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Sex-specificbehavioralsyndromesallowtheindependentevolutionofbehavioraldimorphism
RaphaelRoyauté1,2,4AnnHedrick3
NedA.Dochtermann2
1MovementEcologyGroup,SenckenbergBiodiversityandClimateResearchCentre(SBiK-F),Frankfurt,Germany(currentaddress)2DepartmentofBiologicalSciences;NorthDakotaStateUniversity,Fargo,USA3DepartmentofNeurobiology,Physiology,andBehavior;UniversityofCalifornia,Davis,USA4correspondingauthor:[email protected] :Sex-specificsyndromesandbehavioralsexualdimorphismKeywords:Behavioralsyndromes,evolutionaryconstraints,Gmatrix,personality,behavioralecology,sexualdimorphism,intralocussexualconflictsAuthorContributions:Allauthorsconceivedtheprojectandsupervisedthegatheringofdata.R.Rconductedbehavioraltrialsandanalyzedthedata.R.R.wrotethefirstdraftofthemanuscriptandallauthorscontributedtosubsequentversions.Conflictsofinterests:TheauthorsdeclarenoconflictofinterestsDataAccessibilityStatement:Alldata,codeandanalysesareavailableat:https://osf.io/pnug5/Acknowledgements:WethankMonicaBerdal,KatelynCannon,JeremyDalos,SarahFelde,1
BradyKlock,IshanJoshi,HannahLambert,JennaLaCoursiereandAlondraNeunsingerfor2
assistanceinconductingbehavioraltrialsandinrearingandcareofthecricketsand3
MartoriFarms,DavidLightfoot,ScottBundy,NicoFranz,SangmiLee,CameronJones,4
KennyChapin,TiEriksson,MerandaFeagins,CharlotteMulloney,MelodyMartinez,Allyson5
Richins,MaurielRodriguez,HelenVesselsandDavidWikmanforassistanceincollecting6
thecrickets.WethankforJ.SztepanaczandA.J.Wilsonfortheiradviceonstatistical7
analysesandK.Laskowskiforcommentsonanearlydraftofthismanuscript.Thiswork8
wassupportedbyUSNSFIOSgrants1557951and1558069toN.A.D.andA.H.respectively. 9
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ABSTRACT10
Whenselectiondiffersbysex,thecapacityforsexestoreachoptimalphenotypescanbe11
constrainedbythesharedgenomeofmalesandfemales.Becausephenotypictraitsare12
oftencorrelated,thisdifferenceextendsacrossmultipletraitsandunderlyinggenetic13
correlationscanfurtherconstrainevolutionaryresponses.Behaviorsarefrequently14
correlatedasbehavioralsyndromes,andthesecorrelationsoftenhaveageneticbasis.15
However,whethercross-sexandacrossbehaviorcorrelationsleadtoconstrainedevolution16
remainsunknown.Here,weshowthataboldness-activitysyndromeisstronglysex-17
specificatthegeneticlevelinthewesternfieldcricket(Gryllusinteger)andthatemergence18
fromashelterisgeneticallyindependentbetweenmalesandfemales.However,male19
activityisstronglyrelatedtofemaleshelteremergence,creatingthepotentialforbiased20
responsestoselection.Ourresultsshowthatthesex-specificgeneticarchitectureof21
behavioralsyndromescanshapetheevolutionofbehavioralphenotypes.22
23
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INTRODUCTION24
Malesandfemalessharethesamegenomebutoftenrelyondifferentstrategiestoincrease25
fitness.Thiscanleadtointralocussexualconflictswhereselectionactingonasharedtrait26
displacesonesexfromitsoptimum(HedrickandTemeles1989;Bondurianskyand27
Chenoweth2009).Thissexualconflictisfurthercomplicatedbytheconstrainingpotential28
ofgeneticcorrelations(Lande1980;WalshandBlows2009).Forexample,behaviorsare29
oftencorrelatedascomponentsofabehavioralsyndrome(Sihetal.2004)andthese30
behavioralsyndromeshavethepotentialtoalterevolutionaryoutcomes(Dochtermann31
andDingemanse2013).32
Ingeneral,anysustainedselectionfavoringdifferentoptimabetweensexes,i.e.33
sexuallydiscordantselection,willeventuallyresolvethesexualconflictandattenuate34
geneticconstraintsovertime,thusallowingsexestoevolveindependently(Delphetal.35
2011).Thisconstraintcanbeformallymeasuredasthecross-sexcorrelationcoefficientrmf,36
withvalues<1increasingtherapidityatwhichsexualdimorphismcanevolve.Cross-sex37
correlationsaregenerallylargebuttendtodecreaseinspecieswithstrongersexual38
dimorphism(Poissantetal.2010).Additionalconstraintscanemergewhengeneralizingto39
multiplephenotypesexpressedinmalesandfemalesandtheirinteractions(Lande1980).40
Bydecomposingtheadditivegeneticcovariancematrixintoitssex-specific(Gm,Gf)and41
cross-sexsub-matrices(B),onecanestimateifgeneticcorrelationsacrosssexesandtraits42
createconstrainedevolutionaryoutcomes(Fig.1).43
Thisdecompositionapproachhasbeenusedformorphologicaltraits,revealingthat44
cross-sexcovariances(i.e.theBmatrix,(Lande1980))canprofoundlyaltertheevolution45
