs,179
inheritanceofbreedingcycle,278-83
injuvenileperiod,110
insocializationperiod,106-7
wolf,62-68Sexualrelationship,dog,154Sheep
criticalperiodin,143
developmentofflockorganization,417
effectofhumansocializationupon,129-30Sheepdogs
agonisticbehavior,78
comparedtowolf,403Sheepdogs;seeShedandsheepdogShelter-seekingbehavior
dog,65,73-74
intransitionperiod,92
wolf,65,73-74Sheltie;seeShedandsheepdogShetlandsheepdog
earlylearningin,97
history,50
managementofmerlegenein,390
managementofmerlegenein,390
obesityandmonorchidismin,390
readyhabitformationin,425
sizefactorin,349
skullmeasurements,40-41,43-44
stereotypedbehaviorin,237
seealsoBreedcomparisonSingle-factorinheritance,367-68
behaviorpatterns,292-93
methodsofanalysis,262-66
Size
breedandsexdifferences,329-32
correlationwithbehavior,344-51
effectondominance-subordinationrelationship,164-65
inrelationtohairlength,337
variationindog,401Skeleton
dog,37-44
wolf,51Skullmeasurements,wolf,40-41,51Skullshape,ofdogs,wolves,andother
canids,38-44Smell,senseof;seeOlfactionSocialbehaviorpatterns
changesintransitionperiod,89-93
coyote,62-65
dog,57-83
fox,62-65
methodsofmeasuring,17-19
inneonatalperiod,84-86
insocializationperiod,101-7
wolf,57-83Socialcontrol,indog-humanrelationship,
154-55Socialdevelopment,correlatedwithsocialorganization,416-17Socialenvironment,experimentaldesign,
17-18Socialgenetics,subjectmatter,413-33Socialgroups,61-62Socialorganization
incaninesocieties,414-29
correlatedwithsocialdevelopment,416-17
stabilizingeffectongeneticchange,429-30Socialrelationships
classification,152-53
definition,151
developmentindog,151-82,416
differentiationofbehaviorin,152,416
dogandhuman,152-53
effectofheredityupondevelopment,113,421-24
expressionof"personality"in,166-67,419-20
psychologicalprocessesin,151-52Socialrelationship,tests
scheduleof,18-19
variancecomponents,360Socialization,dog-human,optimumtime
for,385Socialization,primary
inants,141-42
inbees,142
inbirds,142-43
indogs,118-41
inmammals,143-44Socializationperiod
characterizedbydevelopmentofsocialrelationships,416
dog,101-8
rearingpracticesin,385
variationinboundaries,120-22Socializationprocess
analysisof,144-47
behavioralmechanisms,129-33
effectsofadoptionupon,149
effectsofgeneticdifferences,133-41
effectsofseparationupon,149-50
largelyindependentofoutsidestimuli,146-47Somatotype
indogandhuman,339-43
evaluationofconcept,351Songsparrow
rapiddevelopmentin,115
socializationin,143Spain,originofspanielin,46Spaniels
chromosomenumber,53
comparedtowolf,403
history,45-48
seealsoCockerspanielSpatial-orientationtest
breedcomparisons,250-52
correlationwithtrailingtest,374
effectofmaternalenvironment,285
fearofapparatusin,320
geneticvarianceconstantin,426
hybridcomparisons,318-20
loadinginactivity-successfactor,372
methods,248-50
persistencein,250
reliabilityof,254-55
intestschedule,23-24
thresholdeffect,320
timeanderrorsin,251,253-254
variancecomponents,361Specialization
effectofdomesticationupon,402-3
imposeslimitsonadaptation,427-28Species,populationandtypeconcepts
of,30Sport,historicalrecords,45-48Springerspaniel
earlylearningin,97
history,48Staninescalingsvstem,descriptionandprocedure,186-89
SUBJECTINDEX
467
Startleresponse,breedandhybridcomparisonsofdevelopment,94Stereotypedbehavior,inmazetest,237Sterility,inhumanpopulations,410Stoneagedogs
geographicaldistribution,34-35
skullshape,37-38Strainselection,effectofaccidental,283-
84Suckling,effectofsuddenweaningon,90Sucklingbehavior
inneonatalperiod,85
intransitionperiod,89-90"Superman"myth,403,411
T-mazetestapparatus,239
commonvariancewithtrailingtest,377correlationwithtrailingtest,374loadinginactivity-successandheart-ratefactors,372loadinginreactivityfactor,374and"positionalhabitfactor,"370intestschedule,23-24variancecomponents,361,366SeealsoCue-response,motivation,anddelayed-responsetestsTail-wagging
breedcomparisons,136-40
inemotionalreactivitytest,202,313-
