Genotypic covariance between the performance of a …...species and the properties of the community covary genetically (Johnson, Vellend, & Stinchcombe, 2009). The genetic covariance

Functional Ecology 20171ndash12 wileyonlinelibrarycomjournalfec emsp|emsp1copy 2017 The Authors Functional Ecology copy 2017 British Ecological Society

Received10November2016emsp |emsp Accepted13September2017DOI1011111365-243513005

R E S E A R C H A R T I C L E

Genotypic covariance between the performance of a resident species and community assembly in the field

Arthur M Riedel1 emsp|emspKeyne Monro2emsp|emspMark W Blows1emsp|emspDustin J Marshall2

1SchoolofBiologicalSciencesUniversityofQueenslandBrisbaneQueenslandAustralia2SchoolofBiologicalSciencesMonashUniversityClaytonVictoriaAustralia

CorrespondenceArthurRiedelEmailarthur_riedelmaccom

Funding informationUniversityofQueenslandResearchScholarshipUQInternationalResearchTuitionAwardAustralianResearchCouncil

HandlingEditorCharlesFox

Abstract1 Geneticvariationinresidentspeciescaninfluencetheassemblyanddynamicsofcommunitiesbutthepotentialforthesegeneticeffectstopersistacrossgenera-tionsislargelyunresolvedInprinciplepersistentdirectionalchangesincommuni-ties are only predictedwhen community properties covary geneticallywith thefitnessofresidentspecies

2 Estimatesofgeneticcovariancebetweenthefitnessofaresidentspeciesanditscommunityarethereforenecessarytoldquoclosetheeco-evolutionarylooprdquoinstudiesofcommunitygeneticsbutsuchestimatesarerareEmulatingcommunitygeneticsexperimentsinplantsweusedclonalreplicatesof21genotypesofaresidentspe-cies(theencrustingbryozoanHippopodina)toinvestigatethemagnitudeofgeno-typicvariancecontributingtoassemblyofamarinebenthiccommunity

3 Genotypesexplainedupto35ofvariationincommunityassemblyCriticallytheperformanceofHippopodinagenotypescovariedbothwiththeevennessofcom-munitiesandwiththeabundancesofsomeindividualspeciesrepresentinganindi-rect genetic effect that creates the potential for multigenerational interactionsbetweenHippopodina andco-existing speciesOur results suggest thatdifferentgenotypeswill associatewithdifferent communitymembers consistently acrossgenerations and such non-random associations can give rise to specializationFurther interactions between species other thanHippopodina itselfmay also be alteredbyeffectsofgeneticvariationinthefocalspecies

4 FurthermorespeciesinthecommunityotherthanHippopodinaitselfwillinteractmorecommonlyinthepresenceofsomegenotypesoverothers

5 Ourresultssupportthepotentialforgeneticvariationinonespeciestohavedeter-ministiceffectsonthedynamicsofecologicalcommunities

K E Y W O R D S

communityecosystemgeneticsdirectndashindirectgeneticcovarianceeco-evolutionaryfeedbacksgeneticvariationindirectgeneticeffectsinterspecificinteractionsmarineinvertebratesRobertsonndashPriceIdentity

1emsp |emspINTRODUCTION

Therolethatgeneticvariationinoneresidentspeciesplaysinshap-ing the properties of associated communities often referred to as

communityorecosystemgenetics (HaloinampStrauss2008JohnsonampStinchcombe2007Whithametal2006)isakeyissueatthein-terfaceofecologyandevolutionarybiologyThere is increasingevi-dencethatcommunityassemblyinarangeofsystemsisinfluencedby

2emsp |emsp emspenspFunctional Ecology RIEDEL Et aL

geneticvariationbutthepotentialfortheseeffectstopersistremainsunclear An elegant study by Agrawal Hastings Johnson Maronand Salminen (2012) provided the first evidence for real-time eco-evolutionaryfeedbacksbetweenaresidentspeciesanditscommunityunderfieldconditions(Agrawaletal2012)butsuchdemonstrationsareexceedinglyrareandmaynotbeaccessibleinmanysystemsAssuchidentifyingdirectandenduringlinksbetweencommunityassem-blyandgeneticvariationwithinpopulationsmorebroadlyremainsanongoingchallenge

Thecentralobservationunderlyingecosystemgeneticsisthatthegenotypeofaresidentspeciescanaffectothermembersoftheassoci-atedcommunityInthisregardecosystemgeneticshasparalleledthe-oryaddressingindirectgeneticeffectsIndirectgeneticeffects(IGEs)aregeneratedwhenheritablevariationamongindividualsofonespe-ciesinfluencestraitexpressioninotherindividuals(MooreBrodieampWolf1997seeFigureS1)Indirectgeneticeffectsinthecontextofasinglespeciesarewellestablished(PetfieldChenowethRundleampBlows2005WolfBrodieCheverudMooreampWade1998WolfMuticampKover2011)Theyoccurwhengeneticvariationamongin-dividuals modifies the environment for other unrelated individualsleadingtoindirectgeneticvariationinphenotypefitnessamongtheselatterindividuals(Wolf2003)Inacommunitycontexttheeffectofheritabletraitvariationinaresidentspeciesoncommunitypropertiesistermedaninterspecificindirectgeneticeffect(IIGE)(Genungetal2011)OftenIIGEsarereportedasestimatesofcommunityheritabil-ityorhowmuchofthevariation inacommunityproperty isduetogeneticvariationamongindividualsofaresidentspeciesForexampleIIGEshavebeencommonlyreportedinplantsandincludetheeffectofhost-plantgenotypeontheassemblyofitsarthropodcommunityandinfluencesonabove-groundandbelow-groundinteractions(DungeyPotts Whitham amp Li 2000 Genung Bailey amp Schweitzer 2011Johnson amp Agrawal 2005 Rowntree Cameron amp Preziosi 2011Whithametal2006)

Thepatternandmagnitudeofthegeneticbasistomulti-traitvari-ationinapopulationissummarizedinGamatrixwhosediagonalele-mentsaretheadditivegeneticvariances(orinthisinstancegenotypicvariances)oftraitsandwhoseoff-diagonalelementsarethegenetic(orbroad-sensegenotypic)covariancesofthesetraitsthusG1isthegeneticvarianceintrait1andG12isthegeneticcovariancebetweentraits1and2

The value ofmodellingG bringing insights from evolutionaryprocessestobearonecologicaldynamicsliesintheabilitytopre-dictchangeincommunityproperties(RidenhourampNuismer2014)however our methods differ in that instead of evaluatingG and its corresponding selection gradient to estimate changewe hereevaluatethecovarianceoffitness-associatedtraitswithcommunitypropertiesasdescribedbelow In thecontextof IIGEsGenables

examination not only of the indirect effects of a resident speciesonindividualtaxabutalsooffurtheralterationtotherelationshipsamongthosetaxainthecommunityNotwithstandinglimitationstothestabilityofGwhichcanchangeovermultiplegenerationsduetoselectionordrift(McGuiganChenowethampBlows2005)mostcomparative studies find thatG matrices estimated from experi-mental andnatural populations are predominantly stable geomet-rically (ArnoldBuumlrgerHohenloheAjieampJones2008)GiventhereasonableassumptionofstabilityGmatricescanbereliablyusedtoestimate thatpartofecological interactionamongspecies thatderivesfromgeneticvariation

WhiletheexistenceofIIGEsofaresidentspeciesonitsassociatedcommunitysuggeststhatcommunitypropertiesmayrespondtoevo-lutionarychangesintheresidentspeciesitdoesnotinevitablyfollowthatthegeneticvariationinthespeciesdrivingtheIIGEisassociatedwith fitnessThisdistinction iscriticalbecauseonly thatpartof thegeneticvariation intheresidentspeciesthatcovarieswithfitness ispredictedtocausemultigenerationalchangesinthecommunityprop-ertiesinfluencedbythatspeciesMoreformallytheresponsetose-lectiononanytrait (includingthetraitsofresidentspeciesthatmayinfluence community properties) is predicted by that traitrsquos geneticcovariancewithfitness(Robertson1966)

where∆zisthechangeintraitvaluefromonegenerationtothenextand ωisfitnessAppliedtocommunitygenetics∆zisthechangeinthecommunitypropertyfromonegenerationtothenextandωisthefitnessoftheresidentspeciesAnIIGEonacommunityisthere-forepredictedtohavepersistentanddirectionalconsequencesforthatcommunityonlywhenthefitnessofindividualsintheresidentspecies and the properties of the community covary genetically(JohnsonVellend amp Stinchcombe 2009) The genetic covariancebetweenthefitnessof individuals inaresidentspeciesanditsas-sociatedcommunityshouldpredictthereforewhetheranyeffectsofthatspeciesonitscommunitywillpersistacrossgenerationsInthe absence of this genetic covariance (sometimes referred to asdirectndashindirectcovarianceinquantitativegenetics)thereisnopo-tentialforgeneticeffectsinonespeciestoinfluencethetrajectoryofcommunityassemblyorforeco-evolutionaryfeedbacksbetweenthespeciesanditssurroundingcommunity(HaloinampStrauss2008)Withoutthispotentialtheindirectgeneticeffectsgeneratedamonggenotypesofaresidentspeciesonassociatedcommunitiesshouldvarystochastically fromgenerationtogenerationascertaingeno-typesbecomemoreorlesscommonEachgenerationwillinfluenceassemblyanewbut there isnopotential fordeterministicgeneticeffectstobetransmittedfromonegenerationtothenextAppliedtoIIGEsthisistheequivalentofgeneticdrift(Vellend2010)inthatvariation in abundancesofother species in the communitywouldsubsistthroughgenerationswithoutbeinginfluencedbytheevolu-tionoffitnessintheresidentspecies

