Matingconflictinprimates:infanticide,sexualharassmentandfemalesexualit - PDF document

141 Matingconflictinprimates:infanticide,sexualharassmentandfemalesexualityCARELP.VANSCHAIK,GAURIR.PRADHAN&MARIAA.VANNOORDWIJKINTRODUCTIONInavarietyofmammalsandafewbirds,newlyimmigratedornewlydominantmalesareknowntoattackandkilldependentinfants(Hausfater&Hrdy,1984;Parmigiani&vomSaal,1994;vanSchaik&Janson,2000).Hrdy(1974)wasthefirsttosuggest 142 Second,weturntosexualharassment,i.e.maleaggressiontargetedagainstsexuallyactive(‘oestrous’)females,andshowhowitcanbeviewedasanexpressionofmatingconflictbetweenthefemaleandthedominantmale.Becauseharassmentisremarkablyconcentratedincatarrhineprimates,wethenexaminesexualbehaviourandphysiologyinthatradiationrelativetospeciesvulnerabletoinfanticideinotherprimateradiations.Weconcludethatvariousfeaturesofcatarrhinesexualitycanplausiblybeunderstoodasresponsestothisharassmentintheevolutionaryarmsrace,althoughthistopicrequiresmuchadditionalwork.MalesasprotectorsBeforediscussingaspectsoffemalesexualbehaviourasacounterstrategyagainstinfanticidesomeattentiontotheassociationwithlikelysiresisneededinordertoexplainwhyfemalesexualbehaviourtendstoleadtoprotectionbyone,orsometimesmore,likelysires.Protectionofinfantsbylikelysiresismadepossiblebytheyear-roundmale-femaleassociationfoundinvirtuallyallprimatesinwhichfemalescarrytheirinfants(vanSchaik&Kappeler,1997).Atleastinmulti-malegroups,likelysirestendtobeinclosespatialproximitywithinfants(Janson,1986;Pauletal.,2000),andnumerousreportsindicatethatthesemalesactuallydefendtheinfantsagainstattacksbyothermales(Borriesetal.,1999;review:vanSchaik,2000a).Infanticideoftenhappenswhentheformerdominantmale,themostlikelysireofmostinfantseveninmultimalegroups(reviewsinCowlishaw&Dunbar,1991;Paul,1997;vanNoordwijk&vanSchaik,thisvolume),iseliminatedorincapacitated.Infanticidalattackscouldhavebeenprovokedbyhisexperimentalremoval,eitherinthewild(Sugiyama,1966)or(quitefrequently,andinadvertently)in Wefollowtheuseof"harassment"asinSmuts&Smuts(1993),whichdiffersfromthatinClutton-Brock&Parker(1995).captivity(e.g.,Angst&Thommen,1977),orbynaturaldemographicprocesses(e.g.,Steenbeek,1996).Inallthesesituationsinfanticidebythenewmaleiscommonlyobserved.Conversely,whenoneinterpretsthesocialcontextofalldirectlyobservedcasesofinfanticideinwildprimatesthatoccurredspontaneously,thegreatmajority(85%of55cases:vanSchaik,2000a)isassociatedwithachangeinthedominantpositioninthegroup,whichinvolvestheoustingorweakeningoftheformerdominant.Relativetakeoverrate(correctedforvariationininterbirthinterval)alsoexplainsmuchofthevariationininfanticideratesinwell-studiedpopulations(Janson&vanSchaik,2000).Thus,dominantmalesareeffectiveprotectorsofinfantsaslongastheyarenotoustedorincapacitated.Femalesshouldthereforebeexpectedtomatepreferentiallywiththesepowerfulmaleswheneverfemalescanbeconfrontedbymaleswhoareunlikelysires.FEMALESEXUALBEHAVIOURASACOUNTER-STRATEGYTOINFANTICIDETheoryHrdy(1974,1979)hypothesizedthatfemalesexualbehaviourinprimatespeciesvulnerabletoinfanticidehasbeenmodifiedtoreducetheriskofinfanticidebymales.Thebasisfortheargumentisthatprimatemales,likethoseofthemajorityofmammals,donotrecognisetheiroffspring(initselfpossiblytheproductoffemale-drivenevolution),andthereforemustrelyonindirectindicatorsofpaternityprobability.Theseindicatorshavebeenstudiedexperimentallyinrodents(vomSaal,1984;Perrigo&vomSaal,1994),butnotinprimates,wheretheindicatorshavetobepiecedtogetherbyanalysingindividualcases(reviewedinvanSchaik,2000a).Primatemalesarethoughttouserulesofthumbsuchasthequalityoftheirsexualexperiencewiththefemale(i.e.matingfrequencyrelativetoher 143 attractivity[her‘stimulusvalue’tothemale])weightedforhermatingfrequencywithothermales,theintervalbetweenmatingsandbirth,andperhapsthecontinuityofassociationbetweenmaleandfemale.Weassumethatnaturalselectionhasfavouredmalesthatusethoserulesofthumbthatyieldtheclosestaveragematchwiththeprobabilityofpaternity.Conceptually,wecandistinguishtwokindsofmatingsbyfemalesthatmayreducetheriskofinfanticide.First,bymatingpolyandrouslyinpotentiallyfertileperiods,femalescanreducetheconcentrationofpaternityinthedominantmale,andspreadsomeofittoothermales,sothatlong-termaveragepaternityprobabilitieswillbesomewhatbelow1forthedominantandsomewhatabove0forthesubordinates.Second,bymatingduringperiodsofnon-fertility(e.g.duringpregnancy;situation-dependentreceptivity:Hrdy,1979),afemalemaybeabletomanipulatetheassessmentbythevariousmalesoftheirpaternitychances,althoughsheobviouslycannotchangetheactualpaternityvaluesallocatedtothevariousmales.Thisdistinctionistheoreticallyuseful,butthevariousplayersareprobablyquiteunawareofit,withmalesmerelyrespondingtovisual,olfactoryandbehaviouralstimuliemanatingfromthefemalethatcreatevariationinherattractivity(Snowdon,thisvolume;Zinneretal.,thisvolume).Ifmalebehaviourdependsontheirestimateofpaternity,thissexualbehaviourcanbeeffective.Hrdy(1979,1997)reasonedthatwheremaleshavealow,butnon-zeroprobability,theywouldrefrainfromattackingtheinfant,whereastheywoulddefenditwhentheestimateishigher.EmpiricalevidenceThebasicpredictionisthatfemalesthatarevulnerabletoinfanticidebymalesshouldbeactivelypolyandrouswheneverpotentiallyinfanticidalmalesarepresentinthematingpool(i.e.thesexuallymaturemalesinthesocialunitornearbywithwhomthefemalecanmateinprinciple).Thereisampleevidencethatprimatefemalesinvulnerablespeciesactivelypursuepolyandrousmatingsandthattheyoftenengageinmatingswhenfertilizationisunlikelyorimpossible(Small,1993;Manson,1995;summarisedinvanSchaiketal.,1999).Indeed,femalesoftentargetlow-rankingorperipheralmalesreluctanttomateinthepresenceofdominantcentralmales,especiallyduringpregnancy(e.g.,Watts,1991;Wallis&Bettinger,1993;Gust,1994).Therearetwosourcesofmoredirectempiricalevidencetoassesswhetherthesederivedfeaturesofprimatesexualbehaviourareindeedanevolutionaryresponsetovulnerabilitytoinfanticide:(i)directsexualresponsesbyfemalestochangesingroupcompositionormalestatus;and(ii)broadercomparisonsofsexualbehaviourbetweentaxathatareorarenotvulnerabletoinfanticidebymales.Inspeciesvulnerabletoinfanticide,femalesoftenrespondtochangesinthemalecohortofagroupwithimmediateproceptivityandeffectivelysolicitmatingswiththenew(-lydominant)male(Struhsaker&Leland,1985;Cords,1988;Sommeretal.,1992;Swedell,2000),evenshowingrapiddevelopmentofsexualswellingsinspeciesthathavethem(Stein,1984;Colmenares&Gomendio,1988;Zinner&Deschner,2000).Invariouscatarrhineprimatesinwhichmultiplemalestemporarilyenteragroup(‘maleinflux’),matingperiods(durationofoestrus)arerelativelylongercomparedtoperiodswithoutmaleinfluxes(e.g.,Cords,1984,1988;Takahataal.,1994).Similarly,inseveralspecieswithbothsinglemaleandmulti-malegroups,femalematingperiodsarelongerinmulti-malegroups(Brockman,1999;Heistermannetal.,2001).Interspecificcomparisonsprovidesimilarsupport:vanNoordwijk&vanSchaik(2000)foundacleartrendtowardmorepolyandrousmatingamongprimateandcarnivorespeciesvulnerabletoinfanticiderelativetothosethatarenotvulnerable.Post-conceptionmating,whileinfrequentlyreported,wasalsoconcentratedinthoseordersofmammals 