15equivalenttosmile,104Tameness,inheritanceof,266-69Taxonomy,evidenceofdogoriginfrom,
30-33Teeth
eruptionoffirstcaninesandincisors,
95-96eruptionofpermanentteeth,108sizevariationindogs,39,41Temperature,controlandrecordingof,
26Terriers
26Terriers
agonisticbehavior,77comparedtowolf,402-3history,46-47seealsoFoxterrierTerritory
dog,62,69,110wolf,61,69,76Test
effectsofmaternalenvironmenton,
283-85seealsoScheduleoftesting,24,andundernameofspecifictest;seealso;Emotionaltests;Performance
tests;Physiologicaltests;Physique,Problem-solvingtests;Socialrelationship;TrainingtestsThresholdeffects
inemotionalreactivitytest,314inspatialorientation,320Timidity,independentofaggressiveness,
369-70Timidityfactor,375-77Trailingtest
breedcomparisons,246-47commonvariancewithT-mazetest,377correlationwithperformancetests,374effectofmaternalenvironment,285fearofapparatusin,246-47loadinginactivity-successfactor,372method,244-45intestschedule,22,24variancecomponents,361,366Trainability,205-23Trainabilitytests,variancecomponents,
360-61Training
effectongeneticvariance,210-11,
213,222-23,254-55effectonobediencetest,213asformofproblem-solving,225Training,forced,reducesexpressionof
geneticvariation,425Traitconcept,inadequacy,427Traits,littlegeneralityof,323-24,375,
378Transitionperiod
characterizedbydevelopmentofadult
behaviorpatterns,416dog,89-101
rearingpracticesfor,385variationinboundaries,120"Tryondistribution,"264,266,270-73,
280-82"Type,"resultofselectionfor,393-94"Type"concept
appliedtobehavior,371
andemotionalreactivity,195
inadequacyof,351-52
littleevidenceforbehavioral"types,"
427relatedtopleiotropy,353-54inrelationtoraceconcept,354-55ofspecies,30useandabuseindogbreeding,389
Undershotjaw
inbasenji,406
inheritance,389UnitedStates,dogsof,432
SUBJECTINDEX
Variance
betweenbreeds,185,190-91,295effectoftrainingongenetic,210-11,
213,254-55proportionattributedtomatings,litters,andindividuals,364-67insegregatingandnon-segregatingpopulations,357-58Variancecomponents
breedandhybridcomparisons,360-67inmazetest,236-37methodofcomputing,359theoreticalanalysis,190-91Variation
extentinformandbehaviorofdog,4,
400-401useindogbreeding,396Visualclifftest,93-94Vocalization
developmentofreactiontostrangepen,
102^inemotionalreactivitytest,202inleashtrainingtest,305-6onscale,breedcomparisons,92onscale,loadinginheart-ratefactor,
comparisons,92onscale,loadinginheart-ratefactor,
372onscale,loadinginreactivityfactor,
374onscale,variancecomponents,360instrangeroombybeagles,122
Walking,timeofdevelopment,95Weaning
effectonnon-nutritivesucking,90
processof,101Weaningtest,method,173Weight,gainperweekinpuppies,327Whippet,skullmeasurements,40-41"Wilddogexperiment,"oncriticalperiod
hypothesis,124-29Wildness
development,105
effectofdomesticationupon,402
inheritanceof,266-69
Wire-hairedfoxterrier;seeFoxterrier
Wolf
agonisticbehavior,64,75-78allelomimeticbehavior,63,74-75appearanceandproportions,36-37behaviorpatterns,63-65,383-84behavioralsystems,61-80breedingcycle,278classification,29,31
developmentofpackorganization,416domesticationofdogfrom,54-56dominance-subordinationrelationship
in,77ecologicalniche,397eliminativebehavior,65,68-70epimeleticbehavior,63,70-71et-epimeleticbehavior,63,72fossils,33
huntingbehavior,75-76,78-80hybrids,52-53
Indian,asancestorofdogs,38ingestivebehavior,65,72-73investigativebehavior,63,78-80leader-followerrelationship,175inNorthAmerica,Eurasia,31polymorphism,83,398relationshiptomodemdogbreeds,433resultsofhumansocialization,140-41serologicalrelationshipwithotherca-
humansocialization,140-41serologicalrelationshipwithotherca-
nids,45sexualbehavior,62-68shelter-seekingbehavior,65,73-74skeleton,51skullshapeandmeasurements,38-41,
43,51socialbehavior,57-83socialgroups,61-62,414-15territory,61,69,76
unspecializedcomparedtodog,402-3variationinpopulations,43,51
"Wolfchildren,"148-49
Workingdogs,breedingof,394
Worms,intestinal,controlof,13