Polly, P. D. 2019. Geometric morphometric tests for phenotypic divergence between chromosomal races. Pp. 336-364 in J. B. Searle, J. Zima, and P. D. Polly (eds.), Shrews, Chromosomes and Speciation. Cambridge University Press: Cambridge, United Kingdom.

10

Geometric Morphometric Tests for Phenotypic

Divergence Between Chromosomal Races

P.DavidPollyandJanM.Wójcik

Introduction

Asitisinotherorganisms,morphologicaldivergenceisanimportantcomponentofspeciationandevolutioninshrews.GertrudeSteiniswidelyquotedinstatisticaltextsassaying‘adifferencetobeadifferencemustmakeadifference’:thephenotype‘makesadifference’forevolvingbecauseitinteractswiththeexternalworld,regardlessofwhetherthatmeanswithothershrews,withtheenvironmentorwiththeclimate.Becausemutationanddriftacttochangetheaveragephenotypeofapopulation,twopopulationsareexpectedtodivergeiftheyareseparatedbygeographicorbiologicalbarrierstogeneflowunlessstabilisingselectionpreventsit,andiftwoisolatedpopulationsliveindifferentenvironments,thendiversifyingselectionislikelytopromotethatdivergence.PatternsofmorphologicaldivergenceinSorexaraneusthusprovideaninterestinginsightintotheeffectsofchromosomalvariationonevolution,especiallywhenmorphologicalvariationiscomparedatincreasinglyhigherhierarchicallevels:betweenenvironmentsinlocalpopulations,betweenpopulationswithinachromosomalrace,betweencloselyrelatedraces,betweenmajorgroupsofracesandbetweenspecieswithintheS.araneusgroup.Allthingsbeingequal,morphologicaldivergenceshouldincreaseateachoftheselevelsifRobertsonianrearrangementsareimportantbarrierstogeneflowandiftheyaroselongenoughagoformorphologicaldifferencestohaveevolved.

InthischapterwecriticallyreviewthemorphometricdataavailableforthehierarchicalstructuringofphenotypicdivergenceinS.araneus.ManyaspectsofmorphologicaldifferentiationwerereviewedinChapter3,including‘Dehnel’sphenomenon’andanalysesbasedonlinearmorphometrics.Herewecomparephenotypicdifferentiationatdifferenthierarchicallevels,askingwhetherevidenceexistsforincreasingdifferentiationaswemovefromlocalpopulationstochromosomalracestochromosomalphylogroupsandfinallytodifferentspecies.Wefurtherfocusonwhetherenvironmentaldifferencesarecorrelatedwithmorphologicaldifferences,asonemightexpectifthedifferencesare

2

producedbynaturalselectionratherthandrift.Wealsoconsidergeographicdistances,whichmaybeimportantpromotersofmorphologicaldivergenceinsuchsmallanimalswithsuchalargegeographicdistributionindependentofenvironmentalselection.Becausedifferentmorphologicaltraitshavedifferentrelationshipstotheenvironment,weconsideraspartofthisreviewthebiologicalandgeneticunderpinningsofthosetraitsthathavebeenstudiedinS.araneus.Inadditiontoreviewingtheresultsofpublishedstudies,wepresentnewanalysesofmorphologicaldisparityinS.araneusandofthecorrelationbetweenmorphologicaldivergenceandthetotalsizeofmetacentricchromosomes.

Theworkwereviewshowsthatmorphologicaldivergenceisgreater

betweenlocalpopulationsandbetweenlargephylogroupsandspeciesthanitisbetweenchromosomalraces.Thedegreeofmorphologicaldivergencebetweenchromosomalracesdoesnothaveaclearrelationshipwitheitherthecomplexityofhybridkaryotypesorthetotalsizeofthemetacentricchromosomes,bothofwhichareexpectedtoreducegeneflowandfacilitatephenotypicdifferentiation.OurreviewsuggeststhatRobertsonianvariationinS.araneusdoesnothaveasimplerelationshipwithmorphologicaldivergence,eventhoughthereisdemonstrablepotentialforpopulationstodivergerapidly.ThepatternsofmorphologicalvariationinS.araneusareprobablyamosaicofancientdifferentiationderivedfromrepeatedexpansionandcontractioninandoutofglacialrefugiaandrecentdifferentiationthatblossomsinsmalllocalpopulations,onlytoberesorbedintolargermetapopulations(seeChapter13).

WhilemorphologicalinvestigationsofS.araneusstartedinthe1950s(e.g.

Serafiński,1955;Schubarth,1958),itwasHausserandJammot(1974)whofirstsystematicallyinvestigatedmorphologicaldivergenceinconjunctionwithchromosomalandgeneticinformation.Thelatterauthorssetthestandardforsubsequentstudieswiththeirmultivariateanalysisof30measurementsofthemandibleandlowerdentition(Fig.10.1a).Usingprincipalcomponentanalysis(PCA)anddiscriminantfunctionanalysis(DFA),theyestablishedthattwochromosomalgroups,whichwerethenthoughttobeconspecificbutthatarenowrecognisedasthedistinctspeciesS.araneusandS.coronatus,couldbedistinguishedbytheirmandibularshapeaswellastheirchromosomes.ModificationsofHausserandJammot’smeasurementschemehavebeenusedbymanysubsequentresearchers,makingresultsreadilycomparableacrossstudies(Chapter3).Geometricmorphometricanalysisoflandmarkcoordinatesfromthemandible,craniumandmolarswasintroducedinthe2000s(Polly,2001,2007)(Fig.10.1b–d).Themandiblelandmarkdatacloselyparallelthemandiblemeasurementdata,butdifferinthatsizeisnormallypartitionedoutingeometricmorphometricanalysessothatonlypureshapedifferencesareconsidered(Bookstein,1991;DrydenandMardia,1998),whereassizeisnormallyretainedinmultivariateanalysesofmeasurementdata,usuallyappearingonthefirstprincipalcomponentwhenPCAisused.Modifiedlandmarkschemesformandibles,craniaandmolarshavealsobeenadoptedbymanyrecentauthors,resultinginasecondsetofdatathatcanbecomparedacrossstudies.

3

Figure 10.1 Morphometric schemes used in Sorex araneus research. (A) Multivariate measurement scheme for the mandible used by Hausser and Jammot (1974). Left mandible is shown in medial view at bottom, condyle in dorsal view at upper left and molars in occlusal view at upper centre. Scale bar: 10 mm. (B) Geometric morphometric landmarks of the lateral mandible used by Polly (2007). Scale bar: 10 mm. (C) Geometric morphometric landmarks of the ventral cranium used by Polly (2007). Condylobasal length is measured from landmark 5 to 25. Scale bar: 10 mm. (D) Geometric morphometric landmarks of the first lower molar in occlusal view used by Polly (2001). Scale bar: 0.5 mm. Parts B–D are modified from Polly (2007) with permission.