ofsexualdimorphism(Gosdenetal.2012;Bergeretal.2014;GosdenandChenoweth46
2014),especiallywhenselectionfavorsdifferentaveragetraitvaluesforeachsex(Long47
andRice2007;Bergeretal.2014).However,theGm,Gf,andBhaverarelybeenestimated48
forbehaviors.Howmuchthegeneticarchitectureofbehavioralsyndromescanaffect49
evolutionaryoutcomesunderintralocussexualconflictremainsunclear.Thisisan50
importantomissionbecausebehaviorfrequentlyimpactsbothsurvivalandfitness(Moiron51
etal.2020)andsexualdimorphismiscommonforbehaviors(Blanckenhorn2005;Aragón52
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2011;Mainwaringetal.2011;Kokrasetal.2012).Despitemanyconceptualargumentsfor53
whybehavioralsyndromesshoulddifferbysexes(Schuettetal.2010;Hämäläinenetal.54
2018;Immonenetal.2018),sex-differencesintheexpressionofbehavioralcorrelations55
arefrequentlyignoredinpractice.Asaresult,thedegreetowhichcross-sexgenetic56
correlationsmightbeshapedbysexualconflictforbehavioralphenotypesremains57
unknownandtheimportanceofthesecorrelationsfortheevolutionofbehaviorsis58
similarlyunknown. 59
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Figure1.Thegeneticarchitectureofcross-sexcorrelationscanhavenon-intuitive61 consequencesonevolutionaryresponsesandsexualdimorphism.A)Highvaluesofcross-62 sexcorrelationsforthesametraits(here,bodysize)indicatethatmaleandfemaleaverages63 arepositivelycorrelatedamongfamilies.B)Thecross-sexcovariancematrix(Gmf)allows64 tocomparepatternsofgeneticcovarianceswithinsexes(herebetweenbodymassand65 bodysize)aswellasunderstandthestrengthofcross-traitcorrelationswithinandamong66 traits.C)Cross-sexcross-traitcorrelation(rmf)canproducenon-intuitiveresponsesto67 selectivepressures.Hereweshow3scenariosindicativeofthevarietyofresponsesto68 selection(Δz)thatcanoccurdependingonthedirectionofselection(β)andthemagnitude69 andorientationofrmf.Theellipsesrepresentthebivariate(co)variationinfemurlength70 andmass,withthepopulationaverageatthevertexofthe(thinsolid)linesindicatingthe71 directionsinbivariatespacewiththemostvariation.Dashedlinesrepresentthedirection72 selection(β)ispushingapopulation’saverageandthesolidthickarrowsshowthe73 directionandmagnitude(arrowtip)ofselectionresponses.InbothscenariosC.1andC.2,74 selectionisconcordant—i.e.actingthesame—betweensexesandmalesandfemaleshave75 thesamefitnessoptimum.InscenarioC.3,selectionissexuallydiscordantandfavors76 increasedsexualdimorphism.ScenarioC.1showsthatstrongcross-sexcrosstrait77 correlationscanbiassexesawayfromtheiroptimum.InscenarioC.2,nullrmfresultsin78 independenttrajectoriesbysexes.InscenarioC.3,theeffectoffathersontheirdaughters’79 phenotypeisoppositeofthatofmother’sontheirsons’,resultinginasymmetricrmfand80 biasedresponsestoselectioninmales. 81
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Intralocussexualconflictshouldbeparticularlystronginthefieldcrickets82
(Gryllidae).Inmanyfieldcrickets,malesandfemalesdifferintheirbehaviorsand83
reproductivestrategies(HedrickandKortet2012).Forexample,femalesexploretheir84
environmentstosamplemateswhilemalesremainatburrowsfromwhichtheysignal85
(FrenchandCade1987).Further,aboldness-activitysyndromehasaconservedgenetic86
basisinatleastonespecies,theWesternstutter-trillingfieldcricket(Gryllusinteger),87
whichseemstohaveconstrainedbehavioraldivergence(Royautéetal.2020).Whetherthis88
syndromeissex-specificiscurrentlyunknownbutthecombinationofconserved89
syndromestogetherwithalackofsex-specificitywouldfurtherconstraintheabilityof90
populationstorespondtolocalselectivepressures.91
Hereweusedbehavioralmeasurementsofover960Gryllusintegerindividualsto92
estimatetheinfluenceofcross-sexgeneticcorrelationsonevolutionaryresponses.We93
predictedthatcricketswouldexhibitdimorphisminaverageactivitygiventhemate-94
samplingbehavioroffemalesandthatgeneticvarianceforthistraitwouldbelowerfor95
femalecricketsduetoselectionfavoringincreasedtraveling.Wealsopredictedsex-96
specificityinthebehavioralsyndrome,withastrongerpositivegeneticcorrelation97
betweenantipredatorresponseandactivityinfemales.Sinceexitfromrefugiaandactivity98
shouldhaveastrongerinfluenceonfemalefitness,wealsoexpectedastrongercorrelation99
betweenshelteremergencewithactivityandantipredatorresponseinfemales.Although100
therearefewestimatesforcross-sexcorrelationsofbehaviors,thoseavailablesuggest101