Despitemounting evidence for IIGEs studies that link them tofitness remain rareHereunder fieldconditionsweexplore the re-lationship between community properties and heritablevariation in

(1)G =

⎡⎢⎢⎢⎢⎢⎢⎣

G1 G12 G13 hellip G1n

G2 G23 hellip G2n

G3 hellip G3n

hellip

Gn

⎤⎥⎥⎥⎥⎥⎥⎦

(2)Δz = covG(zω)

emspensp emsp | emsp3Functional EcologyRIEDEL Et aL

thefitness-relatedtraitsofaresidentspeciestheencrustingbryozoanHippopodina iririkiensisCommunitypropertieswerequantifiedintwoways (1)commonmetricsofcommunityspeciesdiversity (diversityevennessandcoverage) and (2) thespeciescompositionandabun-danceswithin the communitiesWe estimate a derivation of theG matrix thedirectndashindirect covariancematrixwhich summarizes theindirecteffectsofgenotypeoncommunitypropertiesthecovariancesamongtheseindirecteffectswhichamounttoalteredspeciesinterac-tionsthedirectgeneticeffectsofgenotypeonperformanceCriticallywefurtherestimatethegeneticcovariancebetweentheperformance(fecundityandsize)ofHippopodinawithitsindirecteffectoncommu-nitiesassemblinginthefieldOurexaminationofthecovariationbe-tween fitness-related traits inour resident speciesHippopodina and the genotypic effects on community assembly enables us to deter-minethepotentialofIIGEstoinfluencepersistentdirectionalchangeincommunities

2emsp |emspMATERIALS AND METHODS

21emsp|emspStudy system and resident species

Epifaunalmarinecommunitiesoccurworldwideandarecomposedlargely of filter-feeding specieswithin the same trophic level TheassemblyofsuchcommunitiesisinfluencedbyfactorsthatactbothbeforeandaftersettlementPre-settlementeffects includethedi-rectpredationofimmigrantlarvae(NydamampStachowicz2007)andallelopathicchemicalinteractionsbetweenresidentsandimmigrants(JacksonampBuss1975KohampSweatman2000ThackerBecerroLumbang amp Paul 1998) Post-settlement residents may limitthe growth of neighbours or overgrow thementirely (Buss 1979OsmanampWhitlatch1995Russ1982)Larger individualsarebet-terspatialcompetitors(Buss1979)butinteractivenetworksratherthanhierarchiesmayexistwherebynosinglespeciesdominatesallothers(BussampJackson1979)Inthesesystemsmoreoverspeciesdistributions and abundances are also influenced by non-contactcompetition foroxygen (FergusonWhiteampMarshall2013) food(SvenssonampMarshall2015)aswellas thesizesof feedingstruc-turesinneighbours(DavisampMarshall2014)Somespeciescanhavelastingimpactsbyalteringtheirenvironmentprofoundlywhileoth-erscansimplychangetheavailabilityofresourcesforothers(JonesLawtonampShachak1994)Variationintheidentityofresidentspe-cies isknowntogeneratevariation incommunityassemblywithin(Sutherland 1978) and among (Estes amp Palmisano 1974) trophiclevels Incontrast theroleofvariationwithina residentspecies ispoorlyunderstood

AsresidentspeciesweusedtheencrustingbryozoanHippopodina iririkiensis(Tilbrook1999hereafterreferredtobygenus)Hippopodina growsbytherepeatedbuddingofmodularsubunitsorzooidsofiden-ticalgenotypeSexuallyproducedoffspringeachofthemgeneticallyunique are brooded in specialized zooidswith conspicuous brood-chambers(knownasovicells)priortoreleaseaslarvaeLarvaeswimbriefly(minutestohours)intheplanktonbeforepermanentlyattach-ing to a substrate andmetamorphosing into settlers that formnew

colonies (Eitan1972)Colony size ismajor componentof fitness inHippopodina (as it is inmany colonial organisms JacksonampCoates1986)becauselargerfaster-growingcoloniescanoutperformsmallerslower-growingcompetitorsandcriticallyhavehigherfecunditydueto the positive association of colony size with number of ovicellswhichdevelopwithina fewweeksOvicellnumber is therefore anappropriateassayoffecundityEachcolonyderivedfromasingleset-tlerisauniquegenotypethatcanbereplicatedclonallyviafragmen-tationandtheabilitytofollowclonalreplicates inthefieldthroughtime permits the traits and communities associated with residentgenotypestobeassayedsimultaneouslyindifferentenvironmentsorexperimentaltreatmentsThisuseoffragmentationhasbeenusedre-peatedlyforclonalplants(NyquistampBaker1991)seaweeds(MonroampPoore2009)andcolonialmarineinvertebrates(MonroampMarshall2013YundMarcumampStewart-Savage1997) likeHippopodina toestimatethebroad-senseheritabilitiesofmeasuredtraits(FalconerampMackay1996)

Hippopodinacolonizesavailablespaceearlyinthesummerseasonwhenbenthiccommunitieswhere it is foundshowincreasedsettle-ment and growth It is a regular and persistent species and conse-quentlyco-existswithallsessilespeciesfoundinthissystemwithoutoftendominating itMoreoverthe longevityandgenerationtimeofHippopodina (weeks) isequivalent to thatofmostco-occurringspe-ciessuchthatIIGEsofHippopodinacanpotentiallyinfluencecurrentandnewgenerationsofcommunitymembers(HairstonEllnerGeberYoshidaampFox2005)ImportantlywehavepreviouslyshownthatthepresenceofHippopodinainfluencescommunityassemblyatourstudysite(RiedelMonroBlowsampMarshall2014)

22emsp|emspCollection and cultivation of resident genotypes

Roughened A4 acetate sheets were fastened to ten PVC backingpanels (250times450times4mm)andsuspended facedownc 1 m below thewatersurfaceatManlyBoatHarborQueensland(SeeFigureS2)Panelswerespacedwidelyamongpontoonstominimizerelatednessamong recruits After 13days of natural recruitment resident set-tlersofHippopodinaweresampled fromdistantpanelsandbroughttothelaboratoryTheretheyweregentlystampedoutwithasmall(8mm)hole-punchretainingthemonacircularfragmentofacetateSettlerswerethengluedtonewacetatesheetsreturnedtothefieldandattached tobackingpanels (590times590times4mm) thencultivatedtomaturityassinglecolonieswithinacommongardensetting(withinmetres of each other) These colonies cultivated from settlementwere our resident genotypes Each was genetically distinct and atmostsharedparentswithothersinthesamplethoughoursamplingstrategyminimizedthispossibilityWedeallaterinthedataanalysisstagewiththepotentialforpersistentenvironmentaleffectsaffectinglatergrowthstagesthatacommongardensettingmayhavecreatedGrowingcoloniesweremaintainedweeklyremovingsurroundingor-ganisms anddebris thatmight interferewith lateral growthAt theendofthiscultivationphasewhencolonieshadgrowntoc 100 mm diameter(overc14weeks)theywerereturnedtothelaboratoryforuseintheexperimentproper


23emsp|emspExperimental design and deployment

The experiment was a nested block design using separate equip-ment to the cultivation phase just described Four clonal replicatesfromeachof21residentgenotypesweredistributedacrosstwopan-els(experimentalblocks)Thuspanelswerenestedwithingenotype(allowinggenotypicvariationtobepartitionedfromspatialvariationamongpanels)andtwoclonalreplicatesperpanelformedthebasisfor estimating residual variation (21 genotypestimes2 panelstimes2 repli-cates) Clonal replicateswere obtained by cutting fragments of ap-proximately equal size (c 100 mm2) from each colony and gluingeachreplicateviaitsacetatebasealoneontoarigidPVCsettlementplate(110times110times4mm)Plateswerereturnedtothefieldsitewithin48hrwheretheywereagainattachedtoPVCbackingpanelsPanelsweresuspendedunderwateraspreviouslyinrandomorderalongonesideofasinglepontoonTheexperimentlasted8weeksduringwhichcommunitieswerepermittedtoassemblefreely