Data and Methods Geometricmorphometricdatafromsomeofourpreviousstudieswere

integratedandreanalysedforthischapter(Polly,2007;Pollyetal.,2013).ThepatternsofsizeandshapevariationbasedonthesedataareshowninFig.10.2.Thesepatternsarediscussedindetailandintegratedwithpreviouslyreportedpatternsintheremainingsectionsofthischapter.Thecoloursofthecirclesoneachmapshowtherangeofeachrespectivevariablefromsmalltolarge(orfromnegativetopositive,inthecaseofthePCscores)usingatemperaturemapwherethecool,bluecoloursareatthesmallendandthewarm,redcoloursatthelargeend.Thesizeofthecirclesshowshowdisparatethesamplesarefromthemean.Thelargest,bluestdotsare,thus,thesmallestmostdisparatesamples,andthelargest,reddestdotsarethelargest,mostdisparateones.ForthetwoshapevariablestherelationshipbetweencolourandsizeofthedotsismorecomplicatedbecausethecolourshowstherangeofshapefromthenegativetothepositiveendofPC1(theaxisofgreatestshapevariation),whereasthe

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disparityiscalculatedbasedonallthePCsdefiningthefullmultivariateshapespace.Thus,forexample,thesamplesthataremostdisparateinskullshapearelargest,buttheyhaveanintermediateyellowcolourbecausetheirdisparityarisesinallPCsbutthecolourisbasedonlyonthefirstPC.

Figure 10.2 Morphometric differentiation in Sorex araneus. Data for 27S. araneus karyotypic races and two sister species are shown (A), colour coded by their nearness on the karyotype

AbAi

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5

phylogenetic network of White et al. (2010) (abbreviations in Table 10.1 and Chapter 5). The total size of the metacentric chromosomes is shown for comparison (B), the size of the circles proportional to the total size of the metacentrics (colours grade from cool to warm with proportional size). For each locality, elevation (C), mean annual temperature (D) and the natural log of annual precipitation (E) are also shown for comparison (colours grade from cool to warm as each variable grades from low to high). Mean centroid size of mandibles (F) and skulls (G) are shown with cool colours grading through warm colours as size grades from small to large (mean size is white). Partial size disparity is represented by the size of each circle, the largest circles being the most extreme in size (the darkest blue and brightest reds are the most disparate). Mean shape on principal component 1 (PC1) of mandibles (H) and skulls (I) is shown with cool colours at the negative end of PC1 and warm colours at the positive end. Partial disparity of shape is shown based on all the principal components of shape space: the largest circles show the populations that are most disparate in overall shape, whereas the colours only show shape variation on PC1.

Thedataconsistoflandmarksofthemandibleandskull(Fig.10.1b–c)

from27ofthe74knownraces,plusS.antinoriiandS.coronatus,EuropeansisterspeciestoS.araneus.The27racescoverthefullgeographicrangeofS.araneus.Table10.1liststhesamplesandsummarisestheirmorphometriccharacteristics.ThelandmarksofeachsamplewereProcrustessuperimposed(RohlfandSlice,1990),averagedandthesamplemeansre-superimposed.Principalcomponentswerecalculatedfromthecovariancematrixoftheresiduals(DrydenandMardia,1998).Principalcomponentscoresareshapevariables,coordinatesinamultidimensionalshapespacethatencompassesthevariationinpureshapeofthemandibleandskulllandmarks.Thefirstprincipalcomponent(PC1)isusedtoillustratethemajoraxisofvariationinshapeofthemandibleandskull.Partialdisparities,whichshowtheextenttowhicheachindividualcontributestotheoveralldiversityinshape,werecalculatedfromalltheprincipalcomponentsfollowingtheprocedureofFoote(1993).Disparityisameasureofthedistanceofeachsamplefromtheoverallmean,sothepopulationswhoseshapesarethemostdifferenthavethehighestdisparities.Mandibleandskullsizes,whichareproxiesforbodysize,werecalculatedasthecentroidsizeofthelandmarksoneachspecimen.Centroidsizeisthesumofthedistancesfromeachlandmarktotheshapecentroidandisanumberthatcannotbecomparedbetweendatasets–itisthebestestimateofsizethatisindependentoftheshape(Bookstein,1991).Becausecentroidsizeincreaseswiththenumberoflandmarks,resultscanbecomparedwithinadatasetbutnotbetweenthem.Sizedisparitywascalculatedusingthesameprocedure.DetaileddescriptionsofthesedataandmethodscanbefoundinPolly(2007).

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Table 10.1

Mean trait measurements and associated data for the morphometric samples analysed in this chapter. Note that

elevations are given for the location where the morphometric sample was collected. Mandibles Skulls

Race Abbr N Longitude Latitude Elevation(m)

CentroidSize

SizeDisparity

PC1Score

ShapeDisparity

CentroidSize

SizeDisparity

PC1Score ShapeDisparity

S.antinorii SA 31 13.73 46.03 796 12.03 0.25 -0.00379 0.00059 31.37 0.12 0.00518 0.00027

S.coronatus SC 24 0.01 47.36 98 11.99 0.29 -0.00305 0.00102 32.22 0.25 0.00687 0.00042

Aberdeen Ab 18 -2.03 57.35 23 12.33 0.04 0.00978 0.00076 32.07 0.12 -0.02304 0.00111

Abisko Ai 7 18.83 68.37 340 12.60 0.01 0.00607 0.00038 31.50 0.05 -0.00040 0.00032

Åkarp Åk 15 13.12 55.65 21 12.38 0.02 -0.00141 0.00017 31.28 0.19 0.00335 0.00033

Baikal Ba 4 105.00 51.20 1545 13.51 0.97 -0.02236 0.00097 32.98 1.58 0.01883 0.00072

Białowieża Bi 34 23.87 52.70 156 11.86 0.44 -0.00274 0.00013 31.13 0.35 -0.00289 0.00016

Chysauster Cy 19 -5.55 50.15 142 12.31 0.05 0.00075 0.00030 31.91 0.04 -0.01425 0.00055

Cordon Co 10 6.60 45.90 1263 13.20 0.46 0.00093 0.00019 32.79 1.15 0.00984 0.00032

Drnholec Dr 25 16.50 48.87 169 13.36 0.70 0.00511 0.00113 31.90 0.03 0.00191 0.00024

Hällefors Hä 16 14.50 59.78 190 12.29 0.06 -0.00742 0.00044 30.42 1.70 0.00130 0.00031

Hermitage He 37 -1.27 51.67 52 12.46 0.00 0.00368 0.00025 32.22 0.25 -0.00397 0.00029

Jura Ju 16 6.02 46.48 845 12.84 0.10 -0.00034 0.00036 32.43 0.50 0.00849 0.00035

Kalvitsa Ka 14 27.13 61.90 117 12.05 0.23 -0.00185 0.00015 31.56 0.03 0.00767 0.00023

Kuhmo Ku 3 30.22 63.92 207 11.61 0.84 0.01281 0.00056 30.37 1.83 -0.00298 0.00039

ŁeguckiMłyn Łg 12 19.72 53.37 145 12.15 0.14 -0.01022 0.00023 31.40 0.10 -0.00653 0.00028

Lemi Lm 19 27.27 61.12 104 12.34 0.04 0.00176 0.00048 31.72 0.00 -0.00152 0.00025

Moscow Mo 50 38.50 55.92 141 13.37 0.71 0.02832 0.00111 31.63 0.01 0.00716 0.00614

Novosibirsk No 17 83.23 54.73 106 13.17 0.42 0.00084 0.00018 32.47 0.56 0.00797 0.00034