behaviorsareundersimilarconstraintsasotherphenotypes(Poissantetal.2010).We102
thereforeexpectedthatcross-sexgeneticcorrelations(rmf)wouldnotdepartsignificantly103
from1.Wetestedthesepredictionsbyestimatingthecross-sexcovariancematrix,i.e.Gmf,104
decomposedintoitssex-specificandcross-sexsub-matrices(Gm,GfandBsubmatrices,105
Figure1).Wecomparedthestrengthofcovariancesamongsexesandtheeffectsofthese106
covariancesonresponsestoselectionusingrandomskeweranalysis.107
108
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METHODS109
Wecollectedadultfemalecricketsfromfourpopulationsthroughoutthesouthwesternand110
westernUS:Socorro,NM;LasCruces,NM;Aguila,AZ;andDunnigan,CA(Figure2)during111
thesummerof2017andhousedthemandinourlaboratoryfacilitiesatNorthDakotaState112
University.Femaleswerehousedindividuallyin0.71Lcontainersandprovidedwithad113
libitumfood(PurinaChickStarter)andwater(waterwasprovidedinglassvialscapped114
withcotton).Eachcricketwasalsoprovidedwithasmallpieceofcardboardeggcartonfor115
shelter.Thecrickethousingroomwasmaintained~27Cona12:12dark:lightcycle116
reversedsuchthattheroomwasdarkduringdaytimehours.Werunoffspringofthis117
parentalgenerationthroughmultiplebehavioraltrialsbeforematingindividualsatrandom118
withineachpopulation.Werepeatedthisprocessfortwoadditionalgenerations.119
Behavioraltesting120
Latencytoemergefromshelter121
Gryllidcricketsusesmallburrowsandnaturalcracksasrefugestowhichtheyretreatwhen122
underthreat.Thetimetakentoemergefromashelterafterdisturbancecanthereforebe123
consideredaproxyforrisk-takingbehavioror“boldness”(KortetandHedrick2007).We124
transferredindividualsfromtheirhomecontainersintosmallartificialburrows(40cm3)125
placedwithina34.6×21cmarena.Weleftthecricketstorestfortwominutesafterwhich126
weremovedthecapfromtheburrowandletindividualsemerge.Wethenrecordedhow127
longittookforanindividualtoemerge(inseconds)foruptosixminutesandthirty128
seconds.Individualsthatdidnotemergeweregivenamaximumlatencyof390seconds.129
Openfieldexploratorybehavior130
Weusedopenfieldteststomeasureactivityandexploratorypropensityina30×30cm131
plexiglassarena.Thesetestsareclassicbehavioralassayacrosstaxa(WalshandCummins132
1976)andcanrevealstrongamong-individualdifferencesinexplorationpatterns,133
includingincrickets(Royautéetal.2015,2019;RoyautéandDochtermann2017).134
Individualsthatmovethroughmoreofthearenaareconsideredmorethoroughexplorers135
(Réaleetal.2007).Weintroducedindividualsintothearenaandleftthemtorestundera136
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smallcontainerfor30seconds.Attheendofthis30seconds,weremovedthecontainer137
andthecricketwasallowedtoexplorethearenafor3minutesand40seconds.Thearena138
wascleanedwithisopropylalcoholbetweentrialstoremoveanychemosensorycuesfrom139
thearena.WeusedEthovisionXTtorecordthetotaldistancetheindividualmovedduring140
thetrial(cm).141
Responsetocuesofpredatorpresence142
Wemeasuredtheresponsetocuesofpredatorpresence,abehavioralassaycommonly143
usedinGryllidspeciestodetermineantipredatorresponse(RoyautéandDochtermann144
2017;Royautéetal.2019).Specifically,individualswereintroducedintoa15cmdiameter145
circulararena(7.5cmheight),thefloorofwhichwascoveredwithdryfilterpaperthathad146
beensoakedwithdilutedexcretafromleopardgeckos(Eublepharismacularius).Crickets147
respondtoexposuretoleopardgeckocuesbyincreasingactivityandindividualswith148
higherdistancemovedareconsideredmoreresponsivetothecue(Royautéand149
Dochtermann2017;Royautéetal.2019).Weintroducedcricketstoaportionofthearena150
withoutpredatorcueandleftthemtorestunderasmallshelterfor30seconds.Wethen151
removedtheshelterandallowedtheindividualallowedtofreelymovethroughoutthe152
arenafor3minutesand40seconds.WethenusedEthovisionXTtorecordthetotal153
distanceanindividualmovedduringthetrial(cm).154
155
Statisticalanalyses156
AllanalyseswereperformedusingRversion4.0.3(Rcitation)usingtheMCMCglmm157
package (Hadfield2010).158
Estimationofcross-sexgeneticcovariances(Gmf)159
Weusedamulti-responsemixedeffectanimalmodels(Kruuk2004;Wilsonetal.2010)to160
estimategeneticvariancesandcovariances(i.e.theGmfmatrix).Weincludedtheeffectsof161
temperature,dayandtimeoftestinginthebehavioralarenaroomalongwithsex,life-stage162
andmassoftheindividualasfixedeffects.Weusedtheindividualrelatednessmatrix163