24emsp|emspData collection

Initial fragment size was recorded from digital photographs takenat the start of the experiment and final colony size was recordedfrom another set of photographs taken at its conclusion 8weekslater For each clonal replicate two components of fitness wereevaluated final colony size and the density of brood chambers intwo 100mm2 subsamples of each final colony (a relative measureof fecundity independentof total colony size) Inmarinebiofoulingcommunitieslargercoloniescanhaveasubstantialadvantageincom-petitiveinteractions(Buss1979)Theinitialsizeofclonalreplicates(9959mm2 SD=3717) did not differ systematically among geno-types (ANOVA F2060=151 p=11) Nevertheless to control forslightdifferencesininitialsizeinoursubsequentestimatesofcolonygrowthor available space final colony sizewas regressedon initialfragmentsizeandtheresidualsretainedasestimatesofgrowth(Finalmm2=1063153+(17497timesinitial mm2) R2=0548 F179=956plt001)similarlythemeandensitiesofovicellswereregressedoninitialsize(inmm2)andtheresidualsretainedtoestimatefecundity(Fecundity=1237+(0037timesinitial mm2) R2=0047 F179=3935p=05)

Usingadissectingmicroscopeanddigital imageanalysisofthefinalphotographstheabundancesandsizesofcommunitymemberson each platewere also recordedWe composed twodatasets of (1)communitymetricscommonlyusedinecologyand(2)theabun-dancesof individual speciesFororganisms thatdidnotvary sub-stantiallyinsize(egpolychaetewormsandsponges)weestimatedabundanceasnumericalcountsThepolychaetesHydroides diram-phus and Janua pagenstecheriwereextremelyabundantandcountswereestimatedfromthemeanofthreesubsamplesof100mm2WedidcountsacrosswholesettlementplatesforBalanus balanoides(acommonbarnacle)Bugula stolonifera(anerectbranchingbryozoan)anderectnon-encrustingspongesofthegenusSycon(forwhichweareunabletoobtaingreatertaxonomicresolution) Inthesecasescounting individualswasmostefficientandpilotstudies indicated

that counts and coverage were highly correlated (Table S1) Forencrusting bryozoans (Watersipora subtorquata Celleporaria spSchizoporellaspanunidentifiedencrustingbryozoanandconspe-cific Hippopodina)andthesolitaryascidianMicrocosmus squamiger (allreferredtobygenushereafter)sizevariationwasconsiderableandwe therefore estimated abundance as the cumulative area ofcoverontheplate

Toassaythecommunityoneachplateincomparableunitswees-timated thedensityofeach speciesbydividingallmeasuresby thearea unoccupied by the resident colonyWeexcluded the densitiesof Janua and Hydroidesfromthisstandardizationgiventhesecountswerealreadyindependentofanydirecteffectofresidentcolonysizehavingalreadybeenestimatedonspacefreeoftheresidentspeciescolony

25emsp|emspCommunity metrics

Three standard communitymetricswere calculated from the abun-danceofeachspeciesexcludingmeasuresoftheresidentgenotypeof HippopodinacommunitycoverageShannonndashWienerdiversity(Hʹ)anditsderivativePieloursquosEvenness(Jʹ)Inordertousedataofsimi-larunitsweconvertedallcountdatatoestimatesofcoverageusingregressionsofareaoncountsfortherelevantspecies(TableS1)Hʹwascalculatedas

whereSisthenumberofspeciesNisthecoverageofthewholecom-munityoneachsettlementplateandpiistherelativedensityofspe-cies i(calculatedasthecoverageofagivenspeciesonspacefreeoftheresidentgenotypecolonyniNPieloursquosEvenness(Jʹ)wascalcu-latedasHʹHmaxwhereHmax=ln(S)

26emsp|emspCommunity composition

Wecombinedtheencrustingbryozoansintoasinglegroupforanaly-sis based on their functional andmorphological similarity and thefactthatourstatisticalmodel(seebelow)wouldnotconvergewhenthe five specieswereanalysed separately (most likelydue toa lowlevelofvariation in theabundancesofat leastoneof them)Some25ofsettlementplatesattractednewrecruitsofourresidentspe-ciesHippopodinabutwecouldeasilydistinguishbetweenthesenew(verysmall)settlersandourfocalclonalfragmentsThefinaldatasetcomprisedcountsandcoverageofseventaxaincludingthesummedcoverageofencrustingbryozoansbutexcludingassayoftheresidentgenotype

27emsp|emspData analysis

Asthevariables(growthandfecundityofresidentHippopodinageno-typespluscountsandsurface-areameasuresforassociatedcommu-nities)wereofdifferentunitsandscaleswestandardizedalldataformultivariateanalysisForeachvariabledatawerecentredonzeroby

(3)H=minus

Ssum

i=1

(pi In (pi))


subtractingtheirmeanandthenscaledtoavarianceofonebydivid-ingthembytheirstandarddeviation(QuinnampKeough2001)

TovisualizethecommunitiesassociatedwithdifferentgenotypeswecomputedaBray-Curtisdissimilaritymatrixfromthecommunitycomposition data and derived an ordination plot using non-metricdimensionalscaling(NMDSFigure1)Toanalysethesepatternswethenfittedamultivariate(multi-response)modelinSAS92treatinggenotypeandpanelasrandomeffects

whereX and Zarethematricesoffixedandrandomeffectsrespec-tivelythejthplate(replicate)isnestedwithinthekthpanel(block)andreplicatepanelsarenestedwithingenotype(g)Ateachoftheselevels of plate panel and genotype we estimated trait variationand covariation using restricted maximum likelihood with an un-structuredcovariancematrixtreatingvariationamongplateswithinpanelsas residuals Ina first applicationof themodelwe treatedthreecommunitymetricsandtwomeasuresofperformanceinourresident speciesas the responsevariables the secondapplicationofthemodelreplacedthethreecommunitymetricswiththeabun-dancesofseventaxaOurprimaryinterestlayinthecomponentsofvarianceandcovarianceatthelevelofgenotype(G)astheserepre-sentthedirectgeneticeffectsonperformanceinHippopodinatheindirecteffectsonspeciesinthecommunityandthedirectndashindirectcovariance of performance in the resident species on communityassemblyThesignificanceofeachcomponentofGwastestedusingalog-likelihoodratiotestbycomparingthefullmodeltoareducedmodelinwhichthecomponentofinterestwasheldatzeroasanullhypothesis (Littell Milliken Stroup Wolfinger amp Schabenberger2006) Tests had one degree of freedom andwere one-tailed forvariancesandtwo-tailedforcovariances

We developed the two models (one for the interaction ofHippopodinawithcommunitymetricsandoneforitsinteractionwithsevenindividualtaxa)takingamultivariateapproachtocharacterize

thegeneticdirectndashindirectcovariancebetweenHippopodinarsquosper-formanceandcommunitycompositionAlthoughtestingforgeneticcovariancesbetweencommunity traits and fitnesscomponentsoftheresidentspeciesisreadilyaccomplishedusingtheoriginalmod-els there isnoreasontoexpectthateachspecieswill respondtogeneticvariationinHippopodinaindependentlyfromtheothersandsothegeneticvarianceintraitcombinationsisoftenmoreinforma-tivethanthebivariategeneticcovariancesofmultipletraits(Blows2007Walsh amp Blows 2009)We used factor analytic modelling(Hineamp Blows 2006) to establish the effective dimensionality ofthe variancendashcovariancematrix estimated at the broad-sense ge-neticlevel(G)ineachmodelaboveStartingwithamodelinwhichG was assumed to be full rank (ie have as many dimensions astraits)weusedlog-likelihoodteststocomparenestedmodelsinastepwisemodelreductionstrategyTheeffectivedimensionalityofGwasidentifiedasthenumberofdimensionstowhichitcouldbereducedwithoutsignificantlossofmodelfitWethenextractedtheappropriatereduced-rankmatrixfromourmodeloutputandvieweditsstatisticallysupporteddimensionsasprincipalcomponents(PCs)EachPChadaneigenvaluedescribingtheamountofvariationinG thatitexplainedplusaloadingdescribingthestrengthofitsasso-ciationwitheachtraitWeascribedsaliencetoloadings(TableS3)comprising at least 50of the largestvalue for eachPC (Jolliffe2002) Using this approach we could characterize the multi-trait relationshipsunderlyingthemajorityofgeneticeffectsoncommu-nitystructuregeneratedbyHippopodina

3emsp |emspRESULTS

As evident in the NMDS (Figure1) variation among communitiesexceededvariationwithincommunitiestheoverallspreadofNMDSscores in each dimension was greater than that among communi-ties identified by individual genotypes Therefore the communities