Öland Öl 12 16.42 56.25 11 12.25 0.08 -0.01143 0.00047 30.91 0.66 -0.00180 0.00029

Oxford Ox 8 -1.17 51.80 102 11.91 0.38 0.02230 0.00118 31.43 0.09 -0.02407 0.00093

Savukoski Sa 3 27.27 67.47 234 11.46 1.14 -0.02481 0.00103 29.92 3.24 -0.00426 0.00023

Seliger Se 74 33.50 57.17 270 13.35 0.68 0.03472 0.00143 31.68 0.00 0.00687 0.00610

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Serov Se 9 60.83 59.83 120 12.88 0.13 -0.00426 0.00018 32.64 0.85 0.00458 0.00026

Tomsk To 5 84.92 56.36 74 14.30 3.14 0.02460 0.00123 33.63 3.66 0.00941 0.00626

Ulm Ul 36 9.95 48.30 522 12.21 0.10 -0.01071 0.00023 31.39 0.11 -0.00035 0.00022

Uppsala Up 12 15.67 63.17 229 12.47 0.00 -0.00572 0.00031 31.45 0.08 -0.00567 0.00017

Vaud Vd 32 7.10 46.27 1695 12.76 0.06 -0.01751 0.00049 32.17 0.20 0.01134 0.00030

Wirral Wi 12 -3.13 53.33 8 11.81 0.51 -0.02405 0.00124 31.31 0.17 -0.01902 0.00052

Abbr:abbreviatedchromosomalracename.

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Therelativesizeofthemetacentriccomponentofeachkaryotypewascalculatedusingrankordersizeofthefundamentalarmsmakingupthemetacentrics.The21fundamentalchromosomearmsofS.araneusarelabelledathroughuinorderofdecreasingsize(Searleetal.,1991),givenrankordervaluesof21through1.Foreachmetacentricinthekaryotype,thesizevaluesweresummedforthetwoarmscomposingit,andthesevaluesweresummedacrossthemetacentricsinthekaryotype.Wherethefusionoftwoarmsintoametacentricisvariablewithinarace,themetacentricconditionwascounted.Forexample,thekaryotypeoftheBaikalraceisaf,bc,g,hi,j/l,k,m,n,o,p,q,r,tu,wherejandlarevariablyjoinedinthemetacentriccondition.Thustheranksizeoffundamentalarmsa,f,b,c,h,i,j,l,tanduweresummedtogive128fortheranksizeofthemetacentriccomplementoftheBaikalrace(21+16+20+19+14+13+12+10+2+1).

Ourphenotypicdataarecomparedwithseveralbiologicalandnon-biological

factors.ElevationwastakenfromtheTerrainBasedataset(RoweandHastings,1994)andmonthlyandannualtemperatureandprecipitationwastakenfromWilmottandLegates(1998).

Genetic and Developmental Aspects of the

Phenotypes ThestudyofS.araneusphenotypeshasfocusedprimarilyonsizeandshapeinthe

cranium,mandiblesandteeth.Thesestructureshavedifferentgenetic,developmentalandfunctionalcontrolsandareexpectedtoresponddifferentlytoselectionandtohavedifferentrelationshipswiththeenvironmentandgenetics(CaumulandPolly,2005).Thethreestructuresdifferfunctionally.Sizeisrelatedtometabolicrate,dietandcompetition(Schmidt-Nielsen,1984);mandibleandskullshapearerelatedtojawmechanics,brainsizeandolfaction(HankenandHall,1993;Monteiroetal.,2003);andmolarshapeisrelatedtotheinterlockingofoccludingteethduringmastication(EvansandSanson,2003;Pollyetal.,2005).

Mandibularsizeinlaboratorymice,forexample,isaffectedby12quantitativetrait

loci(QTL),whilecranialshapeisaffectedbyasmanyas50QTLsscatteredoverall19autosomes(Klingenbergetal.,2001,2004;Ehrichetal.,2003;Leamyetal.,2008).Toothshapeisinfluencedbyasmanyas50genesthatarechannelledbymorphogeneticprocessesintosixorsevenindependentfactors(Salazar-CiudadandJernvall,2002,2004,2010).Mandibleandskullbonescanrespondplasticallythroughgrowthandremodellingtoconditionsexperiencedbyanindividualanimal(Grüneberg,1963;HankenandHall,1993),aphenomenonthatisobviousinshrewsthroughDehnel’sphenomenon(seeChapter3).Toothcrowns,ontheotherhand,cannotberemodelledafterenamelmineralisationiscompleted(Hillson,1986;Schroeder,1987),aneventthathappensbeforetheteetherupt.Thus,inS.araneusallnon-geneticenvironmentaleffectsinteethare

9

bufferedbothbytheindividual’sownhomeostasisandthehomogenousenvironmentofthemother’swomb,whereasskeletaltraitsarenot,implyingthattoothtraitsshouldhavehigherheritabilitythanskeletaltraitsandlessnon-geneticcorrelationwiththeanimal’smacroenvironment.Forcomparison,heritability(h2)ofmolarshapeintheshrewCryptotisparvawasestimatedtobe0.34overall,rangingfromzeroto0.81forindividualmolarsubstructures(PollyandMock,2017).Heritabilitiesofthemajorcomponentsofmandibularshapevariationcanstillbehigheventhoughtheyaresubjecttolifelongenvironmentaleffects,withoverallh2being0.29andcomponentsrangingfromzeroto0.73inmice(KlingenbergandLeamy,2001).Multivariateshapetraitsfrequentlyexhibit‘overdominance’,whichmeansthatheterozygotehybridmorphologiesarenotintermediatetothehomozygotemorphologies(Cheverudetal.,2004;Ackermannetal.,2006),aphenomenonthathasbeenfoundincommonshrewmandibleandcranialshape(Pollyetal.,2013).

Size Variation Despitethebiologicalimportanceofbodysizeinmammalianresearch(e.g.McNab,

1980;Schmidt-Nielsen,1984),bodymasshasonlyrarelybeenreportedinS.araneusstudies.Perhapsbecauseoftheirrapidgrowthandthedramaticseasonalchangesintheirbodysize(Pucek,1970),sizehasmoreoftenbeenreportedascondylobasallength,whichisthelengthoftheskullfromthepremaxillaetooccipitalcondyles(e.g.Hausseretal.,1990;Zimaetal.,2003)(Fig.10.1c).Immaturecommonshrewsreachsummerweightsof7–8gduringtheirfirstyear,butthosethatsurviveintothewintersufferadropinbodymassanywherefrom27percent(inBritain)to45percent(inFinland)duringthecold,leanmonthsandultimatelyreach10–12gthenextspringwhentheyreachsexualmaturity(Pucek,1970;Churchfield,1990;Chapter2).Dehnel’sphenomenon,whichisaconsequenceofthedropinbodymass,isdescribedinChapter3.Moreisknownaboutvariationinskullandmandiblesize,however,thanbodymassinthestrictsenseandthesizepatternswereviewherearebasedontheseosteologicalstructures.

Sorexaraneusisgenerallysmallerinthenorththaninthesouth(Ochocińskaand

Taylor,2003;Polly,2007;Shchipanovetal.,2011;butseeStefen,2013).ThesmallestshrewsarefoundinnorthernScandinavia,belongingtotheSavukoskiandKuhmoraces,whilethelargestareintheAlpsandspreadacrossSiberia,theTomskracebeingthelargestofall(Fig.10.2;Chapter3).Ourdataonskullcentroidsizesupporttheconclusionthatsizeissmallerathighlatitudes,withlatitudeexplaining20percentofthevarianceinsize(Fig.10.3a).