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(basedontheknownpedigree)asarandomeffectandthefollowingbehavioraltraitswere164
includedasresponsevariables:(i)thelatencythatanindividualemergedfromtheshelter165
duringthetrial(modeledascensoredGaussian),(ii)thedistancemovedduringtheopen166
fieldtrial(Gaussian),(iii)thedistanceanindividualmovedduringthepredatorcue167
responsetrial(Gaussian).Toestimatebothsex-specificandcross-sexcovariances,we168
treatedthebehaviorofeachsexasaseparatetrait-resultingintheestimationofa6×6169
covariancematrix.Weranthemulti-responsemodelwithanMCMCchainof4.8×106170
iterations,withan800,000burn-inperiodandathinningintervalof4,000andweuseda171
parameterexpandedpriorthatwasminimallyinformativeforbothvariancesand172
covariances.Allvariancesandcovarianceswereestimatedattheadditivegeneticleveland173
onthelatentscale.174
175
Estimationofbehavioraldimorphism176
Wetestedfortheexistenceofsexualdimorphisminbehavioralexpressionbycomparing177
linearcoefficientforthesexfixedeffectincludedinourmultivariateanimalmodelandbase178
ourstatisticalinferenceontheirBayesianprobability(Pmcmc).Thismetricvariesbetween179
0.5and1andindicatestheprobabilityofasignificantdifferencebasedonthenumberof180
posteriorestimatesoverlappingwith0.Pmcmcvalues>0.95werejudgedassignificant.181
182
Comparisonofsex-specificcovariances(GmandGfmatrices)183
Weusedatwo-stepapproachtocomparetheintensityofthedifferenceingenetic184
covariancesamongsexes.First,wecalculatedthedifferenceincovariancebetweenmales185
andfemales(ΔCOVA)foreachpairofbehaviorsandtheirassociatedBayesianprobabilities186
(Pmcmc).Next,wetestedwhethersex-specificcovariancesweresimilarlyoriented.Todo187
so,wecalculatedthevectorcorrelation(r°)betweenaxescontainingthehighestamountof188
geneticvariationusingeigenvaluedecomposition.Wethenestimatedwhetherthe189
resultingvectorcorrelationsamongeigenvectorsofGdifferedsubstantiallyfrom190
expectationsof0(noalignmentofgeneticvariationamongsexes)and1(perfect191
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alignment).Becausevectorcorrelationsareboundedby0and1,weestimatedtheRegion192
ofPosteriorEquivalence(ROPE)whichwedefinedastheintervals[0.0;0.1]and[0.9;1.0].193
EstimatesfallingwithintheseROPEregionsarejudged“practicallyequivalent”tovector194
correlationsof0and1respectively.Weconvertedtheproportionofestimatesfalling195
outsidetheseROPEregionsintoPmcmcvaluestoinfersignificance,withPmcmc>0.95196
indicatingsignificantdeparturefromthesenullhypotheses.197
198
Estimatingthegeneticconstraintimposedbythecross-sexcovariancematrix(B)199
Wefirsttestedwhethercross-sexcovarianceswithintraitsdifferedsignificantlyfrom0and200
1.Cross-sexcovariancesarerepresentedonthediagonalelementsoftheBmatrix.A201
covarianceof0indicatecompletegeneticindependenceamongsexes,whichwe202
determinedusingBayesianprobabilities(Pmcmc).Totestforadeparturefromcomplete203
geneticcouplingamongsexes,weconvertedthecovariancestocorrelationcoefficients204
(rmf)andusedtheROPEtestdescribedabove.Wetheninvestigatedwhethercross-sex205
cross-traitscovariances–representedontheoff-diagonalelementsofB–differed206
significantlyfromoneanotherbycalculatingtheposteriordifferenceincovarianceas207
described(ΔCOVA).208
Next,wecomparedtheevolutionarytrajectoriesofsexeswithascenarioweresexes209
evolvedindependentlywithoneweresexeswerefullyconstrained(Coxetal.2017).Todo210
so,wesimulated500selectiongradientsbasedonamultivariatenormaldistributionthat211
wescaledtounitlength.Wegeneratedconcordantselectiongradientsbyassigningthe212
samevaluestomaleandfemalegradients(βf=βm)anddiscordantselectionbysettingβf=-213
βm.Weappliedeachselectiongradienttoall1,000posteriorcovariancematricesofGmf214
estimatedfromourmultivariateanimalmodel,thusensuringwetooktheuncertaintyin215
estimatesforward.Wethencalculatedtheresultingresponsetoselection(𝛥𝑧̅)byapplying216
themultivariatebreeder’sequationforcross-sexcovariance(Lande1980):217
$𝛥𝑧!̅𝛥𝑧"̅
% = #$$𝐆𝐟 𝐁′𝐁 𝐆𝐦
% $𝛽!𝛽"% (equation1)218
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Wecontrastedtheseresponsestoselectiontocaseswherewesetallcross-sexcovariances219
0andbyfullyconstrainingcross-sexcorrelationsto1.Toachievethislaststep,we220
convertedGmftoacorrelationmatrixandreplacedBelementsby1.Wethenback-221
convertedthismodifiedmatrixintocovariancesbyreplacingthediagonalelementsofBby222