144 whereinfanticideistobeexpectedbasedontheirlifehistory.Withinprimates,post-conceptionmatingsarefoundpredominantly,andperhapsexclusively,inspeciesvulnerabletoinfanticide(vanSchaiketal.1999).However,onepredictionwasnotupheld:inmostothermammalsnosystematictrendtowardslongermatingperiodsinspeciesvulnerabletoinfanticidewasapparent(vanNoordwijk&vanSchaik,2000).Wewilllatershowthatthispredictionisonlyexpectedwheremalesareabletoforcematings.Adifferentsourceofevidencefortheeffectivenessofsexualbehaviourinreducingtheriskofinfanticideisthelowerrateofinfanticideinmulti-malegroups,whencontrollingfortheeffectoftakeoverofdominance(Janson&vanSchaik,2000).Tosomeextentthisreductionisobviouslyduetomaleprotectionbecauseinmulti-malegroupsdefeateddominantstendtoremaininthegroup,atleastforawhile(e.g.,vanNoordwijk&vanSchaik,1988;Perry,1998;Borries,2000).However,sexualstrategiesareimplicatedaswellbecauseweoccasionallyseeprotectionoftheinfantbyotherresidentmales(e.g.,Borriesetal.,1999),orabsenceofattacksbythenewdominantwhowasalong-termresidentandhadmatedbeforewiththemothers(seebelow).AproblemAremarkableaspectofinfanticideisthat–especiallyinmulti-malegroups–onlyasmalltomoderateproportionoftheinfantstypicallyendsupgettingkilled.Whilethishighprobabilityofsurvivalprobablyhasmultiplesources,itisreasonabletoattributeatleastsomeofittothefemale’ssexualbehaviour.Yet,thelatter’seffectivenessissomewhatsurprisingbecausepaternityisaconstant-sumgame,inthateachinfantcanhaveonlyonesireandthatthelong-termaverageprobabilitiesoffertilisationofalltheplayersmustaddupto1.Afemalethereforefacesaconsiderablechallenge.Ontheonehand,byraisingthelong-termprobabilityofsubordinatemalesthroughtheirmatingbehaviour,shereducestheriskofinfanticidebecausethesemalesarelesslikelytoattacktheinfantwhentheybecomedominant.Ontheotherhand,thisbehaviourmustreducethepaternityprobabilityofthedominantmale,andhencemakeitlesslikelythatthedominantwilldefendtheinfantagainstmalesenteringfromtheoutside(cf.Symons,1982).Itisthereforenotimmediatelyobviousthatsexualbehaviourcouldeverachieveanoptimalbalanceandreduceoverallrisk.Here,wewillpresentanovelexplanationfortheeffectivenessofsexualbehaviour.Doingso,however,requiresthatwefirstdeterminetheconditionsinwhichnaturalselectionfavoursinfanticidebymales(cf.vanSchaik,2000a).Whenisinfanticidefavouredbynaturalselection?Inaspeciesinwhichinfanticideadvancesthefemale’snextconception,andinasituationinwhichamalecanbeconfidentthat (i.e.henevermatedwiththefemale,where istheprobabilityofhavingsiredtheexistinginfant),infanticideisobviouslyanadvantageousstrategy,provideditcanbecommittedatlowcost.However,ifthemalehasamatinghistorywiththefemale,amorequantitativepredictionisneeded.Inordertodevelopthisprediction,wecomparetheexpectedmeannumberofoffspringsiredbyadominantmaleduringhisperiodofdominance(tenure)undertwoscenarios:withandwithoutinfanticideuponassumingthedominantposition.Denotetheeffectivetenureperiodofanon-infanticidaldominantmaleas ,i.e.theperiodbetweentheconceptionofthefirstinfantsiredduringthenewtenuretotheendofthemale’stenure.Iftheregularinterbirthintervalis ,andtheinterbirthintervalfollowinginfanticideis ,thetimegainedbyaninfanticidalmaleis.Thus,theeffectivetenureofaninfanticidalmaleis.Nowwecancalculatethebenefitofthetwostrategies( 145 and,fornon-infanticideandinfanticide,respectively).Thesebenefitsintermsofexpectednumberofinfantsare(vanSchaik[2000a],whichoverlookedinfantssiredbynon-infanticidalmalesbeforebecomingdominant): BpP T i B p P =Š+where istheprobabilityofsiringinfantsduringtenure,assumingthatthisprobabilityisconstantregardlessofwhetherthemalecommitsinfanticide.Then,thenetbenefitofcommittinginfanticideis: ttT BpPp Š=Š+ŠŠ Thusispositive(giventhat)if Inequality(1)ignoresanycoststoinfanticide(seevanSchaik[2000a]fordiscussion).Intheaverageprimatespecies,themaximum isaround0.5,whichisattainedwhenanewborniskilled.Inthiscase.Astheinfantgetsolder, hastoincreasetomakeinfanticideadvantageoustothemale.Fortheobservedmeanvaluesof between0.25to0.32(seeabove),infanticideisadvantageousif isgreaterthanapproximately OptimummaledecisionsInequality(1)showswheninfanticideisexpected,butwecannotassumethatmaleshaveperfectestimatesoftherelevantparameters.Wemustthereforetranslatethesecriteriaintodecision-makingrulesformales.Somecasesaresimple.First,ifthenewlydominantmalenevermatedwiththefemale,and,theruleiseasy.Indeed,infanticideiscommonlyseenafteranewmaleimmigranttakesoveragroup(e.g.,Steenbeek,1996;vanSchaik,2000a).Second,ifthemalehasasexualhistorywiththefemalebuthisestimateof isverysmall,infantagemattersbecausethebenefitsdecreaseasinfantsgetolder(cf.Crockett&Sekulic,1984;Sommer,1994;summarisedinFig.2.1invanSchaik,2000a).Inmulti-malegroups,however,amalehasgenerallymatedwiththefemalebefore,andoptimumdecisionmakingmaybemoredifficult.Themaleisforcedtouseindirectindicatorsbasedonhissexualhistorywiththefemale(seeabove)toproduceestimatesthatwilltendtobehighlyimprecise,exceptwhenthemalecouldmonopolisemostmatingswithsexuallyhighlyattractivefemalesorwhenhecouldgetonlyveryfewmatingswhenshewasnotveryattractive.Frequentpolyandrousmatingduringbothperiodsofovarianactivityandperiodsofpatentinfertility(e.g.pregnancy)couldhavetwoconsequences.First,itmayleadtoanincreaseintheestimatedpaternityprobability(henceforth ),especiallyifthemalesarenotfullyinformedaboutthefemalematingactivitywithothermales.Thus,especiallybymatingfrequentlyattimesofnon-fertility,femalesmaymanagetoincrease ofespeciallylow-rankingmales,producingasumoftheseestimatesgreaterthan1(obviously,theactualpaternityprobabilitiesstilladdupto1).Second,frequentpolyandryshouldleadtogreatuncertaintyofeachmale’s .Onemustassumethathigherquantityofmatingscancompensatetosomeextentforlowerquality(i.e.thefemalewaslessattractive).Wesuspectthatnon-dominantmaleshaveveryimpreciseestimatesoftheirchancesofpaternity.Inasituationofhighuncertaintyastothevalueof itmaybeimpossibletofindoptimumdecision-makingalgorithms. 146 Table8.1.Thepayoffsofdecisionsmadebynewlydominantmaleswithrespecttoinfants,dependingonwhetherthemalehadsiredthisinfantornot.textforexplicationofvariables Decision:FatherNotfatherKill T i P tn i P tn Notkill T P t n + T P t n Anewlydominantmalemaydecidetochoosetheoptionthatmaximizesmeanfitness.Ifuncertaintyoverthevalueof approachesignorance,hisbestguessmaybethat ,anditiseasytoshowthatnotkillingtheinfantisonaveragethebestoption(seeTable8.1).However,sinceagivenmaleactuallydidordidnotfathertheinfant,inacaselikethis,anewlydominantmalemayactuallymaximisehisfitnesspayoffbyavoidingcostlymistakes(cf.Resnik,1987,p.28),i.e.minimizetheriskoflosingalargeportionoffitness(cf.riskavoidanceinforaging:Stephens&Krebs,1986).Anewlydominantmalecanmaketwokindsofmistakes:(i)hecankillaninfantthathehadactuallysiredbeforebecomingdominant,thuslosingoneinfantfromhistotalnumberproduced;and(ii)hecanrefrainfromkillinganinfantthathedidnotsire,thuslosingtimetothenextconceptionoftheinfant’smother.Thesetwoerrorshavedifferentcostsattachedtothem.Table8.1presentsthepayoffsofthetwopossiblemaledecisions(killvsnottokill),undertwodifferentconditions(maleactuallyfatheredtheinfantvsdidnot).Thecostofthemistake,i.e.themalekillinghisowninfant,relativetotheoptimumtacticofrefrainingfromkillingit,isthedifferencebetweenkillingitandnotkillingit: 111Ttt P t =Š+ŠŠ t t P =Š+Thusthecostofkillinghisowninfantisintherange 211 Š