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Figure 10.3 Skull centroid size in relation to latitude (A), elevation (B), mean annual temperature (C), and mean January temperature (D). P values for the least squares regression and R2 values are indicated. AnassociationbetweensizeandelevationhasalsobeenreportedforS.araneus,

withlargeshrewstypicallyfoundathigherelevations(Homolka,1980;Polyakov,2003;Polly,2007;Shchipanovetal.,2011).Forthemostpart,thesereportsarebasedonlocallylargerracesbeingfoundathigherelevationsthanlocallysmallerones.SuchlocallylargerracesincludeBaikal,Cordon,Jura,Serov,TomskandVaud.Ourdatasuggestthatthereisonlyaweakrelationshipbetweensizeandelevation,withelevationonlyexplaining11percentofvariationinskullcentroidsize(Fig.10.3b).Amultipleregressionofsizesimultaneouslyontobothlatitudeandaltitudeismarginallysignificantforbothvariables(P=0.07),butcollectivelyexplainsonly22percentofthevarianceinsizecomparedwiththe20percentexplainedbylatitudealone.ThehighestelevationsarefoundintheAlps,whicharealsoatthesouthernpartofthecommonshrew’sgeographicrange,creatingastronginteractionbetweenlatitudeandelevation.

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OchocińskaandTaylor(2003),whostudiedfiveEurasianspeciesofSorex,

suggestedthatthelatitudinalclineinS.araneussizeisanexampleofinverseBergmann’srule.Theyattributedthepatterntoselectionforsmallbodysizeinregionswherefoodisscarceinwinter,basedonthefactthatsizeintheirdatawaspositivelycorrelatedwithspringandautumnevapotranspiration,whichis,inturn,relatedtoplantproductivityandtheabundanceoftheinvertebratefaunathatshrewsconsume.OchocińskaandTaylor(2003)alsohypothesisedthatthesizeofshrewsmaydependonthesizeoftheirinvertebrateprey,whichareprobablysmalleraswellaslessabundantinregionswithcoldwinters,basedonthefindingofHanski(1994)thatsmallshrewsaremoreefficientathandlingsmallpreyitemsthanarelargeshrews.AsimilarexplanationwasofferedearlierbyMezhzherin(1964),whoattributedthesmallsizesatnorthernlatitudestotheinfluenceofwintercoldtemperatureonpreyabundanceandsize.Interestingly,sizeinourdatawasnotrelatedtoeithermeanannualtemperatureormeanJanuarytemperature(Fig.10.3c–d;seealsoChapter3).

Differentiation by Hierarchical Scale Severalstudieshavelookedatvariationbetweenpopulations,betweenraces,

betweenkaryotypegroupsandbetweenspeciesinanefforttodeterminetheextenttowhichkaryotypedifferencesinfluencephenotypicdifferentiation(SearleandThorpe,1987;Wójciketal.,2000;Poroshinetal.,2006;Mishta,2007;Polly,2007;Shchipanovetal.,2011;Stefen,2013).Generally,thesestudieshavefoundthatvariationbetweenpopulationswithinracesisgreaterthanvariationbetweenraces,thoughsomeracesaremoredivergentthanothersdependingontheirphylogeographichistory.Evenincaseswhereparapatricracesbelongtodifferentkaryotypephylogroups(‘karyotypicgroups’;Chapters4and6)thedifferentiationbetweenthemmaybesmallcomparedwiththevariationwithintheraces,suchasinthecaseoftheGuzowyMłynandŁęguckiMłynraces,whichbelongtotheWestandEastEuropeankaryotypicgroupsrespectively(Banaseketal.,2003).

Hierarchicalstructuringinseveralphenotypictraitshasbeenstudiedsystematically

usingF-statistics(Polly,2007).QSTisameasureoftheproportionofbetween-grouptowithin-groupvarianceinquantitativecharacters,andisacommonmetricforassessingdifferentiationbetweenpopulationsatdifferenthierarchicallevels(Wright,1951;Lande,1992;Spitze,1993).Polly(2007)lookedatdatafrom43populationsrepresenting24chromosomalracesofS.araneusandthespeciesS.antinoriiandS.coronatus(asubsetofthosedatacomprisemostofthedatausedinthischapter).Hetestedforhierarchicalstructuringinskullsize(proxyforbodysize),molarshape,skullshapeandmandibleshape(Fig.10.1b–d),theresultsofwhicharereportedagainhereinTable10.2.

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Table 10.2 DivergenceinfourphenotypictraitsatfourhierarchicallevelsmeasuredwithFST.ReproducedfromPolly(2007)with

permission.

FST

SkullSize MolarShape SkullShape MandibleShape

BetweenPopulationsoftheSameRace 0.11(±0.019) 0.11(±0.014) 0.09(±0.024) 0.08(±0.012)

BetweenRaces 0.04(±0.004) 0.04(±0.001) 0.01(±0.002) 0.01(±0.001)

BetweenKaryotypicGroups 0.13(±0.019) 0.15(±0.009) 0.05(±0.005) 0.04(±0.003)

BetweenSpecies 0.06(±0.011) 0.07(±0.004) 0.04(±0.004) 0.08(±0.004)

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ThegreateststructuringofthephenotypesinS.araneuswasfoundatthelevelsofpopulationswithinarace(QST=0.08to0.11)andkaryotypicgroups(QST=0.04to0.15)(Table10.2).Severalotherstudieshavefoundsignificantdifferencesinphenotypesbetweenpopulationswithinraces(SearleandThorpe,1987;Wójciketal.,2000;Shchipanovetal.,2011;Stefen,2013),includingpopulationsthatappeartobepartitionedbylocalhabitatsuchasflatwoods(floodplainashandalderforest),drymeadowsandsedgebogs(Wójciketal.,2003).Structuringamongchromosomalraceswasstatisticallysignificant,butmuchlowerthanbetweenpopulationswithintheracesorbetweenkaryotypicgroups(QST=0.01to0.04).Inotherwords,thehierarchicallevelthathastheleastpronouncedphenotypicstructuringwithinS.araneusisthechromosomalrace.Shchipanovetal.(2014)foundsimilarpatternsonamoredenselysampledgroupofchromosomalracesinEuropeanRussia.Theimplicationsofthelackofstructuringbychromosomalracearediscussedfurtherbelowandelsewhere(Chapters9,11,13and14),butfornowitisworthnotingthatevidenceexiststhatatleastminorphenotypicdifferentiationcoincideswithkaryotypeboundaries,indicatingthatracehassomeeffectonphenotypicdifferentiation.SkullandmandibleshapewerelessdifferentiatedatallthreelevelswithinS.araneusthanweremolarshapeandskullsize.