(4)yijk==Xjkb+Zjk(g)jk(g)+Zj(k)j(k)+ijk

F IGURE 1emspOrdinationplot(NMDS)representingthedissimilaritiesofcommunitiesassociatedwithclonalreplicatesoftheresidentspeciesHippopodinaThecentroidforthecommunityassociatedwitheachgenotypeisshownasalargerfilledcirclewithreplicatecommunitiesofindividualgenotypes(plates)markedasemptycirclesColoursforgenotypesarearbitraryasareletterssolelytoaidgraphicdifferentiation


associatedwithclonalreplicatesofthesamegenotypewereonaver-agemoresimilar toeachotherthantothecommunitiesassociatedwithothergenotypes

Oftheareaavailableonsettlementplates(12100mm2)themeancoveragebyresidentgenotypeswas23whereasmeancommunitycoverage was 17 (Figure2a) Therefore resident genotypes typi-callyoccupiedmoreavailablespacethanthecommunitiestheywereassociatedwithhowevernonewereassociatedwithanabsenceofcommunity assembly Resident genotypes grew to c 30 times theiroriginal size over the 8weeks that communities had to assemblemeanovicelldensitywashighbutvariable(mean496per100mm2SD638)(Figure2b)Communitycompositionwasdominatedbyen-crustingbryozoansoccupyingamean12ofsettlementplatesJanua and Hydroideswere themost numerically abundant groupwhereasBugula Sycon and Balanuswereleastabundant(Figure3)


Estimatesofindirectgeneticvarianceformostcommunitymetricsaswellasforthedirectgeneticeffectsofgrowthandfecundityweresignificant (Table1) Indeed variation among genotypes explained35ofthevariationingrowthand45ofthevariationinfecunditywitha (non-significant) covarianceof018Therewassignificantlypositive genetic covariance between indirect genetic effects oncommunitycoverageandtheestimateofdiversitymeaningthatthelargercommunitiesgeneratedbysomegenotypeswerealsomoredi-verseWefounddiversitytohavesimilarlypositivecovariancewithevennessCriticallythesignificantlypositivegeneticcovariancebe-tweendirecteffectsongrowthof residentgenotypesand indirecteffectsonevennesswereuncovered thoughnotbetweengrowthanddiversity

F IGURE 2emspMeanvalues(plusmnSE) for (a)finalresidentcolonysizeandestimatedcoverage(mm2)byassembledcommunities(b)growthfactorofresidentcoloniesandnumberofovicells(c)communitymetricsamongresidentgenotypesofHippopodina (ShannonndashWienerDiversity(Hʹ)PieloursquosEvenness(Jʹ)

F IGURE 3emspMeandensities(plusmnSE) for speciescompositionincommunitiesassociatedwithresidentgenotypesofHippopodina(per100mm2)twospeciesgroupsbysurfacearea(indarkerbox)fivebyabundances


Genotypeexplainedconsiderableproportions(14ndash27)ofthevariationincommunitymetricsandasmuchas45ofthetotalvari-ationinperformancetraitsoftheresidentspeciesHippopodinaFactoranalyticmodelling ofG for these five traits supported a reductionfromfivedimensionstoonedimension(movingfromonedimensiontononeχ2

5=11089plt05)implyingthatmultipletraitssharedge-

neticrelationshipsthatmaybeoverlookedbysimply inspectingtheindividualelementsofGinTable1AsGisone-dimensionalhereallsuchrelationshipscanbesummarizedinasinglePC(Table2)(factorloadingsallapproximatingtoonearedetailedinTableS3)CommunitymetricsandfitnesscomponentsallloadedstronglyandpositivelyonthisPCindicatingthatlargergenotypesweremorefecundandalsogenerateddensermorediverseandmoreevencommunities

That Hippopodina genotypes were initially cultivated in one en-vironment only raises the possibility that variation among genotypesduringourexperimentmayhavederivedfromresponsetodiscretemi-croenvironmentson individuals Inpartwedealtwiththisbyreducingmicroenvironmental variationweminimized interactionswith residentgenotypesbyremovinganyothersettlersatleastonceweeklyTodeter-minethepossible influenceof thisearlyenvironmentalvariation inflat-ingvariationamonggenotypesduringourexperimentweexaminedtheamong-replicatevariancesforthetwofitnesscomponentsofourresidentgenotypesatthelevelofourblockingfactor(iepanels)Thesevariancecomponentsrepresentmicroenvironmentalvariationinthecultivationen-vironmentwhichshouldbecomparabletomicroenvironmentalvariation

thatactedduringtheassemblyexperimentWefoundthepercentageofthetotalvariationcontainedinthismicroenvironmentalcomponentwas0forgrowthand15forfecunditycomparedtothec37forgrowthand45forfecundityexplainedbygenotypicvariationsuggestingthatitwasnotthepredominantsourceofvariationamonggenotypes


Considerable variation in community composition occurred amonggenotypes compared towithin genotypes (Figure1)We found sig-nificantgeneticvariancesfortheassemblyoffouroftheseventaxaIntheresidentspeciesgrowthandfecundityalsodisplayedsignificantlevelsofgenotypicvariation(Table3)variationamonggenotypesac-countedfor38ofthevariationingrowthwhereasvariationamongpanelsaccountedfornoneSimilarly56ofthevariationinfecunditywasexplainedbygenotypewhereasonly18wasexplainedbyspa-tialvariationamongpanelsWithregardtoindirectgenotypiceffectson community composition the abundances of encrusting bryozo-ansshowedapositivegeneticassociationwiththatof theascidianMicrocosmusThedirectgeneticeffectsofperformance (intermsofgrowth) showedanegativecorrelationwith the indirectgeneticef-fectsonabundancesofSycon and BalanusInotherwordscommuni-tiesassociatedwithfaster-growinggenotypeshadfewerspongesandbarnacles

Variationamonggenotypesaccounted forup to42ofvaria-tioninspeciesabundancesamongallcommunitiesFactoranalyticmodellingofG in this case indicated that threedimensions (of apossible nine) were sufficient to account for all genetic relation-ships among the seven species abundances and twoHippopodina performancemeasures (moving from three dimensions to two di-mensions χ2

8=1521 p=033) The first PC explained 485 of

the variance in relationships between community composition (interms of the abundances of seven taxa) and fitness-related traits(fecundityandgrowth)oftheresidentspecieswhile31and21ofthisvariancewasexplainedbythesecondandthirddimensionsrespectively(Table4)Thetwolargestdimensionsbothprovidedev-idencefordirectndashindirectgeneticcovariancebetweenperformancein Hippopodina and community phenotype (Table4 and Figure 4)On the first PC growth and fecunditywere positively associatedwiththeabundancesofencrustingbryozoansandMicrocosmusbutnegatively associated with the abundances of Bugula Sycon and

Coverage Diversity Evenness Growth Fecundity

Coverage 0145

Diversity 0210 028

Evenness 0192 027 0258

Growth 0179 0234 0243 0348

Fecundity 0081 0131 0139 0179 0459

ThedirectndashindirectcovariancematrixderivedfromtheRobertsonndashPriceIdentity(2)ishighlightedingreyple05inbold

TABLE 1emspCompletecovariancematrixforcommunitymetricsgeneticvariances(onthediagonal)andcovariances(belowthediagonal)forthreeindirecteffectsoncommunitymetrics(communitydensitybiomassShannonndashWienerDiversity(Hʹ)andPieloursquosEvenness(Jʹ)shownabovethehorizontalline)andtwodirecteffectsonfitness-relatedtraits(growthandfecundityshownbelowthehorizontalline)oftheresidentspeciesHippopodina

TABLE 2emspThestatisticallysupporteddimensionsofthematrixinTable1Eachdimension(orPC)hasaneigenvaluethatindicatesthedegreeofvariancethatitaccountsforandeachelementoftheeigenvectorindicatestheproduct(directionandmagnitude)ofitsrelationshipwitheachvariableSalientloadingsinbold(seetextfordetails)

PC1

Eigenvalue 1009

Varianceexplained 100

Coverage 0306

Diversity 0422

Evenness 0429

Growth 0543

Fecundity 0501


BalanusOnthesecondPCincontrastgrowthwasnegativelyasso-ciatedwiththeabundancesofencrustingbryozoansJanuaBalanusand Microcosmusbutpositivelyassociatedwith theabundanceoftheerectbryozoanBugula

4emsp |emspDISCUSSION

Heritable variation inHippopodina had widespread indirect geneticeffectsonboththeecologicalpropertiesofcommunitiesandontheabundancesof individual taxaMost importantly thecovariancebe-tween thedirecteffects inperformanceand the indirecteffectsoncommunitypropertiesprovidesevidencethatonespeciesmayinflu-encethepropertiesofacommunityacrossgenerationsinadetermin-isticwayThepotentialfornon-randomcommunitiestodevelopisanindirectresponsetoselectionofthisresidentspeciesSpecificallyat

leastundertheexperimentalconditionsusedhereourresultspredictthattheproliferationofhigherperforminggenotypeswouldseesomespecies(egSycon)becomerarerwhileothers(egencrustingbryozo-ans)wouldbecomemorecommonGenotypicvariationinourresidentspecies has strong and pervasive indirect genetic effects on subse-quentcommunityassemblyandstructureCovarianceamongindirectgeneticeffectshighlightedthatgeneticvariationinourresidentspe-ciesalsoprecipitatesnon-random interactionsamongother speciessuchthatdifferentgenotypesoftheresidentspecieshavediscernibleemergenteffectsonspeciesinteractionswithinthecommunitiestheygenerateDirecteffectsofgenotypeonfocalspeciestraitsaccountedforalmosthalfofthevariationintheperformanceofresidentcolonies