Š(theseareininfantunits).Ontheotherhand,ifthemaledidnotsiretheinfant,thecostofnotkillingtheinfant(relativetotheoptimumtacticofkillingit)is:Thecostofnotkillinganothermale’sinfantisintherange 120. Š

Committingthefirsterror(killingone’sowninfant)hasfargreatercosts( 1 C )thancommittingtheseconderror(notkillingsomeothermale’sinfant; ).Hence,iffemalematingtacticshaveconfusedpaternityestimatestothepointofnear-ignorance,anewlydominantmalewilldobettertoavoidthemorecostlyerror,andshouldthusrefrainfrominfanticide.Thiseffectofdeceptivefemalematingscouldexplainwhyinfanticideisnotalwaysseeninconditionswhereitmightbeexpected.Weassumethatthedominantmalesusuallyhavelessuncertaintyconcerningtheirdecisionwhethertoprotectvsnottoprotectaninfant,becausetheirestimatesofpaternitywilltendtobecloseto1.However,iftheyalsofaceconsiderableuncertaintyvergingonignorance,theyshouldalsoavoidmakingthecostliermistake.Table8.2providesthepayoffsofthedominantmale’sdecisionsforthetwopossiblestates(fathervsnon-father).Thecostsofnotprotectinganinfantthatthemaleactuallysiredis:3()2 sscs =ŠŠŠ=Š+(where=probabilityofinfantsurvival;and=costofprotection,bothexpressedininfantunits),whereasthecostofprotectinganinfantthathedidnotsireis: = ŠPtTn PtttninŠŠ= PtttTninŠ+ 147 Table8.2.Thepayoffsofdecisionsmadebycurrentlydominantmaleswithrespecttoinfantsdependingonwhetherthemalehadsiredthisinfantornot. Decision:FatherNotfatherProtect c Š Notprotect 0 c =ŠŠ=ŠFor (averyreasonableassumption),thedecisionnottoprotecttheinfantwhenthedominantmaleistheactualsireisthecostlierone.Thus,ifadominantmaleissouncertainofhispaternityastobevirtuallyignorantofitsvalue(i.e.,ifhisestimateiscloseto0.5),thenhisbestdecisionistoprotecttheinfantwhenitisatrisk,uptoapoint.Italsosuggests,however,thatmalesfacinghighercostsofprotection,i.e.lesspowerfulorinjuredmales,arelesslikelytoprotectinfants,ortoprotectwithlesserintensity,eveniftheyhavematedextensivelywiththemother.Asinthecaseofthenewlydominantmale,thisapproachleadstothesameconclusionastheonethatmaximiseshismeanfitness(assumingthat ConclusionsfromthemaledecisionmodelThemainconclusionfromthisanalysisisthatfemalepolyandryandmatingduringnon-fertileperiodsservetoraisetheestimatedpaternityprobability( valuesforallmalesinvolved,andmakingtheirsumexceed1.Polyandrymayalsoconfuse tothepointthatthemales’bestcourseofactionistorefrainfromkillinginfantsandtoprotectthemiftheyhavematedextensively,eveniftheyactuallydidnotsirethem.Thus,femalesexualbehaviourmayservetoovercometheconstant-sumnatureofthepaternitygame.Unfortunately,developingconvincingtestsoftheseideasisnoteasy,especiallybecauseincompleteinfanticidalattacksbynewlydominantmalesandthereducedratesofinfanticideinmulti-malespeciescanhavemultiplesources,asnotedabove.Nonetheless,webelieveitismeaningfultotranslatetheconditionsinwhichnaturalselectionshouldfavouroneactionoveranotherintotheactualdecision-makingprocessesofanimals.However,iftheinterpretationadvancedhereiscorrect,aclearpredictionfollows.Itisinthefemale’sinteresttokeepindividualmalesguessingastotheextenttowhichothermaleshavealsomatedwithher:thelowertheperceptionofthatfrequencythehigheramale’s ,hisestimateofhisownpaternitychances,shouldbe.Hence,femalesshouldbelikelytomatediscreetly,especiallywithsubordinatemales.Wewilldevelopthesamepredictionfromaconsiderationofmatingconflict(seebelow).Toreachthisconclusionwehaveassumedthatthefemalecanbiasthevaluesoftheseestimatesindirectionsfavourabletoher,implyingthatnaturalselectionwasunabletoequipmaleswithbetterassessmentrulesthantheonestheycurrentlyhave.Thus,femalesexualitymayhavebeendesignedtowithholdpotentiallyusefulinformationfrommales.Physiologicalworkdonefromthisperspectivemightberewarding.SEXUALHARASSMENTASANEXPRESSIONOFMATINGCONFLICTMatingconflictbetweenthesexesisnowrecognisedasanintrinsicpartofsexualselection(Hammerstein&Parker,1987).Oneaspectofitconcernsintersexualconflictovertheidentityofeachindividual’smates.Especiallyinsomemammals,thiskindofmatingconflicthasfoundexpressioninsexualcoercionoffemalesbystrongermales.Smuts&Smuts(1993)definedsexualcoercionandconsideredtwocomponents:infanticideandsexualharassment.Manystudentsofprimatebehaviourhavereportedharassmentoraggressiverestrictionofmovementsofsexuallyactive(‘oestrous’)femalesbymales,especiallyhigh-rankingones,sometimestothe 148 00.20.40.6paternityprobability(p)impactoninfantsurvivalFig.8.1.Theimpactofthepaternity( )ofamaleoninfantsurvival.Therelationshiphastheform )(1)(1) gpkAp=ŠŠŠ;theparameterschosenare = 1 = 2 .Asthemale’spaternityincreases,theimpactvariesfromattacktotolerancetoprotection.At ,theinterceptonthey-axisis( ),whichisthemaximumnegativeimpactbyanon-sireonthesurvivaloftheinfant.pointthatthefemaleisinjuredorevenkilled(Smuts&Smuts,1993;chimpanzees:Goodall,1986,p.452;Matsumoto-Oda&Oda,1998;macaques:Chapais,1983;Huffman,1987,1992;Manson,1992,1994;Soltis,1999;hamadryasbaboons:Kummer,1995).Althoughinfanticideisseenbysomeasanextremeformofharassment(Smuts&Smuts,1993),thetwoarenotoftentreatedasbeingdirectlyinterrelatedphenomena.Here,wedevelopamodeltoshowthatatleastsomeofthesexualharassmentinprimatesisdirectlylinkedtofemales’attemptstobepolyandrous.TheoryAssumeamulti-malegroupofaprimatespeciesinwhichfemalesarevulnerabletoinfanticidebymales.Onemaleisdominantandwillguardafemalewhensheisinoestrus,butothermalesarearoundandalsointerestedinmatingwiththefemale.Itisinthefemale’sinteresttodilutethepaternitychancesofthedominantmaleinordertoreducetheriskofinfanticidebymatingpolyandrouslywithothermalesinthegroup,oroccasionallyeveninanadjacentgroup,incaseoneofthemtakesovertopdominanceorouststhecurrentdominant(Hrdy,1979;Hrdy&Whitten,1987;Small,1993;vanSchaiketal.,1999;Soltisetal.,2000;Heistermannetal.,2001).Onemightexpectthatthedominantmalewouldalsobenefitfromreducingtheinfant’sriskofinfanticide.However,wewillnowshowthatthedominantmale’sprobabilityofpaternitythatmaximiseshisfitnessishigherthanthatpreferredbythefemale,andthatheisthereforeexpectedtoattempttopreventmatingsbythefemalewithothermales.Thusamaleisnotonlyincompetitionwithothermales,hemayalsohaveaconflictofinterestwithhismate(s).Amale’sprobabilityofpaternity, ,isthelong-termaverageproportionofinfantssiredbyamaleinsimilarconditions.Weassumethatthevalueof