Structuringbetweenspecies(QST=0.04to0.08)wasnogreaterthanbetween

populationsorkaryotypicgroups,thoughinterestinglythegreatestbetween-speciesstructuringwasfoundinmandibleshape,whichwasthetraitwiththeleaststructuringatthechromosomalraceandgrouplevels(Table10.2).Earlierstudieshadalreadyidentifiedmandibleshapetobeamorereliableindicatorofspeciesidentitythanotherinternalorexternalcharacters(HausserandJammot,1974;Hausseretal.,1990,1991).DiscriminantfunctionanalysisofmandibleshapewasabletoclassifyindividualscorrectlytothespeciesS.araneus,S.coronatusandS.antinorii100percentofthetime(Hausseretal.,1991;Polly,2007);discriminantanalysisofskullshapeidentifiedS.antinorii100percentcorrectly,butdistinguishedS.coronatuscorrectlyonlytwo-thirdsofthetime,andskullsizewasnotabletosignificantlydistinguishthethreespecies(Polly,2007).Differentiationbetweenmoredistantlyrelatedspeciesismorepronounced(Vasil’evetal.,2015;Shchipanovetal.,2016;OnishchenkoandKostin,2017).

Differentiation Across Hybrid Zones Phenotypicdifferencesbetweenchromosomalracesofcommonshrewshavebeen

studiedinclinesacrossseveraldifferenthybridzones,ateachofwhichsignificantdifferenceswerefound.DifferencesinmandibleshapehavelongbeenknownattheinterspecifichybridzonebetweentheVaudraceofS.araneusandS.antinoriiinHaslitalValleyinSwitzerland(Hausseretal.,1991).Differentiationatseveralintraspecifichybridzoneshasalsobeennoted.DifferencesinmandibleshapewerefoundatthetriplejunctionbetweentheMoscow,SeligerandWestDvinaracesintheValdaiHillsnorth-eastofMoscow,Russia(Grigoryevaetal.,2011).Hybridsbetweentheseracesformmeioticchainsconsistingof9–11(Moscow–Seliger)andsixchromosomes(Moscow–WestDvina).Polyakovetal.(2002)foundsignificantdifferencesinsizeandshapebetweenthe

14

NovosibirskandTomskracesinSiberia,wherethehybridsformmeioticchain-of-ninechromosomes(discussedbelow).Sizemeasurementsofthehead,body,tailandfeetofshrewswerefoundtodifferacrossanareaofahybridzonebetweentheDrnholecandŁęguckiMłynracesinPoland,butnotacrossanotherhybridisationareabetweenthetworacesorbetweentheDrnholecandBiałowieżaraces(Chętnickietal.,1996).Hausseretal.(1991)foundagradationofmandiblemorphologyfrompureVaudracetopureCordonracesamplesthroughanareaofintermediateforms.TheCordonraceishighlyacrocentric,whichfacilitateshybridisationand,inprinciple,geneflow.BoththeCordonandVaudracesbelongtotheWestEuropeankaryotypicgroup.

Pollyetal.(2013)lookedspecificallyatphenotypicclinesthroughtwonarrow

hybridzoneswheregeneflowisexpectedtobelow:theNovosibirsk–TomskzoneinSiberiaandtheMoscow–SeligerzoneinEuropeanRussia.Clinesinskullandmandibleshapecorrespondedcloselytoclinesinmetacentricchromosomes,bothintermsofthelocationoftheclinecentresandtheirwidth(seeFig.10.4forclinesinskullwidth).AttheNovosibirsk–Tomskzonethephenotypicclinecentreforskullshapewaslocatedonly0.31kmfromthemetacentricclinecentre,andattheMoscow–Seligerzoneboththemandibleandskullclineswerecentredlessthan0.2kmfromthemetacentriccentre.TheclineinskullshapeattheNovosibirsk–Tomskzonewas6.8kmwide,whereastheclinesinmandibleshapewere24.7and36.0kmwide.Seeminglyinagreement,somemetacentricsthatformameioticchainofnineinthesamezonehadclinesthatrangedfrom8.5to13.3kmwide,buttheonesthatformachainofmthreehadclinesthatwere52.9kmwide(Polyakovetal.,2011).IntheMoscow–Seligerzonethephenotypicclineswere2.5to4.2kmwide,comparedwiththemmetacentricclinesthatwere3.2to3.6kmwide(Bulatovaetal.,2011).Atfouroutofsixhybridzonesforwhichmeasuresofbothphenotypicandgeneticdifferentiationareavailable,phenotypicdifferentiation(QST)wasgreaterthangeneticdifferentiation(FST),suggestingthatselectionplaysaroleindifferentiatingtheracialphenotypes(Pollyetal.,2013)(Table10.3).Interestingly,geneticdifferentiationwashigherthanphenotypicdifferentiationonlyfortheinterspecieshybridzonebetweentheVaudraceandS.antinorii,wherethereisnogeneflowbetweenthegroups(Brünneretal.,2002a,b).

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Figure 10.4 Phenotypic clines in skull shape across two hybrid zones, the Novosibirsk–Tomsk (A) and Moscow–Seliger (B). Each graph shows the mean skull shape at each of several collecting sites (numbers), standardised so that the mean shape of the Novosibirsk and Seliger races equals 0.0 and the mean shape of the Tomsk and Moscow races equals 1.0. A tanh cline has been fit to these data and the centre (dark grey vertical line) and width (light grey bar) have been estimated from the curve. The x-axis is scaled to the centre of the metacentric clines at each hybrid zone. Reproduced from Polly et al. (2013) with permission.

1

2

4

5 6

10

11

12

13

171922

23 242730

3233

34

35 123 45 6

789

10

1112

1314

1617

18

Distance from hybrid zone centre (km)-15 -10 -5 0 5

-0.5

0.0

0.5

1.0

1.5

-15 -10 -5 0 5-0.5

0.0

0.5

1.0

1.5

Novosibirsk side

Tomsk side

Seliger side

Moscow sideCentre: 0.31Width: 6.81

Centre: -0.14Width: 2.50

BA

Skul

l Sha

pe

Distance from hybrid zone centre (km)

16

Table 10.3

Comparative differentiation among hybrid zones.

HybridZone F1Hybrids QST N FST QST/FST Nm ZoneWidth(km)

Uppsala–Hällefors RIV 0.124 13/9 0.021 5.9 92 2.3

Cordon–S.antinorii CV+2CIII 0.101 27/9 0.103 1.0 1 1

Vaud–S.antinorii CXI 0.079 31/27 0.167 0.5 0 0.9

Drnholec–Ulm 2CIII 0.051 22/37 -- -- -- 36

Drnholec–ŁęguckiMłyn

CV+RIV* 0.050 22/14 0.015 3.3 16 5

Novosibirsk–Tomsk CIX+CIII 0.040 68/43 0.032 1.3 -- 6.8

Drnholec–Białowieża

CX 0.037 22/31 0.002 18.5 131 1

Moscow–Seliger CXI 0.021 50/74 -- -- -- 2.5

ForeachhybridzonetheF1hybridmeioticconfiguration(CIII,chainofthree;RIV,ringoffour;etc.),phenotypicdifferentiationinmorphometricshape(QST,thisstudy),morphometricsamplesizeforthetworaces(N,thisstudy),molecularestimateofgeneticdifferentiation(FST,publishedliterature),rateofintrogressionacrossthezone(Nm,publishedliterature)andmetacentriczonewidth(publishedliterature)arereported.ZonesaresortedfromhighesttolowestQST.(UpdatedfromPollyetal.,2013.)