Within generations smaller scale patterns (within this systemlikelymetres rather thankilometres)causedby IIGEsoncommunityassembly are likely to affect the nature of competition in commu-nities (Aarssen1989FridleyGrimeampBilton2007) In themarineenvironment competition is intense at small spatial scales particu-larly among adjacent individualswhere overgrowth interactions arecommon(Buss1979)OurresultssuggestthatsomegenotypesareconsistentlyassociatedwithsomespeciesmorethanothersandthatcertaingenotypesmaycompetewithsomespeciesmoreoftenthanothersThisunderscorestheimportanceofindividualsnotbeingeco-logically equivalent (Bolnick etal 2011WilsonampSwenson2003)thecompetitiveenvironmentsexperiencedbyindividualsofthesamespecies may differ dramatically Our results suggest that differentcommunitymembersmay also interact non-randomly among them-selvesduetogeneticvariationintheresidentspeciesInthepresenceofhigh-performingHippopodinagenotypesforexampleMicrocosmus ismore likely to co-occurwith highdensities of encrusting bryozo-ansandlesslikelytoencounterthespongeSyconMorebroadlynon-randomcompetitiveinteractionsarelikelyinarangeofsystemswheregenotypeaffectscommunityassembly(Fridleyetal2007WhitlockBiltonGrimeampBurke2011)buttheeco-evolutionarydynamicsofsuchinteractionshaveyettobeexplored

AcrossgenerationstheecologicalconsequencesofIIGEsoncom-munityassemblymaydifferaccordingtospatialscale(Chase2003)At


PC1 PC2 PC3

Eigenvalue 113 0714 0484

Varianceexplained 485 307 208

Encrustingbryozoans 044 0347 minus00578

Balanus minus0167 0265 0007

Sycon minus0599 0052 0058

Hydroides 0068 0092 029

Janua 0112 0322 0793

Microcosmus 017 0274 minus0096

Bugula minus0167 minus0604 0443

Growth 0421 minus0479 minus0135

Fecundity 0411 minus0159 024

TABLE 3emspCompletecovariancematrixforcommunitycompositiongeneticvariances(onthediagonal)andcovariances(belowthediagonal)forindirecteffectsoncommunitycomposition(intermsoftheabundancesofsevenmajortaxashownabovethehorizontalline)anddirectgeneticeffectsontwofitness-relatedtraits(growthandfecundityshownbelowthehorizontalline)oftheresidentspeciesHippopodina

Bryozoans Balanus Sycon Hydroides Janua Microcosmus Bugula Growth Fecundity

Bryozoans 043

Balanus minus0081 0


Hydroides minus0088 minus0099 minus0150 0

Janua 0106 minus0064 minus0048 0159 0385

Microcosmus 0422 minus0005 minus0246 minus0067 00279 0

Bugula minus0213 minus0167 0159 minus0107 minus0027 minus0055 042

Growth 0118 minus0333 minus0324 minus0085 minus0118 00122 0088 0387

Fecundity 0086 0049 minus0240 0014 0097 minus0041 0052 0176 0452



smallerscalesforexamplegeneticvariationwithinpopulationsoftheresidentspeciesmayshapelocalcommunities(α-diversity)eveniftheoverallcompositionoftheregionalspeciespool(γ-diversity)weretoremainconstantAtlargerscaleslocalcommunitiesmayvaryinaccor-dancewithgeneticvariationamongpopulationsofthisspeciesHowgenetic variation in a resident species is distributed geographicallymay therefore affect the distribution of other species bothwithinandamongcommunities IfHippopodinaevolvesaspredictedbyourresultsthenvariationamonggenotypesandtheirassociatedcommu-nitiescouldpotentiallygenerateageographicmosaicofspeciesdistri-butionsandabundances(β-diversityThompson1999)Thebroaderimplication is that patterns of β-diversity are influenced by geneticvariationwithinspecieswhichmayinturnbeaffectedbycommunitycontextthusformingthebasisforapotentialeco-evolutionaryfeed-backloop(Wade2007)

Akey limitationof the approachwehave taken isour ability tomeasuretotalfitnessunderfieldconditionsWhilewemeasuredtwokeycomponentsof individual fitness (particularly forsessilecolonialorganisms likeHippopodina) other unmeasured fitness componentsincludesurvivalsettlementandmatingsuccessWedetectedsubstan-tial levels of geneticvariance in our fitness components (consistentwiththegeneralpatternthatsuchcomponentsvarymoregeneticallythan traits underweaker selectionHoule 1992) butwould expectgeneticvariationintotalfitnesstobelowerbecauseselectionshoulddepleteit(BlowsampWalsh2009)ThuswemayhaveoverestimatedtotalvarianceinfitnessandthereforethestrengthoftheIIGEsinoursystemAlternativelygeneticvariationinfitnessmaybemaintainedin

Hippopodinabyspatialortemporalvariation inselection (JohnsonampStinchcombe2007Thompson1999)therebymaintainingvariationincommunitiesassociatedwithdifferentgenotypes(totheextentthatthetwocovary)

ItisunclearbywhatmechanismgeneticvariationinHippopodina affectedcommunityassemblyInprincipletheavailabilityofspacewill always be a limiting factor to community assembly In estab-lished marine benthic communities primary uninhabited space israre and transitory in a setting characterized by competition forspace(Buss1979Sutherland1978)Becausegenotypessystemat-icallydifferedintheirgrowthandthereforeintheamountofspacetheyleftavailableforcolonizationbyothersvariationinsizeamonggenotypesmaywellhaveinfluencedcommunityassemblyTypicallylargerindividualswillreducetheamountofareathatisavailabletoothers(Hughes1984)Ourmethodsstandardizedcommunitymet-ricsasaproportionoftheremainingavailablespacedecouplingthesimpleeffectofareaoncommunitymetricsThoughweprecludedanyartefactualeffectofcolonysize inourmeasuresofcommuni-tiesitmayhaveinfluencedcommunityassemblyindirectlymarineinvertebratescanrecruitdifferentiallytopatchesoffreespacethatvaryinsize(Keough1984)creatingvariationintheassemblyandtrajectoryofsessilemarinecommunitiesWhilewecannoteliminatetheeffectofdifferentgrowthratesamonggenotypesasthedriverof our results there are also othermechanisms that may explainthe community patterns thatwe found For instance variation inmorphological traits related to feeding affectswhat resources areavailabletoothers(Okamura1992)andmayinfluencepatternsof

F IGURE 4emspBiplotsoffactorloadingsforthethreestatisticallysupporteddimensionsofgeneticvariancerelatingcommunitycomposition(intermsoftheabundancesofsevenmajortaxa)tofitness-relatedtraits(fecundityandgrowth)oftheresidentspeciesHippopodina


communityassemblyInthecommunitiesobservedheretheeffectsof different genotypesweremore similar for specieswith similarmorphologiesgeneticvariancesforthetwopolychaetespeciesthatshare similar feeding habits (Janua and Hydroides) remain closelycorrelated in all three dimensions of the PCA Genetic variancesfor Balanus are unrelated to those for the encrusting bryozoansInterestinglyBalanusgrowsupandawayfromthesubstratumandtheonly specieswhich is showedany correlationwithwasSyconanother species that grows vertically away from the substrateDifferential chemical interactions between genotypes and theircommunitiesareanotherpossiblemechanismfor theeffects seenhere Chemical-based interactions (eg allelopathy induced de-fencesandoffencessettlementcues)withinandamongspeciesarewell established inmarineecology (Pawlik2000) suggesting thatbenthicsessilecommunitiesarelikelytobeinfluencedbyacomplexchemicallandscape(ZimmerampButman2000)

Ecological communities are characterized by complex patternsandcyclesof recruitment thatmaycause levelsof geneticvariancetovaryintimeandspace(FreacutedeacutericampWhitlock2007)ConsequentlythestabilityofGacrossmultiplegenerationsinnatureremainsunclear(Arnoldetal2008)InthecaseofHippopodinatheestablishmentofnew recruitsmay be expected to alter themagnitude and specific-ityofgeneticeffectsoncommunityassemblyFurthermoregivenwepredictthatsomegenotypecommunitycombinationswillhavehigherfitnessthanothersgeneticvarianceisexpectedtodepleteovertimeassuchgenotypesincreaseinabundanceWhileGhaslimitationsasapredictivetoolitmaynonethelessshowconservationofitsgeom-etry (JonesArnoldampBuumlrger2007)remainingstableformanytraitcombinations (JonesArnoldampBuumlrger2003)evenafterpopulationdivergence(HineChenowethRundleampBlows2009)Fromaprag-maticperspectivedespiteuncertaintyoveritsstabilityGremainsthebesttoolforpredictingevolutionarychangeacrossgenerations(BlowsampWalsh2009)