thegeometricmeanofmaleandfemalegeneticvariances(i.e.thediagonalelementsofGf223
andGmrespectively).Wethenestimatedthevectorcorrelationbetweentheresponse224
calculatedfromourestimatedmatrixandthoseestimatedwithunconstrained(rB=0)and225
constrainedmatrices(rB=1).Next,wecomparedhowconsistentmaleandfemaleresponse226
waswhenevolvingtowardthesameoptimum(concordantselection)andwhenselection227
wasdiscordant.Thiswasachievedbycalculatingthevectorcorrelationbetweenthe228
directionofselectionforeachsexandthecorrespondingresponse(rβ×Δz).229
RESULTS230
Malesandfemalesshowedlittleevidenceforsexualdimorphisminaveragebehavior(all231
Pmcmc<0.57,TableS1,S2).WedidfindevidenceofaG×Sexinteraction,andfemaleshad232
lowerheritabilityandevolvabilitycomparedtomales(meanfemaleh2=0.10;meanmale233
h2=0.47;meanfemaleI=3.04%;meanmaleI=15.73%).Thisisconfirmedbythefact234
thattheadditivegeneticvariancewaslowerinfemalescomparedtomalesforallthree235
behaviors(posteriormedian[89%CI];shelteremergence:ΔVA(females–males)=-50.12[-236
110.18;8.18],Pmcmc=0.92;activity:ΔVA=-43.38[-89.01;-9.19],Pmcmc=0.99;237
antipredatorresponse:ΔVA=-17.63[-44.47;5.45],Pmcmc=0.92)(Figure2,3;TableS3).238
Wealsofoundstrongevidenceforthesex-specificexpressionofbehavioral239
syndromes,withweakergeneticcorrelationsbetweenbehaviorsinfemales.Malesand240
femalesdifferedprimarilyinhowshelteremergencerelatedtoopen-fieldactivityand241
antipredatorresponse(Figure2),whiletherelationshipbetweenopen-fieldactivityand242
antipredatorresponsewasstablebetweensexes(females:rmf=0.65[0.20;0.98],Pmcmc=243
0.94,Pmcmc=0.91;males:rmf=0.64[0.27;0.92],Pmcmc=0.98).Femalesthatstayed244
longerintheshelterhadlowerantipredatorresponseandtravelledfurtherintheopen-245
field(shelteremergence×open-field:rmf=-0.45[-0.92;0.11],Pmcmc=0.86;shelter246
emergence×antipred.:rmf=-0.48[-0.90;-0.01],Pmcmc=0.91).Incontrast,maleswith247
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slowshelteremergencehadhigheractivityandantipredatorresponse(shelteremergence248
×open-field:rmf=0.47[0.06;0.87],Pmcmc=0.93;shelteremergence×antipred.:rmf=249
0.50[-0.01;0.84],Pmcmc=0.92).Inaddition,thecorrelationbetweenmajoraxesof250
geneticvariation(gmax)wassignificantly<1,providinganotherlineofevidenceforthe251
presenceofasex-specificsyndrome(vectorcorrelationr°=0.36[0.00;0.76],Pmcmc≠1=252
0.97)(TableS2,S3).253
254
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255
Figure2.Geneticcorrelationmatrix(Gmf)indicatingsex-specificandcross-sexgenetic256 correlations.Heritabilities(h2)areindicatedonthemaindiagonalandgeneticcorrelations257 (r)ontheoff-diagonalelements.Off-diagonalelementsrepresenteitherthesex-specific258 geneticcorrelations(rfandrminlightgrey)orthecross-sexgeneticcorrelations(rmfin259 darkgrey).BoldindicatesignificantcorrelationsbasedonPmcmc>0.95.Correlationswith260 Pmcmc>0.90areindicatedinitalics.Cross-sexcorrelationssignificantlydifferentfrom1261 areindicatedwithanasterisk.262
263
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Allbehaviorsshowedweaktomoderatecross-sexcorrelationsandwere264
significantlybelow1(shelteremergence:rmf=-0.09[-0.59;0.39],Pmcmc≠1=1.00;activity:265
rmf=0.65[0.22,0.97],Pmcmc≠1=0.94;antipredatorresponse:rmf=0.64[0.26;0.94],266
Pmcmc≠1=0.96)(TableS3).Inaddition,sexeshadbiasedexpressionofdifferenttrait267
combinations,asindicatedbythehighproportionofasymmetryinB—thecross-sex268
covariancematrix(proportionofskew-symmetry=0.25[0.04,0.42]).Thisdegreeof269
asymmetrywasmostpronouncedforthecross-sexcorrelationsbetweenshelter270
emergenceandactivity(ΔCOVA=-21.39[-43.72;-0.56],Pmcmc=0.97)andbetween271
shelteremergenceandantipredatorresponse(ΔCOVA=-14.8[-32.33;1.46],Pmcmc=272
0.95).Incontrast,thecorrelationbetweenactivityandantipredatorresponsedidnotdiffer273
amongsexes(ΔCOVA=-3.02[-11.73;6.73],Pmcmc=0.71)(Figure3).274
Thismeansthathighlyactivefathersproduceddaughterswithfastershelter275
emergence(rmf=-0.50[-0.85;-0.06],Pmcmc=0.94)andhigherantipredatorresponse(rmf276
=0.57[0.12;0.95],Pmcmc=0.93).Incontrast,activemothersonlyweaklycontributedto277
theirsons’shelteremergence(rmf=0.39[-0.14;0.85],Pmcmc=0.85)andantipredator278
response(rmf=0.42[-0.01;0.85],Pmcmc=0.90).279
280
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281