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Theevidencefromindividualhybridzonesthussuggeststhatkaryotypeboundariesbetweenparapatricracesareimportantintersectionsofphenotypicdifferentiationandthatthebarrierstogeneflowcreatedbyhybridzonesaresubstantialenoughthatdiversifyingselectioncanacttofurtherdifferentiatethephenotypesoneithersideofhybridzones.Chromosomalracethusseemstobeanimportantfactorinphenotypicdifferentiation,despitethefactthatlessvarianceisassociatedwithitthanwithdifferencesinindividualpopulationsorwithlargerphylogroupandspeciesdifferences.

Phenotypic Differentiation in Relation to

Metacentric Size Hausser(1994)proposedthatthepresenceoflarge,incompatible

metacentricchromosomesintwohybridisingracesmayreducegeneflowtoagreaterextentthansmallmetacentricsoracrocentrics,anideasimilartothelatertheorydevelopedbyNooretal.(2001)andRieseberg(2001).Wetestedthishypothesisbymeasuringtherelationshipbetweendifferentiationandthecombinedsizeofthemetacentriccomponentofthekaryotypeinourdata.Forourmorphometricsamples,weassignedfundamentalchromosomesarankordersizeusingtheproceduredescribedaboveandcalculatedthedisparityinsizeandshapeofeachsample.Ifthecombinedsizeofthemetacentricchromosomesdecreasesthepossibilityofgeneflowthen,onaverage,theraceswithmore,largermetacentricsshouldbetheonesthataremostdifferentiatedordisparate.ThegeographicdistributionofthesizeofthemetacentricsisshowninFig.10.2b,thelargestbeingpredominantlyintheeastandinScandinavia(butnotetherelativelysmallsizeoftheBaikalmetacentricsattheveryeasternendoftherange).DisparityinsizeandshapeareshownbythesizeofthecirclesinFig.10.2f-g.Wefoundnorelationshipbetweencombinedmetacentricsizeanddisparityinmandiblesize(P=0.34),skullsize(P=0.11),mandibleshape(P=0.98)orskullshape(P=0.56).Inotherwords,ourdatashownoevidencethatraceswithlargemetacentricsaremorelikelytobedifferentiatedthanthosewithsmallmetacentrics.

WhileourdatadonotsupportHausser’shypothesis,theydonot

necessarilycontradictitbecausehisargumenthingedonthecomparativesizeofthemetacentricsinbothmembersofaparapatricpairofraces.Ifonememberhadlargemetacentricsbuttheotherwaspredominantlyacrocentricgeneflowcouldstillbesubstantial.

Nevertheless,ourdatasuggestthatraceswithlargemetacentricsarenot

morelikelytobehighlydifferentiated,asonewouldexpectwithcomparativelyrestrictedgeneflow,eventhoughthegeographicpatternofmetacentricsizeindicatesthatraceswithlargemetacentricsareoftenfoundadjacenttooneanother.

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Isolation by Distance

ThegeographicrangeofS.araneusstretchesnearly5000kmeasttowestandasmuchas3000kmnorthtosouth.Regardlessofphysicalorgeneticbarrierstogeneflow,physicaldistanceislikelytobeasignificantbarrier,especiallyforanimalswhosehomerangesarelessthanonesquarekm(seeChapter2).Alatitudinalclineinskullsizehasalreadybeendiscussed,accountingfor20percentofthevarianceinsizeamongraces(Figs10.2gand10.3a).Aclineinskullshapeisvisibleinourdata,butthereisseeminglynoclineinmandibleshape(Fig.10.2h–i).Skullshapegradesroughlyfromeasttowest,withtheBritishandScandinavianshrewsbeingsimilarononeextreme(darkblue,lightblueandyellow-greencolours)andthesouthernEuropeanandSiberianshrewsbeingsimilarontheother(yellowandredcolours).

Theeast-westdifferencesinskullshapearepartlydrivenbyfrequencychangesinthepolymorphicpresenceandabsenceofthefifthupperantemolar(Fig.10.5).Inshrews,theteethbetweenthefirstincisorandthefourthpremolarareoftentermedantemolarsbecausetheirhomologytoincisors,caninesorpremolarshasnotalwaysbeenclear(Dannelid,1998;butseeHutterer,2005).InpopulationsofS.araneusintheeasternpartofitsrangethefifthantemolarisalmostuniversallypresent,butitisvariablyabsentinthewest.PolymorphicabsencehasbeenreportedinpopulationsfromPoland,Germany,Sweden,FinlandandBritainatlevelsaround1–2percent,withthegreatestfrequencyreportedfromtheIsleofIslayinwesternScotland,at52percent(Reinwaldt,1961;Skarén,1964;Schmidt,1967;CorbetandSouthern,1977;Hausseretal.1990;Polly,2007).Theshapeoftherostrumiscorrelatedwiththepresenceandabsenceofthefifthantemolar,andthehigherfrequencyofthepolymorphisminthewesthasaneffectonthemeanskullshapeforthepopulationsthere.

Figure 10.5 Palate of Sorex araneus showing the differences in the number of antemolars and shape of the rostrum that contribute to the east-west gradient in skull shape. A specimen of

19

the Aberdeen race from Dumbreck, Scotland at the western end of the geographic range (A) and the Novosibirsk race from Kemerovo, Russia at the eastern end (B) are shown. Black arrows point to the antemolars, four of the latter in the Aberdeen specimen and five in the Novosibirsk specimen, and the grey arrows show the relative elongation of the rostrum. Both of these features are polymorphic within populations. Whenlatitudeandlongitudearecombinedasactualgeographical

distancebetweensamples,smallbutsignificantcorrelationshavebeenfoundwithdifferencesinskullsize(R2=0.03,P=0.00),skullshape(R2=0.01,P=0.02)andmolarshape(R2=0.19,P=0.00),butnotinmandibleshape(R2=0.00,P=0.51)(Polly,2007)(Fig.10.6).Thesegeographicpatternsareconsistentwiththehierarchicalpatternsofstructuring,becausemandibleshapeshowedthemoststructuringatthepopulationandspecieslevels,whichareroughlyrandomwithrespecttogeography,whereasskullsizeandmolarshapehadcomparativelystrongstructuringatthelevelofkaryotypicgroups,whicharearrangedinbroadgeographicpatterns.

Figure10.6Isolationbydistanceinskullcentroidsize(A),skullshape(B),

molarshape(C)andmandibleshape(D).ReproducedfromPolly(2007)withpermission.

Phenotypic Variation and Environment Environmentssortspeciesandpopulationsonthebasisoftheir

phenotypes,andenvironmentalselectioncausesspeciestoadapttotheirlocalconditions.makingitcommonforthegeographicdistributionofphenotypestobecorrelatedwithenvironmentalparameters(Pollyetal.,2011).SeveralstudieshaveshownthatS.araneusisnoexception.Correlationsbetweenmorphologyandenvironmenthavebeendocumentedatseveralspatialscales.Atsmallscales(withintherangeofmigrationofindividualshrews)thecorrelationbetweenenvironmentandmorphology(e.g.Wójciketal.,2007)islikelyduetonon-geneticplasticity,becausepopulationmixingfromindividualmovementswouldoverwhelmanyselectivedifferencesthatexistbetweenhabitats.Atlargerscalesthecorrelationbetweenenvironmentandphenotypemaybeduetoevolutionaryadaptationtodifferentenvironments,tochanceassociationbetweenenvironmentandgeneticdifferentiation,or,asatsmallspatialscales,tonon-geneticplasticresponsestodifferentenvironments.Noneofthestudieswereviewherehavespecificallycontrolledforthesedifferentpossibilities.