relatedtoamale’sassessmentofit,althoughthisrelationshipmaybeimprecise(seeprevioussection).Ingeneral,amale’sattitudetowardtheinfantisafunctionof ,sothatwithincreasingvaluesof themalechangesfromattack(ifgivenanopportunitytodosoandifprospectsforfuturematingaccesstothefemaleexist),toindifferenceortolerance,andfinallytoanincreasinglystrongtendencytowardprotection(Hrdy,1979).Wecanrepresenttheimpactoninfantsurvivalofthesechangingattitudesas ,withnegativeeffectsatlow p andincreasinglypositiveeffectsas increases(seeFig.8.1).Weexpect toincreasemonotonicallywith ondomain[0,1]andsaturateat ThefunctioninFig.8.1canbeexpressedas: ()(1)(1) gpkAp=ŠŠŠwhere (integer, )isashapeparameterthatdetermineshowfast risesandhowsoonitsaturatesas increases,and and arepositiveconstants(suchthat ).Thevalueof isthemaximumpositiveimpactofthelikelysireontheinfant’ssurvival,whereas canbeseenasthemaximumnegativeimpactofanon-sire(theY- 149 interceptinFig.8.1isat ).Theassumptionof iscriticalfortheresultbelow,butinmakingit,wefollowpreviousanalysesofmaleparentalcare(Harada&Iwasa,1996).Itimpliesthatas increases,thecostsofmaleprotectioneffortsarealsolikelytoriseduetoincreasedcompetitionwithotheractivitiesorincreasedriskofinjury,leadingtoarelativeslowdownininvestmentin,andthuseffectivenessof,protection(inotherwords,onemustassumeprotectioneffortstosaturate).Thequestionisatwhatvalueofthedominantmale’s (herecalled toavoidconfusion)thefitnessofthedominantmaleandofthefemalearemaximised.Ingeneral,femalefitness, ,ismaximisedwhentheinfant’ssurvivalismaximised,assumingtherearenoothermajoreffectsonfitness,suchasvariationinmaleintrinsicgeneticqualityorrelatednesstothefemale.Ontheotherhand,thedominantmale’sfitness, F ,ismaximisedwhen ismaximised,whereasthefitnessofasubordinatemale( F ,ormorepreciselythehighestrankingamongthem)ismaximisedwhen (1)* ismaximised.Wewillnowdevelopexpressionsfor D M F and F Weassumethatinfantsurvivalisafunctionof ,butweightedforthedominantmale’seffectivepower),aswellasafunctionof (1) ,i.e.thestrongestsubordinatemale’spaternity, ,butweightedforhiseffectivepower.Thisyields: ()(1)(1) F gqgq=Š+Š {()(1)(1)} DMF qFqgqgq==Š+Š (1){()(1)(1)} qgqgq=ŠŠ+ŠTheparameterestimatesthemaximumstrengthofthestrongestothermaleinthegrouporthevicinity(i.e.withinthefemale’spotentialpoolofmates).Thisstrengthparameterisbestinterpretedasthelikelihoodthatthismalewillsuccessfullychallengethecurrentdominantinthenearfuture(andthusalsoprotecttheinfantinthefuture),hence .Itspaternityprobabilityofdominantmale(q) 0.20.40.60.8strongestsubordinatemaledominantmaleFig.8.2.Thefitnessofthefemale,dominantmaleandthestrongestsubordinatemaleasafunctionofthepaternity ofthedominantmale(Eq.2-5).Theoptimalfitnessforeachofthethreeisatdifferentvaluesof ,whichcannotbesatisfiedsimultaneously,reflectingaconflict.complement,1,representstheprobabilitythatthedominantmalewillbeabletowithstandchallengestohisdominantposition,andhencealsohisabilitytoprotecttheinfantagainstinfanticidalattacksbyanyofthesemales(oryetothers).Figure8.2illustratestheresultingmatingconflict:thedominantmale’sfitnessismaximisedatahighervalueof comparedtothevalueof atwhichthefemale’sfitnessismaximised.WedidnotfindanalyticalsolutionstoEqs.3-5satisfyingallvaluesof .However,for ,thevalueof atwhichthefemale’sfitnessismaximised( )isat1;inotherwords,sheisexpectedtofavourmatingsbyothermalesinproportiontotheirrelativestrength.Stillassuming =, D M F ,thedominantmale’sfitness,ismaximizedat 2133(1)4 33(1)(1)  ==Š++Š orat ,whicheveristhesmaller.Itcaneasilybeshownthat q isgreaterthan(inotherwords,thereisaconflictofinterestbetweenthefemaleandthedominantmale),provided 150 thefactor ()(1) .Thefactor (1) reachesitsmaximumvalueat whichmeansthatif ()0.25 theconflictisguaranteedforallvaluesof ;for ()0.25 thematingconflictmightstillexistbutisnotguaranteed,sinceitwilldependonthevalueof .Forvaluesof ,wefoundmatingconflictinallnumericalsolutionsthatweattemptedforrealisticvaluesof and ,and suchthat ()0.25 Ofcourse,thisresultraisesthequestionastotheinterpretationof ()0.25 .Thisinequalitywilloftenholdbecauseprotectionisagainstinfanticidalattacks;hence,ifprotectionweretotallyeffective, .Sinceinfanticidemostoftenhappenswhenthedominantmaleiseliminatedorincapacitated,thisimpliesthatnormally iscloseto ,i.e. 0.25 .Hence,forallrealisticrangesofvaluesofallthreeparameters,therewillbeamatingconflictbetweenthedominantmaleinthegrouporneighbourhoodandthefertilefemale.AsimpliedbyFigure8.2,amatingconflictexistsbetweenthefemaleandthesubordinate/peripheralmalesaswell,becausethedominantmale’spaternityathermaximumfitness, ,ishigherthanthatofthebestsubordinatemale(thegraphshowshisoptimumintermsofthedominantmale’spaternity;hisownoptimumisthecomplementofthatvalue).However,thebehaviouralexpressionofthisconflictisusuallypreemptedbymatingcompetitionbetweenthedominantandthesubordinatemales,forcingthelattertomatemuchlessthantheywouldotherwisedo.Hence,thesubordinatesneverreachthezoneinwhichfemaleswouldprefertomatelesswiththem.Indeed,thesubordinatemalesreachtheiroptimumpaternity, ,atavaluemuchlessthan1,becausethedominantmaleisexpectedtoattackinfantsobviouslysiredbythem.Ontheotherhand,whendominantmalesarenotaround,forinstancebecausefemalesarerathersolitary,theytooareexpectedtoharassoestrousfemales.Inourequationsweonlyincorporatedtheroleof Fortheunrealisticcaseof (seeabove),thereisnomatingconflict,withbothsexesreachingtheirhighestfitnessat onesubordinatemale,theonemostlikelytosucceedinchallengingthedominantmaleinthenearfuture.Ifonlyoneclearlystronger,youngsubordinatemaleresidesinthegroup,thisapproachisacceptable,becauseoneexpectsfemalestorecognisesuchmales.Forinstance,malebaboonsabouttoriseindominancerankhavedifferentbehaviouralstylesandendocrineprofilesfromothersofsimilarrankwellbeforetheiractualrise(Virgin&Sapolsky,1997).However,iftherearemoresuchmales(andfemalesrecognisethemassuch),ourtreatmentisconservativeandmatingconflictbetweenthefemaleandthedominantmaleisevenmoreintense.Forinstance,iftwomaleshaveareasonablechanceofupsettingthedominantmale(i.e.with ),thefemale’sfitnesswillmaximiseat 1 PredictionsandevidenceAbasic,albeittrivial,predictionisthat,ifnoothermalesareinthematingpool,i.e. ,boththedominantmaleandthefemalewillreachtheiroptimumfitnessat .Hence,intheabsenceofothermales,nomatingconflictisexpected,andthusnoharassmentbythedominantmale.Whenothermalesarepresent,however,variouspredictionscanbemade.Wedevelopthemhereandalsoofferapreliminaryevaluationoftheirfitwiththeprimateliterature.1.HarassmentbydominantmalesObservationsofharassmentofoestrousfemales,especiallybyhigh-rankingmales,inspiredthedevelopmentofthemodel.Itsfundamentalpredictionisthattheconflictofinterestbetweenthefemaleandthedominantmalemayfindexpressioninabehaviouralconflictifthemalehasthemeanstocoercethefemale,e.g.bycoercivemateguarding,andthefemalewilltrytoescapeinordertomatewithothermales(which,accordingtothismodel,she 151 islikelytodo).Thisisastrongpredictionbecauseitcontrastswiththenaiveexpectationthatthemalesmostlikelytoforcematingswillbenon-preferred,andhencegenerallysubordinate.Onemightobjectthatattackingthefemaleinsteadoftherivalmaleofamatingorconsortingpairissimplytheleastriskyoptionforadominantmale,andisalsolikelytopreventthefemalefrommatingwithathirdmalewhileheisengagedinfighting.However,thereisabundantevidenceforharassmentoffertilefemalesbymaleswhenthefemaleisnotactuallymatingorevennearanothermale(seeSmuts&Smuts,1993;andseebelow).Moreover,ifdominantmalesarenotnearthefertilefemale,lower-rankingmalesarealsoexpectedtoemployharassment.Thus,inbothchimpanzees(troglodytes)andorangutans(Pongopygmaeuspossessivemateguardingandforcedmatings,respectively,bysuchnon-dominantmalesarecommonlyobserved(Tutin,1979;Mitani,1985;Goodall,1986,pp.457-64;Schürmann&vanHooff,1986;Fox,1998).2.FemalepolyandryinrelationtothenumberofmalesThematingconflictmodelindicatesthatastheeffectivepowerofthedominantmale1declines,theconflictofinterestbetweenthedominantmaleandthefemalewillincrease(seeFig.8.3).Onecommonsourceofthereducedpowerofthedominantisanincreasednumberofmalesinthematingpool,becausethisprobablyincreasesthestrengthofthestrongestamongthemandperhapsalsobecausethelargernumberitselfmaywearoutthedominantmale,eitherdirectlyorbecausecoalitionsaremorelikely(Bercovitch,1989;Noë&Sluyter,1990).Themodelpredictsthatifthefemalewinstheconflict,theconcentrationofpaternityinthetop- Notethatharassmentofmatingpairsbyjuveniles(forexampleDrukkeretal.,1991)andfemales(Linnetal.,1995)alsooccurs.Suchharassmentisofcoursenotexplainedbythematingconflictmodel.matingconflict 0.00.20.40.60.8Fig.8.3.Themagnitudeofthematingconflict( D ,seethetext)betweenthedominantmaleandthefemaleasafunctionofthestrengthofthestrongestsubordinatemale().Theconflictbetweenthedominantmaleandthefemaleclearlyincreaseswith,albeitnotmonotonically.rankingmalewilldeclineasthenumberorstrengthofrivalsincreases.Thefemalemayachievethisoutcomebymatingmorepolyandrouslyduringfertilecyclesorbymatingafterconception.ThematingconflictmodelthusoffersanamendmenttotheexplanationforthedistributionofpaternitiesovertheavailablemalesprovidedbythePriority-of-Access(PoA)model(Altmann,1962).AccordingtothePoAmodel,adominantmaleexcludesothermalesfrommatingaslongasthereisonlyonefemalenearovulation.Lackofabsoluteconcentrationofpaternityindominantmaleswouldbeduetoareductioninmalematingmonopolyattimesofoverlapoffemaleoestrousperiodsorhighintruderpressure.Themating-conflictmodelclaimsthatthispatternisduetoactivefemalepolyandry,whereasPoAassumesfemalesdonotactivelyseekpolyandry.PoAalsoassumesthatmale-maleaggressionservesonlytomonopoliseaccesstofemales,andisthereforeconsistentwithattacksonmatingpairs,butnotwithmaleaggressiontargetedatthefemaleinparticular(seealsovanNoordwijk&vanSchaik,thisvolume).Todistinguishbetweenthetwomodels,detaileddataon(changesin)male 152 dominancerelationsaswellasmatingsandtheirtiming(i.e.thenumberoffemalessexuallyactivesimultaneously)areneeded.Ifchallengermalesfromwithinthegrouparemorelikelytosucceedthanrecentimmigrants,asisoftenfound(Henzi&Lucas,1980;Cheney,1983;vanNoordwijk&vanSchaik,1985,2001;Robinson,1988;Perry,1998),asubsidiarypredictionfollows:femalesmayprefertoliveinmulti-malegroups,allotherthingsbeingequalbecausethe‘insider’malesposelessofaninfanticideriskprovidedthattheyweregrantedashareofthematings.Thisideahasbeensuggestedbeforebutremainshardtotest(cf.vanSchaik,1996;Nunn&vanSchaik,2000).However,ouranalysisheresuggeststhateventhedominantmalemayfinditinhisinteresttotoleratesomeunrelatedsubordinatemales,becausehisoptimumpaternitymaybeslightlylessthan1,assuminghecancomecloseenoughtothisvalueinreality.3.FemalepolyandryinrelationtopotentialchangeofmaledominancerelationsTheeffectivepowerofthedominantmalemaybereducedbyincreasedstrengthofoneormoreofthesubordinatemales,increasingtheriskofaneffectivechallenge.Ifafemalecanrecognisethatthecurrenttop-rankingmaleislikelytobedefeatedbeforethebirthofherinfant,sheshouldselectivelydecreasehermatingswithhim.Thisscenarioassumesthatthetoprankamongmalesisacquiredthroughchallengeandnotbysuccession,asinsomemacaquespecieswithlargegroupsandseasonalbreeding(reviewedinvanNoordwijk&vanSchaik,thisvolume).Inmanyprimatespeciesfemalesareknowntoattempttobreakawayfromthemonopolisationofthedominantmalesandactivelyattempttomatewithsubordinateorperipheralmales(Hrdy,1981;Small,1993).Theprimateliteraturecontainsafewreportsthatfemalesaremoreactivelypolyandrouswhenthedominancesituationamongthehigh-rankingmalesisnotstable(Samuelsetal.,1984;vanNoordwijk,1985;Janson,fideManson,1995;Mansonetal.1997;Albertsetal.,2003)orwhenthesinglemaleinthegroupisweak(Agoramoorthy&Hsu,2000).Amorerefinedpredictionisthatweexpectfemalestoattempttomatepreferentiallywiththosesubordinateorperipheralmalesmostlikelytosuccessfullychallengethecurrentdominantmaleinthefuture.Hence,oestrousfemalesshouldnotseekmatingswithothermalesthanthedominantrandomlybutshowdistinctpreferences,whichshouldbelinkedtothetargetmales’prospectsforfuturedominance.Inseveralpopulationsyoungmaturingmalesareknowntorapidlyriseinrankandtakeovertoprank,surpassingseveralmalesoveraperiodofonlyafewmonths(e.g.,Cheney,1983;vanNoordwijk&vanSchaik,1985,1988,2001;Hamilton&Bulger,1990;Virgin&Sapolsky,1997;Soltisetal.,2000).Sincesuchchallengesbymaturingmalesareratherpredictable,weexpectthefuturetop-rankingmale(ifalreadypresentinthegroup)tohavealargershareofthematingsthanexpectedforhiscurrentdominanceposition.Atleastonestudytodateseemstoconfirmthispoint:Smith(1994)reportsforalargecaptivegroupofrhesusmacaquesthathighmalesiringsuccess,attributedtofemalechoice,precededarisetohighdominancerankforyoungmales.4.SurreptitiousmatingwithsubordinatemalesThenon-zerovalueof thatmaximizesthesubordinatemales’fitnessleadstothepredictionthatitisintheinterestofboththefemaleandthesubordinatemaletomateasinconspicuouslyaspossibleinordertopreventthedominantmalefromadjustinghis estimatedown,andwithholdprotectionfromtheinfant.Wethereforeexpectthatmatingsbetweenfemalesandsubordinatemalestendtotakeplaceoutofsightofthedominantmale,e.g.attheperipheryorawayfromthegroup,andshouldlessoftenbeaccompaniedbycalls.Inordertodistinguishthispatternfromgeneralmatingcompetition,itshouldevenhappenifthedominantmaleisinvisiblecontactbuttoofarawaytoattackthepaireffectively.Wecanfurtherpredictthatinconspicuousmating 