Figure3.Thegeneticstructureoftheboldness-activitysyndromedifferedbothintermsof282 itssex-specificgeneticvariances(A)andcorrelations(B)aswellasitscross-sex283 correlationswithintraits(C)andcross-sexcross-traitscorrelations(D).284
285
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Finally,bysimulatingresponsestoselection,wefoundthatevolutionarytrajectories286
weremoreconsistentwithbehaviorsbeingsexuallyindependentthanwithaconstrained287
expressionofbehaviors.Thiswasthecaseregardlessofwhetherselectionfavoredsex-288
specificoptima(i.e.discordantselection:rB=0= 0.95 [0.73;1.00];rB=1=0.28[0.00;0.56];Δr289
=0.64[0.24;0.98],Pmcmc=0.96)orwhenbothsexeshadthesameoptimum(i.e.290
concordantselection:rB=0=0.95[0.74;1.00],Δr=0.23[-0.04;0.66],Pmcmc=0.95)(Figure291
4).Wenextcomparedtheagreementbetweensimulatedselectiongradientsandpredicted292
responsetoselection(rβ×Δz)betweensexes.Malesandfemaleshadequallyconsistent293
responsestoconcordantselection(femalerβ×Δz=0.72[0.29;1.00];malerβ×Δz=0.75[0.47;294
1.00];Δrβ×Δz=-0.19[-0.67;0.07],Pmcmc=0.88).However,femaleresponsetendedtobe295
biasedawayfromselectioncomparedtomaleswhenselectionwasdiscordant(femalerβ×Δz296
=0.50[0.06;0.95];malerβ×Δz=0.77[0.46;1.00],Δrβ×Δz=-0.27[-0.75;0.11],Pmcmc=0.86).297
Thiscouldmeanthatthemagnitudeofthegeneticconstraintisexpressedmorestronglyin298
males,whichisconsistentwiththeasymmetricnatureofthecross-sexcovariancematrix.299
However,thislastresultshouldbeinterpretedwithcautiongiventhewidecredible300
intervalsaroundtheseestimates. 301
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302
Figure4.Theresponsetoselectionismoreconsistentwithmodelsweresexesevolve303
independently(B=0)thanmodelswheresexesarefullyconstrained(B=1).Thistrendis304
mostpronouncedwhenselectionfavoursoppositeoptimaamongsexes(discordant305
selection).Positivevaluesindicatethattheobservedresponsetoselection(Δz)ismore306
stronglycorrelatedwithresponsestoselectionwhereelementsofthecross-sexcovariance307
matrixaresetto0(B=0)comparedtoresponsestoselectionwherethecross-sex308
covarianceisfullyconstrained(B=1),basedon1,000randomselectiongradientsapplied309
toeach1,000posteriorcovariancematrices. 310
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DISCUSSION311
Ourresultsshowthatmalesandfemalesdiffersubstantiallyintheirbehavioralsyndromes312
atthegeneticlevel.Shelteremergencewasgeneticallyindependentbetweenmalesand313
females,whereasthegeneticconstraintforactivityandantipredatorresponsewas314
strongerbutstilldepartedfrom1.Theabsenceofastronggeneticconstraintlinkingthe315
sexesissurprisinggiventhatthebehaviorswemeasuredarenottypicallyconsidered316
distinctsex-specifictraits.Inthecaseofshelteremergence,across-sexcorrelation317
approachingzeroimpliesthatthesamebehaviorisunderpinnedbycompletely318
independentsetsofgenesinmalesandfemales.Suchgeneticuncouplingmeansthatthis319
behaviorcanfulfilldifferentfunctionsineachsexandcanevolveindependently.Our320
resultssuggestthatsexualconflictmayhavebeenresolvedinthisspecieseveninabsence321
ofobservablebehavioraldimorphism.322
Byapplyingaquantitativegeneticapproach,wewereabletouncovermultipleways323
inwhichsexesdifferedintheirbehaviors.Whilemalesandfemalesdidnotdifferinmean324
behaviors,weuncoveredasignatureofbehavioraldimorphismintheamountofgenetic325
variationexpressedbyeachsex.ThisG×Sexeffectwascharacterizedbyfemalebehavior326
beinglessheritablethanobservedformales.Inourcase,traitswithlowerheritabilities327
alsohadlowerevolvabilities,indicatingthatfemalesarelessresponsivetoselective328
pressuresthanmalesinthisspecies.Thisstrongdifferenceingeneticvariancebetween329
sexescouldresultfromstrongerstabilizingselectioninfemaleserodinggeneticvariation330
intraitsrelatedtoexplorationandrisktakingwhilemaintainingasimilaroptimumineach331
sex.Multivariatestabilizingselectionhasindeedbeenshowntobeanimportantdriverof332
traitevolution,forexampleingenitalmorphologyinarthropods(Arnqvist1997;Houseet333
al.2020).Anotherpossibilityisthatrearingindividualsinlaboratoryconditionswithad-lib334
accesstofoodandsheltercouldalleviatetheresourceacquisitionandallocationtrade-offs335
thatmaybenegotiateddifferentlybyeachsex.Thisexplanationisespeciallyplausibleif336
malesandfemalesmodifytheirphenotypestodifferentdegreeinresponsetocaptivity.337
Notetoothattheenvironmentalcontributiontofemales’behavioralphenotypewasmuch338
greaterthanthatofmales,leavingspacefordifferentialadjustmentofbehaviorbysexesto339