Thefirstscalewewillconsideristhelocalscale,measuredinmetresto

kilometres.Thisisthescaleatwhichlocalhabitatsmayvary,butmacroclimaticvariableslikeannualprecipitationormeanannualtemperaturedonot.StudiesofshrewsinBiałowieżaPrimevalForest,Poland,havefoundphenotypicdifferencesbetweenthreehabitattypes:drymeadows,floodplainforest(‘flatwoods’)andwetsedgebogs.Bothmandibleshape(Wójciketal.,2003)and

20

non-metricmeristictraits(Wójciketal.,2007)weresignificantlydifferentamongthesehabitats.Thephenotypicdifferenceswerestrongenoughthatdiscriminantfunctionanalysiswasabletocorrectlyassignshrewstooneofthesethreehabitats70.3percentofthetimebasedontheirmandibleshape.Someevidencesuggeststhattherearealsodifferencesinthefrequenciesofgeneticandchromosomalpolymorphismsbetweenshrewslivinginthesethreehabitats(Wójciketal.,1996),butitislikelythatboththegeneticandphenotypicdifferencesaretransientfluctuationsinlocalpopulationsthatarecontinuallydifferentiatingandeitherbecomingextinctorresorbedintothegenepoolofthelargermetapopulation(Wójciketal.,2003).

Thesecondscaleweconsiderisanintermediatescaleoftenstohundreds

ofkilometres.Atthisscaleregionalhabitatsvary,withsometimessharpdifferencesintopography(mountainsversusvalleys,hillsversusplains)andsmalldifferencesinmacroclimaticvariables.Severaldifferentchromosomalraces(orspecies)maybeinvolvedincomparisonsatthisscale,andgeneticdifferencesamongpopulationsaremoreprobablethanatthelocalscale.Hausser(1984)lookedattheenvironmentalandmandibularshapedifferencesinfivespeciesoftheS.araneusgroupinsouth-easternEurope:S.araneus,S.antinorii,S.samniticus,S.coronatusandS.granarius(atthetimeofhiswork,S.antinoriiwasconsideredconspecificwithS.araneus).Hefoundthatmorphometricdifferencesinmandibleshapewerenotcorrelatedwithgeneticdifferences(measuredasallozymedistances),suggestingthatsomethingotherthanphylogeneticdivergenceexplainedthephenotypicdifferences.Usingindividualshrewsratherthanspeciesmeans,acanonicalvariatesanalysisshowedthat26.3percentofthevarianceinmandiblemorphologywasexplainedbythecombinationofelevation,meanannualtemperature,annualtemperaturerange,annualprecipitationandannualprecipitationrange.TheseshrewsaredistributedfromnorthernSpainthroughthePyrenees,acrosssouthernFrance,throughthevalleysoftheAlps,alongtheItalianpeninsulaandintothenorthernBalkans–regionsthatincludeconsiderabledifferencesinalltheseclimaticvariables.Hausserconcludedthatregionalselection(ornon-geneticplasticresponse)influencedbothindividualvarianceandinterspecificvariance,thelattersoextensivelythatitobscuredthephylogeneticvariance.ThesamephenomenonmayoccurbetweenchromosomalraceswithinS.araneus.Mishta(2007)lookedatmorphometricvariationinthemandibleandskullof18populationsbelongingtoatleasttwochromosomalraces(KievandNeroosa)acrosssouthernBelarus,Ukraine,Moldova,Romaniaandsouth-westernRussia(seeChapter3).Shefoundastrongnorth-southgradientinphenotypes,withthepopulationsintheCrimeaandneartheBlackSeabeinghighlydifferentiatedfromthosefoundmoreinland.Seventy-onepercentofthemorphologicalvariancewasexplainedbyclimaticvariables.Intheseshrews,theintraspecificvariationisexpectedtobelessthaninHausser’sinterspecificstudy,butsoistheclimatevariation.Thus,climaticvariationatintermediatescalesappearstoexplainconsiderablewithin-speciesvariation.

Atthelargestscaleofhundredstothousandsofkilometres,thescaleof

theentiregeographicdistributionofS.araneus,therearephenomenaldifferencesinclimateandtopography.Siberianlocalities,forexample,canhave

21

meanannualtemperaturesbelow0°CandmeanJanuarytemperaturesof-20°C,whereaslocalitiesalongtheEnglishChannelmayhavemeanannualtemperaturesof10°CandmeanJanuarytemperaturesof5°C.Thecorrelationbetweensizeofindividualsandenvironmentatthisscaleisstrong;thecorrelationsbetweensizeandlatitude,elevationandtemperatureinourdatahavealreadybeendiscussedabove.However,thecorrelationbetweenphenotypicshapeandenvironmentatthisscaleisweak.Thecorrelationbetweenskullshape(PC1)andlatitudeisnotsignificant,butskullshapeandmeanJanuarytemperatureexplains28percentofthevariance(P=0.003),althoughannualprecipitationisnotsignificantlycorrelatedwithskullshape(P=0.82).Mandibleshapeisnotsignificantlycorrelatedwithanyofthesevariables.Thus,atacontinentalscalesizeappearstobecorrelatedwithenvironmentviabiologicalprocessesrelatedtophysiology,metabolismandwinternutritionalstress(discussedabove),butthedifferencesinshapeareunrelatedtoenvironment,morelikelyresultingfromphylogeographicpatterningrelatedtohistoryratherthanenvironmentalselectionorsorting.

Synthesis and Conclusion SeveralpatternsemergefromthestudyofphenotypictraitsinS.araneus

andrelatedspecies.Differentiationamonglocalpopulationsishigh,ashighasdifferentiationamongspecieswhenmeasuredasQSTvaluesforthebodysizeandcranialtraitsreviewedhere.Thisisnottosaythatdifferentiationamongpopulationsisasgreatasamongspeciesinabsolutemagnitude,butasaproportionofthewithin-groupvariationpopulationsareasdivergentasspecies.Significantstructuringofquantitativephenotypicvariationamongpopulationsisnotuniquetoshrews(e.g.marmotsPolly,2003;CaumulandPolly,2005)andthelargeQSTvaluesresultfromthecomparativelysmallrangeofvariationfoundwithinalocalpopulationcomparedwiththevariationfoundinachromosomalrace,subspeciesorspeciesacrossitsentirerange.Whileitisthecasethatphenotypesdifferamongpopulationsfoundindifferentlocalhabitats,thereisnoevidencethatthetraitswereviewedherearespecificallyadaptedtothosehabitats.Rather,itseemslikelythatthedifferencesamongpopulationsandlocalhabitatsrepresentrapidburstsofchangeassociatedwithdrift,pleiotropyorenvironmentalplasticityfacilitatedbytheoccasionaldropsinlocalpopulationsize,whichprobablynumberinthetenstohundreds(Churchfield,1990;Chapter2).Indeed,evidenceexistsformeasureablechangeinskeletalphenotypesinlocalmammalpopulations,includingshrews,onannualtodecadalscales(Wójciketal.,2006;Poroshinetal.,2010).