153 withsubordinatesisevenfoundinspecieswithouteffectivemaleharassmentoffemales.Despiteaseriouslackofquantitativedata,ithasbeennotedforseveralspeciesthatmatingsbetweenfemalesandsubordinatemalestendtooccurrathersurreptitiously(Pantroglodytes:Tutin,1979;Goodall,1986;Macacafuscata:Huffman,1992;mulatta:Berardetal.,1994;M.arctoidesNieuwenhuijsenetal.,1986;M.sylvanus:Paul,1989).Onestudyfocusingonmatingsinconcealedplacesnotedthatespeciallylower-rankingmalesfasciculariswereinvolvedinmatingsoutsideofvisualcontactwiththerestofthegroup(Gygax,1995),aspredicted.Inmanyspeciesfemalesgiveaspecificcopulationcall,towhichothermalesdorespondbylookingatthepair(vanNoordwijk,1985)orevenattackingthem(Oda&Masataka,1995).Inatleastonestudyatendencywasfoundformatingswithsubordinatemalestobequiet(M.thibetana:Zhao,,althoughanotherstudyfoundnoeffectofmaleidentityonfemalecallingtendency(fascicularis:vanNoordwijk,1985).Hence,renewedexaminationofthepatternsindiscreetmatingsmaybeworthwhile,alsoinspecieswithouteffectivemaleharassment(aslongasinfanticidebymalesposesarisk).SEXUALHARASSMENTANDREPRODUC-TIVEPHYSIOLOGYThedistributionofsexualharassmentThemodelpresentedaboveconfirmstheexistenceofaconflictofinterestbetweenthebreedingfemaleandthegroup’smales.Theconflictwiththedominantmale(s)ismostlikelytobeexpressedbecausethismale(ormales)willtrytomonopolisethefemalemostofthetime,thuspreemptinganyconflictwiththeothermales.Thequestion,ofcourse,iswhowinsthisconflict?Whenevermaleharassmentoccurs,femalescanonlywinatseriouscosts.Coercivemateguardingmakesitmoredifficult,andmorecostly,forthefemaletoseekthematingswithsubordinateandperipheralmalesneededtoachievethedistributionof valuesoptimaltoher.Harassmentismorecommonwherefemalesarelesspowerful,bothphysicallyandsocially(Smuts&Smuts,1993).Givingintocoercionmakesthefemalemorevulnerabletoinfanticide,andifthisriskissufficientlyincreased,weexpectthatnaturalselectionhasproducedphysiologicalorbehaviouraltendenciesinfemalestoreducethedominantmale’smonopolisationpotential,providedthattheircostsdonotexceedthegainsofreducedinfanticiderates.Sinceitisnotaprioriclearwhatformsthesefemalecounter-strategiescantake,wewillfirstexaminethetaxonomicdistributionofsexualharassmentofsexuallyactive(‘oestrous’)femalesinprimates,buildingonexistingreviews(especiallySmuts&Smuts,1993;Dixson,1998),andthensearchforderivedreproductivefeaturesinthetaxawithharassment.Inordertocapturethevariationinmalebehavioursdirectedatsexuallyactiveor‘oestrous’females,weproposethefollowingcategoriesofsexualharassment(definedasaggressionbysexuallymaturemalesagainstsexuallyactiveor‘oestrous’females):(1)Nosexualharassment,noranyattempts,reported.(2)Sexualharassmentattemptsreported,butonlyinthedirectmatingcontextandmostlyineffective,i.e.thefemalewardsoffthemaleorcounterattacks,andthemaleisunabletopreventthefemalefrommovingawayormatingwithothers.(3)Effectivesexualharassmentisobservedinboththedirectmatingcontextandofoestrousfemalesingeneral,asevidencedbycoercivemateguardingandphysicalattacksontheoestrousfemalefollowedbysubmission.Malebehaviourssometimesincludebitesthatresultinwoundingorevendeath,forcedmatings,andattackson 154 femaleswhenmatingwithothermales.Thesecondcategoryisneededbecauseinseveralspecies(includingalsomanynon-primatemammals),malesshowaggressiontowardfemalesinthematingcontextthatisnotaccompaniedbyanyattemptsatcoercivemateguarding.Thepresenceofthesebehaviourssuggeststhataggressionmaybeanintegralcomponentofmatinginthesespecies.Theextenttowhichtheseattemptsatharassmentwouldconstitutedefactoharassmentdependsonthedegreetowhichtheystopfemalesfromachievingthepreferreddegreeofpolyandry.Theliteratureisunderstandablyvagueonthis,butitisourimpressionthatfemalescanstillmatewithothermales.Inanycase,itisusefultokeepthissecondcategoryseparatefromthecaseswheremalesalsoattackoestrousfemalesoutsidethedirectmatingcontextorforcematings,thecategoryofeffectiveharassment.Forthepresentpurpose,welimitourreviewtospeciesvulnerabletoinfanticide.Aspeciesisconsideredvulnerableifinfanticidebymalesisreportedforit,orifithasalifehistorythatmakesthefemalesofthespeciesvulnerabletosuchattacks,orboth(vanNoordwijk&vanSchaik,2000;vanSchaik,2000b).Theadvantageofthisdefinitionisthatweneednotrelyonlyonreportsofinfanticide,whichtendtoberare.Asrequired,allspeciesknowntohaveinfanticidearealsopredictedbythelifehistorymeasuretobevulnerable.Althoughdataonharassmentarestillveryincompleteafewclearpatternsemerge.Consistentwithearliercompilations,weseenoevidenceforeffectiveharassmentinLemuroidea(lemurs)orinPlatyrrhini(NewWorldprimates),butmanyreportsfortheCatarrhini(OldWorldprimates;Fig.8.4).Examplesofadultfemalesbeingabletosystematicallyelicitsubmissionfromadultmalesaremostcommonlyfoundinlemurs,inseveralmonomorphicNewWorldprimatesandinthefewpair-livingOldWorldprimates(Kappeler,1993;Strier,1994).Inallthesespecies,malesattackrivalmalesbutweseeatmostattemptsatharassmentof%speciesw/harassment LEMPLACAT Fig.8.4.Theincidenceofeffectivesexualharassment(whichmayincludeinjuryoffemalesandforcedmatings)amongprimatespeciesvulnerabletoinfanticidebymalesinthreeradiations(LEM=Lemuroidea;PLA=Platyrrhini-NewWorldprimates;CAT=Catarrhini-OldWorldprimates).Basedonliteraturereview(startingwithSmuts&Smuts,1993),availablefromtheauthorsuponrequest.Numberofspecieswithinformationindicatedabovecolumns.females,e.g.inlemurs(e.g.,Pereira&Weiss,1991;Sauther,1991;Brockman,1999),andfemalesoftencounter-attackandbeabletochoosetheirmates(Richard,1992).Likewise,onlyinsomeNewWorldprimatesdoweseeevidenceofcoalitionsofmalesbeingrequiredtoinspectafemale’ssexualstate(inSaimirioerstediAtelesLagothrix:Boinski,1987;Smuts&Smuts,1993).Remarkably,effectivesexualharassmentisabsentamongNewWorldprimates,eventhemoredimorphicones:forinstance,femaleAlouattapalliatasuccessfullyrebuffattemptsatforcedmatingsbymales(Jones,1985).Conversely,effectivesexualharassmentbymalesisreportedformanyOldWorldprimatespecies.Inthislineage,wealsoencountermanyrecordsofmalesgenerallyharassingfemales,orfemalesrequiringcoalitionsinordertodefendthemselvesagainstharassingmales(Smuts,1987;Smuts&Smuts,1993).However,bynomeansallOldWorldprimatespeciesshowsexualharassmentbymales.Oursampleisasyettooincompletetoallowanalysisoftheinterspecificpatterninsexualharassmentin 155 %ofspeciesphase(days) (b)5 PLACATdays(median)%ofspecies 510152025 05101520253822 LEMPLACATFig.8.5.Variationamongspeciesvulnerabletoinfanticidebymalesinthreeprimateradiations(seeFig.4forabbreviations)inavarietyofsexualfeatures:(a)themediandurationofthemating(‘oestrous’)period(P0.001);(b)themeandurationofthefollicularphase(indays)oftheovariancycle(P0.01);(c)thepercentageofspeciesshowingexaggeratedsexualswellings(P0.001);(d)thepercentageofspecieswithmatingcallsbyfemales(P0.01).TestedwithKruskal-Wallisone-wayAnova.Numbersofspeciesindicatedabovecolumns.