occur.340
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Malesandfemalesdifferedsubstantiallyinhowtheyexpressedaboldness-activity341
syndrome.Contrarytoourpredictions,inbothsexesactivegenotypeswerealsomore342
sensitivetopredatorycues,withnochangetothemagnitudeofthegeneticcorrelation.The343
primarydifferencewasthereforeinhowshelteremergencerelatedtoactivityand344
antipredatorresponse.“Bold”females–i.e.femaleswithfastemergencefromtheshelter–345
hadhigheractivityandantipredatorresponse.Incontrast,activemalesweremore346
sensitivetopredatorcuesandbehavedcautiouslywhenemergingfromtheshelter.This347
resultprovidesimportantinsightintohowmaleandfemalecricketshandlerisky348
situations.Femalemusttravelthroughriskyenvironmentsinordertolocatemates.349
Therefore,boldandactivegenotypesmayneedtocompensatefortheseriskybehaviorsby350
beingmorereactivetothepresenceofpredatorcues.Males,incontrast,stayclosetotheir351
shelterbutproducecourtshipsignalsthatmakethemthetargetofpredatorsandparasites.352
Asaresult,boldermalesmayignorethepresenceofpredatorycuesifthisstrategyyields353
higherfrequencyofencounterswithfemales.Thistypeofriskcompensationstrategyhas354
alreadybeenshowninpreviousstudieswheremaleswithmoreattractivesongsstay355
longerinshelters(Hedrick2000).356
Ourfindingsthatmalesandfemalesdifferedinthegeneticexpressionbehavioral357
syndromesandthatcross-sexcorrelationsareuncoupledsuggestthatrisk-takingis358
regulatedbydifferentphysiologicalpathwaysineachsex.Incrickets,severalmonoamine359
neurohormonesareinvolvedintheregulationofmultiplebehaviorstiedtoa“fightor360
flight”response,includingaggression,courtship,dispersalandresponsetosimulated361
predationexposure(Adamoetal.1995,2013;StevensonandRillich2016;Adamo2017;362
Lundgrenetal.2021).However,experimentstendtoeitherfocusonmalesexclusivelyor363
arenotdesignedtoaddresssex-differencesinphysiologicalmechanisms.However,sex-364
differencesinasimilaraxisofvariation,theproactive/reactiveaxis,havealsobeen365
describedinseveralvertebratetaxa(Kokrasetal.2012;Immonenetal.2018).366
Thegeneticstructureofbehavioralsyndromesishighlyconservedinthisspecies,367
evenacrossisolatedpopulations(Royautéetal.2020).Thisindicatesthatbehavioral368
syndromesmaynotvarymuchwhenexposedtodifferentselectivepressures.Instead,369
geneticconstraintsresultingfrompleiotropywasthemorelikelyexplanationsforthe370
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presenceofbehavioralsyndromeinthisspecies.Here,weshowthatbehavioralsyndromes371
differedmorestronglybetweensexesthanamongpopulations.Alikelyexplanationisthat372
malesandfemalesexpresssex-specificbehaviorsregardlessofthepopulationoforigin.As373
aresult,selectionmaybemorelikelytodifferbetweensexesthanbetweenpopulations.374
Whilecomparisonsofdifferencesinselectionamongsexesandpopulationsarescarce,375
previousstudiessuggestthatsexuallydiscordantselectioniscommoninthewildand376
tendstobestrongerintraitsinwhichsexualdimorphismispronounced(Coxetal.2009).377
Whilerarelyinvestigated,sexspecificdifferencesinbehavioralsyndromeshave378
beendemonstratedinsomespecies.However,mostofthesestudieshavefocusedon379
comparisonsofbehavioralrepeatabilitiesbetweenmalesandfemalesinsingletraits380
(Jenkins2011;Debeffeetal.2015)ratherprovidingabroaderexplorationofmultivariate381
patternsofcross-sexcorrelationinbehavioraltraits,aswedidhere.Interestingly,(Hedrick382
andKortet2012)previouslyidentifiedsexdifferencesintherepeatabilityofshelter383
emergenceinaseparatepopulationofG.integer.Contrarytowhatwedetected,maleshad384
lowerrepeatabilitycomparedtofemales.Notethatrepeatabilityandheritabilityarenot385
directlycomparablebecauserepeatabilityalsoincludessourcesofvariationduetothe386
“permanentenvironment”whileheritabilityonlyincludesadditivegeneticvariation.More387
recentlyseveralstudieshavealsocomparedsyndromestructureamongsexeswithmixed388
results.Somestudiesreportedlargedifferencesinbehavioralsyndromesbetweenmales389
andfemales(Fresneauetal.2014;Hanetal.2015;Royauté2015;Wayetal.2015)while390
otherssupportaconservedsyndromestructurebetweensexes(Michelangelietal.2016;391
Gouletetal.2021).Ourresultssupplyanadditionallineofevidenceinfavorofsex-specific392
syndromes.393
Thereisonlylimitedexplorationofmultivariatepatternsofcross-sexcorrelationin394
behavioraltraits.Moststudiesreportedfrom(Poissantetal.2010)concernsingletraits395