Ithaslongbeenrecognizedthattheidentityanddensityofresi-dentspeciescaninfluencesubsequentcommunityassemblyparticu-larlyinthemarineenvironment(Sutherland1978)Notwithstandingour limitations inunderstanding themechanismdrivingour resultsit is clear that genotypes and communities covary significantlyNotably that such covariance further involves the performance ofthosegenotypesoffersrareevidencethatcommunitiesmaychangein response to evolutionary change in a resident species Furtherif species influencetheassemblyofcommunitiesabout them thentheyalso influencetheenvironmentswheretheyevolveandwhichevolveaboutthem(Mooreetal1997)suggestingthatopportunitiesfor feedbacksbetweenecologyandevolutionmaybecomplexbutwidespread

ACKNOWLEDGEMENTS

Theauthorsaregrateful to twoanonymousreviewersatFunctional Ecologywho contributedmanyhelpful and insightful commentsonthemanuscripttoEastCoastMarinaManlyBoatHarbourfortheirgenerousaccesstothestudysiteandthankJasmineLeeforherhelp

with fieldwork AR was supported by a University of QueenslandResearch Scholarship and a UQ International Research TuitionAwardMBWDJMandKMweresupportedbyfundingfromtheAustralianResearchCouncil

AUTHORSrsquo CONTRIBUTIONS

ARKMMBampDMconceivedtheexperimentandmethodologyARcollectedthedataARampKManalysedthedataARampDMledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication

DATA ACCESSIBILITY

Data deposited in the Dryad Digital Depository httpsdoiorg105061dryad30dg0(RiedelMonroBlowsampMarshall2017)

ORCID

Arthur M Riedel httporcidorg0000-0002-3297-7209

Dustin J Marshall httporcidorg0000-0001-6651-6219

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ArnoldSJBuumlrgerRHohenlohePAAjieBCampJonesAG(2008)Understanding theevolutionand stabilityof theG-matrixEvolution622451ndash2461httpsdoiorg101111j1558-5646200800472x

BlowsMW (2007)A taleof twomatricesMultivariateapproaches inevolutionarybiology Journal of Evolutionary Biology201ndash8httpsdoiorg101111j1420-9101200601164x

Blows M W amp Walsh B (2009) Spherical cows grazing in flatlandConstraints to selection and adaptation In JWerf H-UGraser RFrankhamampCGondro (Eds)Adaptation and fitness in animal popu-lations (pp 83ndash101) Dordrecht Springer Netherlands httpsdoiorg101007978-1-4020-9005-9

BolnickDIAmarasekarePAraujoMSBurgerRLevineJMNovakMhellipVasseurDA(2011)WhyintraspecifictraitvariationmattersincommunityecologyTrends in Ecology amp Evolution26183ndash192httpsdoiorg101016jtree201101009

BussLW (1979)Bryozoanovergrowth interactionsndashThe interdepen-dence of competition for space and food Nature 281 475ndash477httpsdoiorg101038281475a0

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DavisKampMarshallDJ(2014)Offspringsizeinaresidentspeciesaf-fects community assembly Journal of Animal Ecology 83 322ndash331httpsdoiorg1011111365-265612136

DungeyHSPottsBMWhithamTGampLiH-F(2000)Plantgenet-icsaffectsarthropodcommunityrichnessandcompositionEvidencefromasyntheticeucalypthybridpopulationEvolution541938ndash1946httpsdoiorg101111j0014-38202000tb01238x


Eitan G (1972) Types of metamorphosis and early astogeny inHippopodina feegeensis (Busk) (Bryozoa-Ascophora) Journal of Experimental Marine Biology and Ecology 8 27ndash30 httpsdoiorg1010160022-0981(72)90053-6

Estes JA amp Palmisano J F (1974) Sea ottersTheir role in structur-ing nearshore communities Science 185 1058ndash1060 httpsdoiorg101126science18541561058

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FergusonNWhiteCRampMarshallDJ(2013)CompetitioninbenthicmarineinvertebratesTheunrecognizedroleofexploitativecompetitionforoxygenEcology94126ndash135httpsdoiorg10189012-07951

Freacutedeacuteric G ampWhitlock M C (2007) Effects of migration on the ge-netic covariance matrix Evolution 61 2398ndash2409 httpsdoiorg101111j1558-5646200700193x

Fridley JDGrimeJ PampBiltonM (2007)Genetic identity of inter-specificneighboursmediatesplantresponsestocompetitionanden-vironmentalvariationinaspecies-richgrasslandJournal of Ecology95908ndash915httpsdoiorg101111j1365-2745200701256x

Genung M A Bailey J K amp Schweitzer J A (2011) Welcome tothe neighbourhood Interspecific genotype by genotype interac-tions in Solidago influence above- and belowground biomass andassociated communities Ecology Letters 15 65ndash73 httpsdoiorg101111j1461-0248201101710x

GenungMASchweitzerJAUacutebedaFFitzpatrickBMPregitzerCCFelker-QuinnEampBaileyJK(2011)Geneticvariationandcommu-nitychangendashSelectionevolutionandfeedbacksFunctional Ecology25408ndash419httpsdoiorg101111j1365-2435201001797x

Hairston N G Ellner S P Geber M A Yoshida T amp Fox J A(2005) Rapid evolution and the convergence of ecological andevolutionary time Ecology Letters 8 1114ndash1127 httpsdoiorg101111j1461-0248200500812x

HaloinJRampStraussSY(2008)Interplaybetweenecologicalcommu-nitiesandevolutionReviewof feedbacks frommicroevolutionary tomacroevolutionaryscalesAnnals of the New York Academy of Science113387ndash125httpsdoiorg101196annals1438003

HineEampBlowsMW(2006)DeterminingtheeffectivedimensionalityofthegeneticvariancendashcovariancematrixGenetics1731135ndash1144httpsdoiorg101534genetics105054627

Hine E Chenoweth S F Rundle H D amp Blows M W (2009)Characterizingtheevolutionofgeneticvarianceusinggeneticcovari-ancetensorsPhilosophical Transactions of the Royal Society B Biological Sciences3641567ndash1578httpsdoiorg101098rstb20080313

Houle D (1992) Comparing evolvability and variability of quantitativetraitsGenetics130195ndash204

Hughes T P (1984) Population dynamics based on individual sizeratherthanageAgeneralmodelwithareefcoralexampleAmerican Naturalist123778ndash795httpsdoiorg101086284239

JacksonJBCampBussLW(1975)AllelopathyandspatialcompetitionamongcoralreefinvertebratesProceedings of the National Academy of Sciences of the United States of America72 5160ndash5163 httpsdoiorg101073pnas72125160

JacksonJBCampCoatesAG(1986)Lifecyclesandevolutionofclonal(Modular) animals Philosophical Transactions of the Royal Society of London Series B Biological Sciences3137ndash22httpsdoiorg101098rstb19860022

JohnsonMT J ampAgrawalAA (2005) Plant genotype and environ-ment interact to shape a diverse arthropod community on eveningprimrose (Oenothera biennis) Ecology 86 874ndash885 httpsdoiorg10189004-1068

JohnsonMTJampStinchcombeJR (2007)Anemergingsynthesisbe-tweencommunityecologyandevolutionarybiologyTrends in Ecology and Evolution22250ndash257httpsdoiorg101016jtree200701014

JohnsonMTJVellendMampStinchcombeJR(2009)Evolutioninplantpopulationsasadriverofecologicalchangesinarthropodcommunities

Philosophical Transactions of the Royal Society (London) B Biological Sciences3641593ndash1605httpsdoiorg101098rstb20080334

JolliffeIT(2002)Principal component analysisNewYorkNYSpringerJonesAGArnold S J amp Buumlrger R (2003) Stability of theG-matrix

in a population experiencing pleiotropic mutation stabilizing se-lection and genetic drift Evolution 57 1747ndash1760 httpsdoiorg101111j0014-38202003tb00583x

JonesAGArnold SJampBuumlrgerR (2007)Themutationmatrix andthe evolution of evolvability Evolution 61 727ndash745 httpsdoiorg101111j1558-5646200700071x

Jones C G Lawton J H amp Shachak M (1994) Organismsas ecosystem engineers Oikos 69 373ndash386 httpsdoiorg101111j1558-5646200700071x

Keough M J (1984) Effects of patch size on the abundance of ses-sile marine invertebrates Ecology 65 423ndash437 httpsdoiorg1023071941405

Koh E G L amp Sweatman H (2000) Chemical warfare among scler-actinians Bioactive natural products from Tubastraea faulkneri Wells kill larvae of potential competitors Journal of Experimental Marine Biology and Ecology 251 141ndash160 httpsdoiorg101016S0022-0981(00)00222-7