(a,c,anddbasedondatacompiledinvanSchaiketal.,1999;bondatacompiledbyvanSchaiketal.,2000.)relationtotheknownriskfactors(largermalebodysizeorweaponry,lackoffemaleallies:Smuts&Smuts,1993).Lemursarelargelymonomorphic(Kappeler,1991)andNewWorldprimatesarefarlessdimorphicoverallthanOldWorldprimates(e.g.,vanSchaiketal.,2000).However,additionalfactorsareprobablyinvolvedbecauseclearlydimorphicNewWorldprimatespeciesandevensomehighlydimorphicOldWorldspecies(e.g.Erythrocebuspatas)failtoproduceclearevidenceofsexualharassment.Hence,asyetunidentifiedadditionalfactorsarealsoinvolvedinshapinginterspecificvariationintheoccurrenceandintensityofsexualharassment.Femalecounter-strategiestomalesexualharassmentHavingfoundthateffectivesexualharassmentoffemalesbymalesislimitedtoOldWorldprimates,weemployatwo-stepproceduretoidentifyderivedfeaturesofsexualityinOldWorldprimatesthatpossiblyrepresentcounter-strategiestothegreaterriskofsexualharassment.ThefirststepisasystematiccomparisonoffemalesexualityinspeciesvulnerabletoinfanticideinthethreeprimateradiationscomparedaboveandseeinwhichrespectOldWorldprimatesstandout.ThesecondstepistoconductcomparisonswithintheOldWorldprimateswithvariationincoerciveabilitiesorinfanticiderisk 156 matingperiod(estrus’)(days) nofmatespercycleCATLEM+ Fig.8.6.Mean(±s.d.)durationofthemating(‘oestrous’)periodinspeciesvulnerabletoinfanticidebymalesinrelationtothedegreeoffemalepolyandry,inthosevulnerabletomalesexualharassment(CAT)andthosenotvulnerable(LEMandPLA).Degreeofpolyandry:1-matingwithasinglemalein�90%ofcycles;m-matingwithmultiplemalesin10-50%ofcycles;andM-matingwithmultiplemalesinmorethan50%ofthecycles(cf.vanNoordwijk&vanSchaik,2000).Samplesizes(numberofspecies)indicatedateachpoint.DataonmatingperiodtakenfromvanSchaiketal.(1999).Rankcorrelationissignificant(P0.01)forcatarrhines.Thematingperiod(‘oestrous’period,i.e.periodbetweenfirstandlastmating)withinanovariancycleisatleastthreetimeslongerintheaverageOldWorldprimatethanintheotherradiations(Fig.8.5a).Moreover,matingperiodincreaseswiththenumberofmalesthatafemalesendsupmatingwith,inOldWorldprimatesbutnotinothers(Fig.8.6),consistentwiththeexpectationthatonlyinsomeOldWorldprimatesfemaleswouldfinditdifficulttoescapefromthemonopolisationofthedominantmaleinordertomatewithothermales.ThelongmatingperiodsinOldWorldprimatesaremadepossiblebyachangeintheovariancycle,inthattheirfollicularphasesareabouttwiceaslongasintheotherradiations(Fig.8.5b).ComparisonswithintheOldWorldprimatessuggestedthatfollicularphasesarelongerwherethesexesaremoredimorphicinbodysizeorweaponry;specifically,wefoundevidenceforcorrelatedevolutionbetweenthelengthofthefollicularphaseandthedegreeofcaninedimorphism(vanSchaiketal.,2000),suggestingthatthefactorexplainingvariationamongradiationsisalsoatworkwithintheOldWorldprimateslineage.ThelongperiodsofsexualactivityshownbyOldWorldprimatefemalesrequireeitherthatspermremainsviableinthefemalereproductivetractforlongperiodsoftime,orthatovulationislesstightlylinkedtothevisual,olfactoryorbehaviouralsignalsthanusuallyassumed,orboth(cf.Martin,1992).Thereisnoworkinsupportoftheformerpossibility,butrecentworkhassupportedthesecondidea.Nunn(1999)andvanSchaiketal.(2000)reviewendocrinologicalworkshowingthatovulationisonlypoorlylinkedtothesesignalsandthusshouldberatherunpredictableformales.RecentworkbyHeistermannetal.(2001)onhanumanlangursconfirmedthisprediction,showingthatovulationcantakeplacewithapproximatelyequalprobabilityatanytimeinthevariableperiodoffemalesexualactivityandthatmalesdonotrecognisethefemale’stimeofovulation,bothintermsofbehaviourandofthedegreetowhichpaternityisconcentratedinthedominant.Ifunpredictabletimingofovulationwasfavoured 157 S.D.cyclelength 0 2 4 6 8 10 12 14 16 CAT LEM PLA Fig.8.7.Thestandarddeviationofthelengthoftheovariancycleinspeciesvulnerabletoinfanticideinthreeprimateradiations(seeFig.8.4).Numberofspeciesindicatedabovecolumns.Arrowsindicatemedians.TestedwithKruskal-Wallisone-wayAnova(P0.01).bynaturalselectionbecauseitallowedthefemaletohavelongermatingperiodsofvariablelength,thenthereshouldbelessneedforitamongthespeciesthat,whilevulnerabletoinfanticide,arenotvulnerabletomalesexualharassment,i.e.lemursandNewWorldprimates.Thereareasyetnodetailedstudiesofthekinddoneonlangursforanyofthesespecies.However,wecangetanindicationoftheextenttowhichovulationisunpredictablebyexaminingthevariabilityinthedurationofthefollicularphaseoftheovariancycle(inmostspecies,malescanrecognizewhenthelutealphaseiswellunderway;e.g.,Dixson,1998).Dataonvariationinfollicularphaselengtharescarce,butbecausethevariabilityinthefollicularphaseexceedsthatinthelutealphase(onaveragebyaboutafactoroftwo:seecompilationinvanSchaiketal.,2000),variabilityinthetotaldurationoftheovariancyclemayprovidearoughindicationofunpredictableovulation.Figure8.7showsthatthestandarddeviationofthelengthoftheovariancycleinoursample(basedonHayssenal.,1993andacompilationbyK.Hodges&U.Moehle,unpubl.)isindeedhigherforOldWorldprimatesthanitisforthetwootherradiations(includingonlyspeciesvulnerabletoinfanticide).Thedifferencesamongthemaresignificant(Kruskal-Wallistest,H[2]=11.37;P0.01),andintheexpecteddirection.OldWorldprimatesdifferfromtheotherradiationsintwomoreaspectsofsexualbehaviour:sexualswellingsandcopulationcalls.ThefirsthasgeneratedmuchinterestfromDarwin(1876)on(e.g.,Dixson,1983;Hrdy,1997;Nunn,1999):femalesofseveralspecieshaveexaggeratedsexualswellings(Fig.8.5c).AmongOldWorldprimatestheseswellingsarefoundonlyinspeciesthatareactuallyorpotentiallypolyandrous(cf.Clutton-Brock&Harvey,1976),andamongthempredominantlyinnon-seasonalbreeders(vanSchaiketal.,1999).TherestrictiontoOldWorldprimatesandthepredominanceamongnon-seasonalbreedersisconsistentwiththehypothesisthattheseswellingsareneededwheretheriskofharassmentbydominantmalesisparticularlyserious(femalesinseasonalbreederscanmovemorefreelyfrommaletomalebecausetheytendtobesexuallyactivesimultaneously).Thus,asarguedbyNunn’s(1999)graded-signalhypothesis,sexualswellingsfunctionnotonlytoattractthedominantmale(s)duringtheirmaximumsize(whentheprobabilityofovulationishighest),butthroughtheirexaggerationtheycanalsoattractlower-rankingorperipheralmaleswhenthedominantmalesarelessattractedduetothecoststothesemalesofmateguardingfortoolong.ForfurtherdiscussionofexaggeratedswellingsseeZinneretal.