andpointtostrongcross-sexcorrelationswithrelativelyweakdimorphismforbehavior.396
Themajorityoftheseestimateswere,however,fromstudiesinterestedinsexualselection,397
with<4%ofestimatescomingfromexplicitlybehavioralstudies.Becausewealso398
estimatedthecross-sexcorrelationattheadditivegeneticlevel,wewereabletodetermine399
thatbehavioraltraitsmaybelessconstrainedbysexthanpreviouslythought.Indeed,our400
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meanestimateforrmfwasmuchweakerthanobservedinpreviousstudiesevaluatingintra-401
locussexualconflictsinbehavior(meanrmf=0.46vs.0.77,Poissantetal.2010).Our402
resultssuggestthatbehavioraltraitsmaycommonlyfulfilldifferentfunctionsbetween403
sexesandshouldthereforebeanalyzedasseparatetraitsbetweenthesexesinbehavioral404
syndromeandanimalpersonalitystudies.405
Veryfewstudieshavebeenabletoestimatethegeneticcontributionofsexesto406
behavioralsyndromesaswehavedonehere.Intheorb-weavingspiderNuctenea407
umbratical,cross-sexcorrelationsforactivityandaggressionwereinthesamerangeasour408
estimatesforactivityandantipredatorresponse(rmf=0.50)(Kralj-Fišeretal.2019).In409
Gryllusbimaculatus,whichiscloselyrelatedtoG.integer,explorationandaggressionare410
morestronglycorrelatedinfemalesandthesetraitshaveasymmetriccontributionsacross411
sexes(Hanetal.2019).However,cross-sexcorrelationswithintraitswerequalitatively412
strongerthanobservedinourstudy(meanrmf=0.70vsmeanrmf=0.46),pointingtoa413
strongergeneticconstraintbetweensexesthanweobservedinGryllusinteger.Finally,414
Whiteetal.(2019)showeddifferencesbetweensex-specificcovariancesinguppiesto415
similarG.integer.However,theyreportedamuchweakersignalofasymmetryinB.The416
factthatthesefewstudiesdifferwidelyinconclusionsshowsthatthereisnoconsensusyet417
onhowbehavioralsyndromesdifferbetweensexesandevencloselyrelatedspeciesmay418
showstrongdifferencesintheexpressionofbehavioraldimorphism.419
Otherstudies,conductedprimarilyonmorphologicaltraits,pointtostrong420
constraintsimposedbygeneticcross-sexcovariances(Gosdenetal.2012;Gosdenand421
Chenoweth2014;SztepanaczandHoule2019).Inourcase,theconstrainingeffectofcross-422
sexcovarianceswasweakatbestandresponsestoselectionweremoreconsistentwith423
independentevolutionarytrajectoriesforeachsex.Thisissimilartoapreviousstudyon424
sexuallydimorphicornamentsinbrownanoleswhichshowedthatthecross-sex425
covarianceamongornamentsdidnotsubstantiallyconstraintheevolutionofdimorphism426
(Coxetal.2017).427
Wefoundahighdegreeofasymmetryinthecross-sexcross-traitscomponentsof428
thegeneticcovariancematrix.Inparticular,maleactivityhadastrongercontributionto429
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femaleshelteremergencethanfemaleactivityonmaleshelteremergence.Thistypeof430
asymmetriccontributiontothephenotypeisexpectedtobiasresponsesawayfrom431
selection.InDrosophilaforexample,wingshapeevolutionisprimarilyshapedbycross-sex432
covariancesforthesametrait(i.e.thediagonalelementsofB)ratherthancross-sexcross-433
traitcovariances(SztepanaczandHoule2019).Thiswasthecaseeventhoughupperand434
lowerelementsoftheBmatrixfrequentlyhadoppositesignsanddespiteageneral,though435
weaker,signalofasymmetrysuchaswereporthere(5%vs.25%).Despitestrong436
asymmetryinourestimateofcross-sexcovariances,wefoundonlyweakevidencefor437
biasedresponsestoselection.Instead,oursimulationsoftheresponsestoselections438
showedthattheevolutionofbehavioraldimorphismswasmoreconsistentwithscenarios439
inwhichsexesaregeneticallyuncoupledandallowedtoevolveindependentlycomparedto440
afullyconstrainedcross-sexgeneticarchitecture.Thismeansthattheindependent441
evolutionarytrajectoriesbysexeswereportarelikelyaresultoftheweakcross-sex442
correlationswithintraitswedetected(meanrmf<0.50).443
Weshowthattraitsinvolvedinstudiesofanimalpersonalityhaveasex-specific444
geneticarchitecture.Thesebehaviorsaregeneticallyuncoupledbetweensexesandallow445
sexestofollowindependentevolutionarytrajectories.Ourresultsareintriguingbecause446
theorypredictsthatcross-sexcovarianceswillactasconstraintsandlimittheabilitiesof447
sexestoreachtheiroptimum.Thetypeofgeneticindependencewefoundsuggestsapast448
historyofdiscordantselectionthathasstronglyshapedbehavioraldimorphismandhas449
resolvedsexualconflictinthisspecies.450
451
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