LittellRCMillikenGAStroupWWWolfingerRDampSchabenbergerO(2006)SASreg for mixed models2ndedCaryNCSASInstituteInc

McGuiganK Chenoweth S FampBlowsMW (2005) Phenotypic di-vergencealonglinesofgeneticvarianceThe American Naturalist16532ndash43httpsdoiorg101086426600

MonroKampMarshallDJ(2013)Evolutionaryconstraintsandthemain-tenanceof individual specialization throughoutsuccessionEvolution673636ndash3644httpsdoiorg101111evo12220

Monro K amp Poore A G B (2009) The evolvability of growth formin a clonal seaweed Evolution 63 3147ndash3157 httpsdoiorg101111j1558-5646200900802x

MooreA J Brodie ED ampWolf J B (1997) Interacting phenotypesand the evolutionary process I Direct and indirect genetic ef-fects of social interactions Evolution 51 1352ndash1362 httpsdoiorg101111j1558-56461997tb01458x

NydamMampStachowiczJ J (2007) Predator effects on fouling com-munity developmentMarine Ecology - Progress Series 337 93ndash101httpsdoiorg103354meps337093

NyquistWEampBakerRJ(1991)Estimationofheritabilityandpredic-tionofselectionresponseinplantpopulationsCritical Reviews in Plant Sciences10235ndash322httpsdoiorg10108007352689109382313

OkamuraB(1992)MicrohabitatvariationandpatternsofcolonygrowthandfeedinginamarinebryozoanEcology731502ndash1513httpsdoiorg1023071940693

Osman R W amp Whitlatch R B (1995) The influence of residentadults on recruitment ndash A comparison to settlement Journal of Experimental Marine Biology and Ecology 190 169ndash198 httpsdoiorg1010160022-0981(95)00035-P

Pawlik J R (2000) Marine chemical ecology Marine Ecology- Progress Series207225ndash226httpsdoiorg103354meps207225

Petfield D Chenoweth S F Rundle H D amp BlowsMW (2005)Genetic variance in female condition predicts indirect geneticvariance in male sexual display traits Proceedings of the National Acedemy of Science USA1026045ndash6050httpsdoiorg101073pnas0409378102

QuinnGPampKeoughMJ(2001)Experimental design and data analysis for biologistsCambridgeUKCambridgeUnivesityPress

RidenhourBJampNuismerSL(2014)AquantitativegeneticapproachforpredictingecologicalchangeinbiologicalcommunitiesTheoretical Ecology7137ndash148httpsdoiorg101007s12080-013-0206-4

RiedelAMonroKBlowsMWampMarshallDJ(2014)Relativeinflu-ence of resident species and environmental variation on communityassemblyMarine Ecology Progress Series 499 103ndash113 httpsdoiorg103354meps10695


RiedelAMMonroKBlowsMWampMarshallDJ(2017)DatafromGenotypiccovariancebetweentheperformanceofaresidentspeciesandcommunityassemblyinthefieldDryad Digital Depositoryhttpsdoiorg105061dryad30dg0

Robertson A (1966) A mathematical model of the culling process indairycattleAnimal Production7319ndash324httpsdoiorg101017S0003356100037752

RowntreeJKCameronDDampPreziosiRF(2011)Geneticvariationchanges the interactions between the parasitic plant-ecosystem en-gineerRhinanthusanditshostsPhilosophical Transactions of the Royal Society (London) B Biological Sciences 366 1380ndash1388 httpsdoiorg101098rstb20100320

Russ G R (1982) Overgrowth in a marine epifaunal communityCompetitivehierarchiesandcompetitivenetworksOecologia5312ndash19httpsdoiorg101007BF00377130

SutherlandJP(1978)FunctionalrolesofSchizoporella and StyelainthefoulingcommunityatBeaufortNorthCarolinaEcology59257ndash264httpsdoiorg1023071936371

Svensson J R amp Marshall D J (2015) Limiting resources in ses-sile systems Food enhances diversity and growth of suspensionfeeders despite available space Ecology 96 819ndash827 httpsdoiorg10189014-06651

Thacker R W Becerro M A Lumbang W A amp Paul V J (1998)AllelopathicinteractionsbetweenspongesonatropicalreefEcology79 1740ndash1750 httpsdoiorg1018900012-9658(1998)079[1740AIBSOA]20CO2

Thompson J N (1999) Specific hypotheses on the geographic mosaicof coevolution The American Naturalist 153 S1ndashS14 httpsdoiorg101086303208

Tilbrook K J (1999) Description of Hippopodina feegeensis and three other species of Hippopodina Levinsen 1909 (BryozoaCheilostomatida) Journal of Zoology 247 449ndash456 httpsdoiorg101111j1469-79981999tb01008x

VellendM(2010)ConceptualsynthesisincommunityecologyQuarterly Review of Biology85183ndash206httpsdoiorg101086652373

WadeMJ(2007)Theco-evolutionarygeneticsofecologicalcommuni-tiesNature Reviews Genetics 8 185ndash195 httpsdoiorg101038nrg2031

WalshBampBlowsMW(2009)Abundantgeneticvariation+strongse-lection=multivariategeneticconstraintsAgeometricviewofadap-tationAnnual Review of Ecology Evolution and Systematics4041ndash59httpsdoiorg101146annurevecolsys110308120232

WhithamTGBaileyJKSchweitzerJAShusterSMBangertRKLeRoyCJhellipWooleySC (2006)Aframeworkforcommunity

and ecosystem genetics From genes to ecosystemsNature Reviews Genetics7510ndash523httpsdoiorg101038nrg1877

Whitlock R BiltonMCGrime J P ampBurkeT (2011) Fine-scalecommunity and genetic structure are tightly linked in species-richgrasslands Philosophical Transactions of the Royal Society (London) B Biological Sciences 366 1346ndash1357 httpsdoiorg101098rstb20100329

Wilson D S amp Swenson W (2003) Community genetics andcommunity selection Ecology 84 586ndash588 httpsdoiorg1018900012-9658(2003)084[0586CGACS]20CO2

WolfJB(2003)GeneticarchitectureandevolutionaryconstraintwhentheenvironmentcontainsgenesProceedings of the National Academy of Sciences of the United States of America1004655ndash4660httpsdoiorg101073pnas0635741100

Wolf J B Brodie E D Cheverud J M Moore A J ampWadeM J(1998) Evolutionary consequences of indirect genetic effectsTrends in Ecology and Evolution 13 64ndash69 httpsdoiorg101016S0169-5347(97)01233-0

Wolf J BMutic J J ampKover P X (2011) Functional genetics of in-traspecificecologicalinteractionsinArabidopsis thaliana Philosophical Transactions of the Royal Society (London) B Biological Sciences 3661358ndash1367httpsdoiorg101098rstb20100239

YundPOMarcumYampStewart-SavageJ(1997)Life-historyvariationin a colonial ascidianBroad-senseheritabilities and tradeoffs inallo-cationtoasexualgrowthandmaleandfemalereproductionBiological Bulletin192290ndash299httpsdoiorg1023071542722

Zimmer R K amp Butman CA (2000) Chemical signaling processes inthemarineenvironmentBiological Bulletin198168ndash187httpsdoiorg1023071542522

SUPPORTING INFORMATION

Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle

How to cite this articleRiedelAMMonroKBlowsMWMarshallDJGenotypiccovariancebetweentheperformanceofaresidentspeciesandcommunityassemblyinthefieldFunct Ecol 2017001ndash12 httpsdoiorg1011111365-243513005


geneticvariationbutthepotentialfortheseeffectstopersistremainsunclear An elegant study by Agrawal Hastings Johnson Maronand Salminen (2012) provided the first evidence for real-time eco-evolutionaryfeedbacksbetweenaresidentspeciesanditscommunityunderfieldconditions(Agrawaletal2012)butsuchdemonstrationsareexceedinglyrareandmaynotbeaccessibleinmanysystemsAssuchidentifyingdirectandenduringlinksbetweencommunityassem-blyandgeneticvariationwithinpopulationsmorebroadlyremainsanongoingchallenge