Differentiationamongchromosomalracesiscomparativelysmall

comparedwiththedifferencesamongtheirconstituentpopulations.Atfirstglancethispatternseemstosuggestthatkaryotypedifferencesareinsufficientbarrierstogeneflowtoallowphenotypicdifferencestoaccumulate.However,wehavereviewedseverallinesofevidencewhichsuggestthatthesmallphenotypicdifferencesthatdoexistbetweenracesaremaintainedbythesamekaryotypicincompatibilitiesthatmaintainchromosomalhybridzones.Indeed,

22

thelevelofdifferentiationacrosshybridzonescomparedwithgeneticdifferentiationsuggeststhatphenotypictraitsoftheskullandmandiblehaveundergonediversifyingselectioninsomeoftheopposingraces.Differentiationamongkaryotypicgroupsisrelativelylarge,especiallyinsizeandmolarshape.Theformerisrelatedtolatitudinalandaltitudinalgradientsthatbroadlycorrespondtothegeographicdistributionofthekaryotypicgroups.TheNorthEuropeankaryotypicgroup,forexample,predominantlyinhabitsScandinavia,whichisoneoftheprimarygeographicregionsassociatedwiththegreatestlatitudinalrangeofthecommonshrew.Molarshapeisthetraitexpectedtohavethegreatestheritabilityoftheonesstudiedandis,thus,theoneexpectedtohavethestrongestcorrelationwithphylogeneticdifferences(Polly,2001).Differentiationamongspeciesisproportionallygreaterinsometraits,especiallymandibleshape,butlesssoinothers,suchassize.ThehighestQSTvaluesamongspeciesareonlyaslargeasthelowestonesamonglocalpopulations.

Ifevenasmallproportionofthephenotypicstructuringamong

populationsisgenetic,thenthephenotypesofcommonshrewshavethecapacitytoevolveveryrapidly.Whythenaredifferencesbetweenchromosomalracesandspeciessosmall?Onereasonthedifferencesbetweenracesaresmallmaybethattheyformedrelativelyrecently,perhapsonlyinthefewthousandyearsfollowingthebeginningoftheHolocene.However,thepotentialforphenotypicchangemeasuredinlocalpopulationssuggeststhatdifferencescanevolveveryrapidly,evenenoughtodifferentiateracesovertimeperiodsasshortas10000years(seealsoChapter13forargumentsagainstsuchascenario).

Theevidencereviewedabovesuggeststhatenvironmentaladaptation(or

plasticity)mayoverridegeneticdifferentiationonthescaleoftenstohundredsofkilometres,whichisthescalerelevanttoparapatricracesandhybridzonesbetweenthem.Incaseswhereparapatricracesarephylogeneticallycloselyrelated,thesmalldifferencesintheirmeanmorphologicalshapemaybeswampedbytherelativelylargedifferencesinlocalenvironmentsacrosslandscapesatthatscale(mountainversusvalley,coastversusinland).Giventhatlocalpopulationshaverapidphenotypicevolution,thepossibilityexiststhatparallelenvironmentalselectionacrosssmalllocalpopulationshasagreatereffectonphenotypesthandoestheslowerchangeinmeanphenotypebetweenchromosomalraces.Asjustmentioned,however,littleevidenceexiststhattheskullandmandibletraitsthathavebeenstudiedarespecificallyadaptedtolocalenvironments,exceptinthecaseoftheirsize,whichislinkedtoenvironmentthroughprocessesrelatedtooverallbodymass.

Anotherlikelyexplanationforhighlevelsofinterpopulation

differentiationbutlowlevelsofinterracialdifferentiationismetapopulationdynamics(Hanski,1999).Becauseoftheirsmallsize,microhabitatspecialisations,comparativelysmallhomerangesandcomparativelyshortindividualdispersaldistances,shrewsfrequentlyformverysmalllocalgeneticpopulationswithrapidphenotypicresponsestodriftandselection(HanskiandKaikusalo,1989;PeltonenandHanski,1991).Theselocalpopulationsaretransientintheirisolation,however;theirdifferentiationcanbelostbyimmigrationandemigration,orbyextinction,whichisacommonoutcomefor

23

suchsmall,localisedpopulations(PeltonenandHanski,1991).Theoveralleffectislikeslowlyboilingwater,withbubblesoflocaldifferentiationarisingfrequentlybutwithoutsubstantiallychangingtheaveragephenotypeinthelargermetapopulation.Thismodelfitsthedatawehavereviewedhereverywellinthatitexplainsthehighdifferentiationamonglocalpopulations,therapidchangeinphenotypesovertime,theadaptationtoenvironmentonaregionalbutnotlocalorcontinentalscales,andthecomparativelysmalldifferentiationamongracesorspecies.

Thehighlevelofdifferentiationamonglocalpopulationsmeansthatthe

denominatorislargeintheQSTratioforchromosomalraces;thedifferencebetweenraces(whicharethemetapopulationsinthisscenario)issmallcomparedwiththevariationamonglocalpopulations.Movingupthehierarchicalscale,thelowdifferentiationamongchromosomalracesmeansthatthedenominatorofQSTamongkaryotypicgroupsissmall,allowingthedifferencesbetweentheselargerphylogroupstoresultinhighQSTvalues.Inotherwords,aswemoveupthehierarchicalscaleawayfromlocalpopulations,thetransientvariationtheregiveswaytostructuringthatismorepredictableintermsofphylogeny,geographyandbarrierstogeneflow.

Perhapsthemostimportantconclusiontobereachedfromtheevidence

wehavereviewedisthatthepotentialforrapidphenotypicevolutioninS.araneusistremendousbecauseoftheirdivisionintolocalpopulations.Thepotentialforselectionordrifttocausephenotypicchangesissubstantialbecauseoftheverysmalllocalpopulationsizesandtheirabilitytopersistinlocalisedmicrohabitats.Intypicalcontinentalsituations,thispotentialgoesunrealisedbecauseofmetapopulationdynamicsthatresorbthedifferentiationthroughmigrationoreraseitthroughextinction,butincircumstanceswherethelocalpopulationpersistsinisolation,evolutioncouldbequiterapid.Incaseslikeislandpopulations,thispotentialisrealisedasdemonstratedbythesignificantdifferencesinthephenotypesofpopulationsinhabitingScottishislands(Polly,2005;WhiteandSearle,2006,2007).Indeed,thepotentialissogreatthatevenphenotypiccovariancestructurehasevolvedintheseScottishislandpopulationsoverrelativelyshortperiodsoftime(Polly,2005).Whilethepotentialforphenotypicevolutionmaynotberealisedinordinarycircumstances,thereisapossibilityforitduringperiodsofenvironmentallocalisation,suchasduringglacialadvanceswhensmallpopulationscouldfeasiblyhavebeenisolatedinsmallpocketsofrefugialhabitat(Chapter13).Thecuriousmosaicofphenotypicdifferentiation,suchasthepatternofmandibleshapeshowninFig.10.2h,acrosstherangeofS.araneusmayresultfromsuchahistoryofisolationinmanysmallrefugia,asmightthepatchworkofspeciesmorphologiesintheS.araneusgroupacrossEurope.

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