(thisvolume).Second,wefindthatfemalesmatingcallsaremorecommonamongOldWorldprimates(Fig.8.5d).Matingcallsaregivenduringorafterejaculation.Theyarenottobeconfusedwith‘oestrouscalls’givenwhenthefemaleisreceptivebeforeactuallymating(generallyinterpretedasalertingallmaleswithinhearingdistancetohercondition),orwith‘distress’callsgivenbyfemalenorthernelephantsealsorchickenswhenmountedbyasubordinatemaleoratatimethefemaleisnotreceptive,oftenfollowedbyinterferencebyahigher-rankingmale(Cox&LeBoeuf,1977;Pizzari& 158 Birkhead,2000).Matingcallsmayalertothermalesthatthefemalehasmated,andmaythusattractthem(O’Connell&Cowlishaw,1994;vanSchaiketal.1999).Matingcallsmaybeagradedsignalwhosequalityvariesthroughoutthecycle(Semple&McComb,2000)andthussomehowindicatestheprobabilityofovulation,muchlikeswellings(theirdistributionacrossspecieslargelymirrorsthatofswellings:vanSchaiketal.,1999).Femalesmayalsousethemtactically,callingonlyormoreoftenwithparticularmalesthanwithothers(seeabove).Moredetailedfieldstudiesandcomparisonsbetweenspecies,includingseveralNewWorldprimates,mayhelpusdeterminewhethertheirfunctionis,asproposedhere,linkedtothereductionofmalesexualharassment.Thuswefoundstrongevidenceforalinkbetweenthedistributionofphysiological,morphologicalandbehaviouralcharactersticsoffemalesexualitywiththeoccurrenceofharassmentbymaleswhoarephysicallystronger.LineagedifferencesinsexualityThesignificantdifferencesbetweenradiationsinvariousfeaturesservetoshowtheexistenceofagradeshift.Explaininggradeshiftsisinherentlydifficultbecausemanyfactorshavechangedinparallel.Forinstance,amongOldWorldprimates,wesee,relativetothetwootherradiations,thepresenceofterrestrialadaptations,largermeanbodysize(relativetoextantspeciesintheotherlineages),largermeangroupsize,ageneralreductioninrelianceonolfactorycommunication,greatertendenciestowardfolivory(relativetoNewWorldprimates),etc.ItisofcourseentirelypossiblethatoneoracombinationofthesefactorsfacilitatedtheevolutionoflongerfollicularphasesorexaggeratedswellingsinOldWorldprimates.However,thevariationwithinthelineage,withrespecttothedurationoffollicularphasesinrelationtomaleharassmentpotential,tothedurationofmatingperiodinrelationtopotentialforpolyandry,andtotheconditionsinwhichexaggeratedswellingsoccur,suggeststhatsubsequentevolutionwithinthelineageinthesetraitsdidcorrelatewithvariationinharassmentpotential.Thus,variationwithinthelineageisinthesamedirectionasthatbetweenthelineages.Wethereforebelievethattheideathatthecombinationofmaleharassmentandinfanticideriskfacilitatedtheevolutionofthesederivedsexualfeaturesisaviableworkinghypothesis,worthyoffurtherevaluation.DISCUSSIONANDPROSPECTSItshouldbestressedthatwedonotproposethatprimatesexualityismoldedbyinfanticideriskalone:therearenumerousselectivefactorsonwhatisperhapsthebehaviourmosttightlylinkedtofitnessandthusmostdirectlyresponsivetonaturalselection(Dixson,1998).Birkhead&Kappeler(thisvolume)discussadditionalhypothesesforfemalepolyandryinprimates,butthesearenotnecessarilyincompatiblewiththeinfanticideavoidancefunction.Nonetheless,theaimofthischapterhasbeentoevaluateHrdy’s(1979)predictionsconcerningtheimpactofinfanticideriskonsexualbehaviourandreproductivephysiologyinprimates.Theoriginalpredictionsareupheldbutalinktosexualharassmentcanalsobeaddedtothelist.Ourpreliminaryexplorationsuggeststhatharassmenthasimpactedfemalereproductivebehaviourandphysiologybutasalways,theroleofcomparativeworkisbestregardedascomplementarytofocusedobservationalorexperimentalstudies.Thestudiesusedtoevaluatethehypotheseswerenotdesignedwiththeseideasinmind,andconfoundingfactorscanthereforerarelybeexcluded.Wethereforemakethefollowingsuggestionsforfuturework.Moredetailedstudiesoffemalesexualbehaviorcouldincorporatetheroleofsocialdynamicsintheoptimalbalancebetweenpaternityconcentrationindominantsanddilutionormanipulationofits 159 assessment.Forexample,ifnewdominantsarealwaysrecentimmigrants,verylittlepaternitydilutionisexpected,butifnewdominantsarealwayslong-termresidens,muchmorepaternitydilutionisexpected.StrongtestswouldcorrectfortheexpectationbasedonthePriority-of-Accessmodel.AstomaledecisionmakingitwillbedifficulttoimproveonthebehaviouralmonitoringofBorriesal.(1999)onhanumanlangurs,althoughadditionalworkondifferentspecieswouldbeworthwhile.Withrespecttomatingconflict,detailedstudiessuchasthoseofGygax(1995)onthetendencyofparticularindividualsorpairstoengageinmatingsinconcealedlocationsoronthefemales’tendencytogivecopulationcallscanbeconducted.Futureworkonfemalereproductivephysiologycouldfocusonthreeissues.First,detailedworkonthesexualbehaviouroffemalesinspeciesinthedifferentradiationsalongthelinesofthestudybyHeistermannetal.(2001)isneeded,wheresocialandsexualbehaviour,femaleovarianstateandpaternityareallrecordedsimultaneously.Second,weshouldstudy(ifnecessarybyexperimentalmanipulation)theimpactofmalerepresentationinthesocialunitonfemalereproductivephysiologyandbehaviourinspeciesofdifferentlineages.Third,morefine-grainedcomparativeworkontherelationshipbetweensexualharassmentandpossiblecoercionindicatorsinOldWorldprimates,aswellasdetailedstudiesofhighlydimorphicNewWorldprimates,mayhelpusunderstandthedistributionofmalesexualharassmentinrelationtofemalereproductivephysiology.SUMMARY&CONCLUSIONSWeexploredthehypothesisthatthevulnerabilityoffemalestoinfanticidebymaleshasaffectedfemalesexualbehaviourandgivenrisetosexualharassmentinmanyprimates.Afterestablishingtheadaptivenatureofinfanticidalbehaviourformaleswhoattackinfantstheydidnotfather,webrieflyreviewedsexualcounter-strategiesbyfemales(polyandrousmating,matingduringpregnancy).Wethenaddressedtwomainissues.First,becausepaternitydistributionisaconstant-sumgame,afemalefacesaconsiderablechallenge.Wearguedthatthefemale’ssexualbehaviourservestoproducepaternityestimatesamongthevariousmalesthatadduptomorethan1.Moreover,paternityuncertaintymayforcemalesintoavoidingthecostliestmistakes,makingthemrefrainfromattackinginfantstheyprobablydidnotsireandmakingthemprotectthosetheymayhavesired.Second,weproposedanexplanationthatlinksinfanticidewiththecommonobservationthathigh-rankingmalesoftenharassoestrousfemales.Wedevelopedamodelthatshowsthatamatingconflictexistsbetweenthefemaleandthedominantmale(s),andexaminedseveraldetailedpredictionsaboutmatingbehaviour.Matingconflictcanfindexpressioninharassmentifmalescancoercefemales.Thismodelledtoseveralpredictions,andapreliminaryevaluationshowedagoodfitwithexistingdataonprimatesexualbehaviour.WealsonotedthateffectivesexualharassmentamongprimatesisprobablylimitedtoOldWorldprimates,inwhichitmayhaveproducedanarmsrace,leadingtofurtherchangesinfemalesexualbehaviourandphysiologyinthislineage,includinglongermatingperiods,longerfollicularphaseswithmoreunpredictableovulation,exaggeratedsexualswellingsandperhapsmoreextensivefemalecopulationvocalisations.ACKNOWLEDGMENTSWethankKeithHodgesandUlrikeMoehleforallowingustousetheircompilationofdataonprimateovariancycles,HelenZayacforcompilingmanyoftheharassmentreferences,andTimBirkhead,PattyGowaty,SarahHrdy,PeterKappeler,RebeccaLewis,andSagarPanditforhelpfulcomments. 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