Thecentralobservationunderlyingecosystemgeneticsisthatthegenotypeofaresidentspeciescanaffectothermembersoftheassoci-atedcommunityInthisregardecosystemgeneticshasparalleledthe-oryaddressingindirectgeneticeffectsIndirectgeneticeffects(IGEs)aregeneratedwhenheritablevariationamongindividualsofonespe-ciesinfluencestraitexpressioninotherindividuals(MooreBrodieampWolf1997seeFigureS1)Indirectgeneticeffectsinthecontextofasinglespeciesarewellestablished(PetfieldChenowethRundleampBlows2005WolfBrodieCheverudMooreampWade1998WolfMuticampKover2011)Theyoccurwhengeneticvariationamongin-dividuals modifies the environment for other unrelated individualsleadingtoindirectgeneticvariationinphenotypefitnessamongtheselatterindividuals(Wolf2003)Inacommunitycontexttheeffectofheritabletraitvariationinaresidentspeciesoncommunitypropertiesistermedaninterspecificindirectgeneticeffect(IIGE)(Genungetal2011)OftenIIGEsarereportedasestimatesofcommunityheritabil-ityorhowmuchofthevariation inacommunityproperty isduetogeneticvariationamongindividualsofaresidentspeciesForexampleIIGEshavebeencommonlyreportedinplantsandincludetheeffectofhost-plantgenotypeontheassemblyofitsarthropodcommunityandinfluencesonabove-groundandbelow-groundinteractions(DungeyPotts Whitham amp Li 2000 Genung Bailey amp Schweitzer 2011Johnson amp Agrawal 2005 Rowntree Cameron amp Preziosi 2011Whithametal2006)

Thepatternandmagnitudeofthegeneticbasistomulti-traitvari-ationinapopulationissummarizedinGamatrixwhosediagonalele-mentsaretheadditivegeneticvariances(orinthisinstancegenotypicvariances)oftraitsandwhoseoff-diagonalelementsarethegenetic(orbroad-sensegenotypic)covariancesofthesetraitsthusG1isthegeneticvarianceintrait1andG12isthegeneticcovariancebetweentraits1and2

The value ofmodellingG bringing insights from evolutionaryprocessestobearonecologicaldynamicsliesintheabilitytopre-dictchangeincommunityproperties(RidenhourampNuismer2014)however our methods differ in that instead of evaluatingG and its corresponding selection gradient to estimate changewe hereevaluatethecovarianceoffitness-associatedtraitswithcommunitypropertiesasdescribedbelow In thecontextof IIGEsGenables

examination not only of the indirect effects of a resident speciesonindividualtaxabutalsooffurtheralterationtotherelationshipsamongthosetaxainthecommunityNotwithstandinglimitationstothestabilityofGwhichcanchangeovermultiplegenerationsduetoselectionordrift(McGuiganChenowethampBlows2005)mostcomparative studies find thatG matrices estimated from experi-mental andnatural populations are predominantly stable geomet-rically (ArnoldBuumlrgerHohenloheAjieampJones2008)GiventhereasonableassumptionofstabilityGmatricescanbereliablyusedtoestimate thatpartofecological interactionamongspecies thatderivesfromgeneticvariation

WhiletheexistenceofIIGEsofaresidentspeciesonitsassociatedcommunitysuggeststhatcommunitypropertiesmayrespondtoevo-lutionarychangesintheresidentspeciesitdoesnotinevitablyfollowthatthegeneticvariationinthespeciesdrivingtheIIGEisassociatedwith fitnessThisdistinction iscriticalbecauseonly thatpartof thegeneticvariation intheresidentspeciesthatcovarieswithfitness ispredictedtocausemultigenerationalchangesinthecommunityprop-ertiesinfluencedbythatspeciesMoreformallytheresponsetose-lectiononanytrait (includingthetraitsofresidentspeciesthatmayinfluence community properties) is predicted by that traitrsquos geneticcovariancewithfitness(Robertson1966)

where∆zisthechangeintraitvaluefromonegenerationtothenextand ωisfitnessAppliedtocommunitygenetics∆zisthechangeinthecommunitypropertyfromonegenerationtothenextandωisthefitnessoftheresidentspeciesAnIIGEonacommunityisthere-forepredictedtohavepersistentanddirectionalconsequencesforthatcommunityonlywhenthefitnessofindividualsintheresidentspecies and the properties of the community covary genetically(JohnsonVellend amp Stinchcombe 2009) The genetic covariancebetweenthefitnessof individuals inaresidentspeciesanditsas-sociatedcommunityshouldpredictthereforewhetheranyeffectsofthatspeciesonitscommunitywillpersistacrossgenerationsInthe absence of this genetic covariance (sometimes referred to asdirectndashindirectcovarianceinquantitativegenetics)thereisnopo-tentialforgeneticeffectsinonespeciestoinfluencethetrajectoryofcommunityassemblyorforeco-evolutionaryfeedbacksbetweenthespeciesanditssurroundingcommunity(HaloinampStrauss2008)Withoutthispotentialtheindirectgeneticeffectsgeneratedamonggenotypesofaresidentspeciesonassociatedcommunitiesshouldvarystochastically fromgenerationtogenerationascertaingeno-typesbecomemoreorlesscommonEachgenerationwillinfluenceassemblyanewbut there isnopotential fordeterministicgeneticeffectstobetransmittedfromonegenerationtothenextAppliedtoIIGEsthisistheequivalentofgeneticdrift(Vellend2010)inthatvariation in abundancesofother species in the communitywouldsubsistthroughgenerationswithoutbeinginfluencedbytheevolu-tionoffitnessintheresidentspecies

Despitemounting evidence for IIGEs studies that link them tofitness remain rareHereunder fieldconditionsweexplore the re-lationship between community properties and heritablevariation in

(1)G =

⎡⎢⎢⎢⎢⎢⎢⎣

G1 G12 G13 hellip G1n

G2 G23 hellip G2n

G3 hellip G3n

hellip

Gn

⎤⎥⎥⎥⎥⎥⎥⎦

(2)Δz = covG(zω)


























(3)H=minus

Ssum

i=1

(pi In (pi))







3emsp |emspRESULTS























Coverage 0145

Diversity 0210 028

Evenness 0192 027 0258

Growth 0179 0234 0243 0348

Fecundity 0081 0131 0139 0179 0459




PC1

Eigenvalue 1009


Coverage 0306

Diversity 0422

Evenness 0429

Growth 0543

Fecundity 0501









PC1 PC2 PC3






Hydroides 0068 0092 029

Janua 0112 0322 0793







Bryozoans 043

Balanus minus0081 0



















ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES







































































































(3)H=minus

Ssum

i=1

(pi In (pi))







3emsp |emspRESULTS























Coverage 0145

Diversity 0210 028

Evenness 0192 027 0258

Growth 0179 0234 0243 0348

Fecundity 0081 0131 0139 0179 0459




PC1

Eigenvalue 1009


Coverage 0306

Diversity 0422

Evenness 0429

Growth 0543

Fecundity 0501









PC1 PC2 PC3






Hydroides 0068 0092 029

Janua 0112 0322 0793







Bryozoans 043

Balanus minus0081 0



















ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES





























































































(3)H=minus

Ssum

i=1

(pi In (pi))







3emsp |emspRESULTS























Coverage 0145

Diversity 0210 028

Evenness 0192 027 0258

Growth 0179 0234 0243 0348

Fecundity 0081 0131 0139 0179 0459




PC1

Eigenvalue 1009


Coverage 0306

Diversity 0422

Evenness 0429

Growth 0543

Fecundity 0501









PC1 PC2 PC3






Hydroides 0068 0092 029

Janua 0112 0322 0793







Bryozoans 043

Balanus minus0081 0



















ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES




















































































3emsp |emspRESULTS























Coverage 0145

Diversity 0210 028

Evenness 0192 027 0258

Growth 0179 0234 0243 0348

Fecundity 0081 0131 0139 0179 0459




PC1

Eigenvalue 1009


Coverage 0306

Diversity 0422

Evenness 0429

Growth 0543

Fecundity 0501









PC1 PC2 PC3






Hydroides 0068 0092 029

Janua 0112 0322 0793







Bryozoans 043

Balanus minus0081 0



















ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES

































































































Coverage 0145

Diversity 0210 028

Evenness 0192 027 0258

Growth 0179 0234 0243 0348

Fecundity 0081 0131 0139 0179 0459




PC1

Eigenvalue 1009


Coverage 0306

Diversity 0422

Evenness 0429

Growth 0543

Fecundity 0501









PC1 PC2 PC3






Hydroides 0068 0092 029

Janua 0112 0322 0793







Bryozoans 043

Balanus minus0081 0



















ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES


























































































Coverage 0145

Diversity 0210 028

Evenness 0192 027 0258

Growth 0179 0234 0243 0348

Fecundity 0081 0131 0139 0179 0459




PC1

Eigenvalue 1009


Coverage 0306

Diversity 0422

Evenness 0429

Growth 0543

Fecundity 0501









PC1 PC2 PC3






Hydroides 0068 0092 029

Janua 0112 0322 0793







Bryozoans 043

Balanus minus0081 0



















ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES






















































































PC1 PC2 PC3






Hydroides 0068 0092 029

Janua 0112 0322 0793







Bryozoans 043

Balanus minus0081 0



















ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES
























































































ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES


















































































ACKNOWLEDGEMENTS





DATA ACCESSIBILITY


ORCID



REFERENCES









































































































































































Documents

Genotypic covariance between the performance of a …...species and the properties of the community covary genetically (Johnson, Vellend, & Stinchcombe, 2009). The genetic covariance