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Female Reproductive Strategies and the Ovarian Cycle in Hamadryas

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Female Reproductive Strategies and the Ovarian Cycle in Hamadryas Femalereproductivestrategiesandtheovarian cycleinhamadryasbaboons AthesissubmittedinpartialrequirementoftheMaster’sDegreeof ScienceinConservationBiologyatVictoriaUniversityofWellington by R.E.Tobler ABSTRACT: Thisthesisexaminestherelationshipbetweensexualbehaviourandthe ovarian cycle in a group-living primate, Papio h. hamadryas . Of particular interest is whetherfemalesmodifytheirovariancycleinamannerthatisexpectedincreasetheir reproductivesuccess.Thestudywasconductedonacaptivecolonywheretheresident males (RM) had been vasectomised prior to start of the study resulting in all mature femalesundergoingrepeatedovariancyclingthroughoutthestudyperiod.Thismadethe analysisofsexualbehaviourrelativetofinescalechangesintheovariancyclepossible. One year of ovarian cycle data and 280 hours of behavioural data was collected via observationalsamplingduringthestudy.RMvasectomisationdidnotalterthearchetypal one male unit social structure nor the typical socio-spatial organisation of wild hamadryas populations. Females were found to be more promiscuous than in wild populations, however, presumably because of the confounding effect that the high number of simultaneously cycling females had on RM herding (Chapter 1). RMs dominatedcopulationsovertheoptimalconceptiveperiodoftheovariancycle,whilethe majorityofextra-OMUcopulationsoccurredoutsidethisperiodandwererarelysolicited by females. This pattern supports a dual paternity concentration/paternity confusion strategy,andnotfemalechoiceorfertilityinsurancestrategies(Chapter2).Femaleswere not found to synchronise or asynchronise their cycles over the 1 year study period, althoughareviewoftheliteratureonhamadryasbreedingpatternssuggeststhattheymay be able to do so over shorter periods (Chapter 3). Females did, however, appear to regulatethelengthoftheturgescentphaseoftheirovariancycleinamannerthatwould facilitate a paternity confusion strategy and maximise their expected fitness payoff (Chapter4).Consequently,thisstudyprovidesempiricalevidencethatfemalehamadryas baboons manipulate their ovarian cycle in a manner that is expected to increase their reproductivesuccess. i Tableofcontents Listoffigures v Listoftables vi Acknowledgements vii 1 GeneralIntroduction 1 Themammalianovariancycle 2 Evolutionoftheovariancycleinmammals 5 Evolutionoftheovariancycleinprimates 6 Exaggeratedperinealswellings 9 Femalecontroloftheovariancycle 10 Hamadryasbaboons 13 Thesisstructureandresearchquestions 15 References 17 2 Thestructureandorganisationofsocialandsexualinteractions intheWellingtonZoohamadryasbabooncolony 29 Abstract 29 Introduction 30 Methods 31 Results 45 Discussion 63 Conclusion 76 References 79 3 Thepatternandfunctionofsexualbehaviourinrelationto theovariancycleinhamadryasbaboons 84 Abstract 84 ii Introduction 85 Methods 87 Results 95 Discussion 116 Conclusion 124 References 125 4 Noevidenceforovariansynchronyorasynchrony inhamadryasbaboons 131 Abstract 131 Introduction 132 Methods 134 Results 141 Discussion 145 Conclusion 152 References 152 5 Manipulationoftheovariancycleinresponsetobehavioural andphysiologicalfactorsinhamadryasbaboons 160 Abstract 160 Introduction 161 Methods 165 Results 171 Discussion 177 Conclusion 182 References 182 6 Summary 187 iii Futurework 190 References 191 Appendix1:Ageclassesforhamadryasbaboons usedinthisstudy 193 Appendix2:Distributionofsamplesacrossovarian cycleforindividualfemales 194 iv ListofFigures Figure1.SchematicoverheadviewofWellingtonZoohamadryasenclosure 35 Figure2.Temporaldistributionofsampling 46 Figure3.Nearestneighbourdendrogram(socialorganisationofthecolony) 48 Figure4.Spatialdistributionofindividualsbygroups 49 Figure5.Activitybudgetinrelationtothetimeofyear(bymonth) 52 Figure6.Activitybudgetforindividualcolonymembers 53 Figure7.Distributionofaffiliativeinteractionsforeachindividualbygroup 55 Figure8.Distributionofapproachesforeachindividualbygroup 56 Figure9.Distributionofagonisticinteractionsforeachindividualbygroup 58 Figure10.Distributionofconciliatoryinteractionsforeachindividualbygroup 59 Figure11.Distributionofsexualinteractionsforeachindividualbygroup 60 Figure12.Averagehourlymountraterelativetoovariancycleday 100 Figure13.Proportionofmountsaborted/rejectedforeachdayofovariancycle 101 Figure14.Averagehourlyejaculatorymountraterelativetoovariancycleday 105 Figure15.Averagehourlypresent/inspectionraterelativetoovariancycleday 108 Figure16.Averagehourlyapproachraterelativetoovariancycleday 112 Figure17.Changesinovariancyclestatusforeachfemaleoverstudyperiod 147 Figure18.Turgescentphasefitnesscosts/benefitsmodel 164 Figure19.Boxplotsofturgescentphasebiasforindividualfemales 173 Figure20.TurgescentphasebiasagainstcyclelengthforfemalesgroupedbyOMU 174 v Listoftables Table1.DemographicprofileofmembersofWellingtonZoocolony(Ch.1) 32 Table2.Ethogram(Ch.1) 37 Table3.DemographicprofileofmembersofWellingtonZoocolony(Ch.2) 88 Table4.Ethogram(Ch.2) 92 Table5.Talliedsexualinteractionsbetweenindividualfemalesandmalesbygroup 97 Table6.Pemutationtestresults:attemptedmounts 103 Table7.Pemutationtestresults:successfulmounts 104 Table8.Pemutationtestresults:ejaculatorymounts 106 Table9.Pemutationtestresults:presents 109 Table10.Pemutationtestresults:perinealinspections 111 Table11.Pemutationtestresults:approachesinitiatedbyfemales 114 Table12.Pemutationtestresults:approachesreceivedbyfemales 115 Table13.DemographicprofileofmembersofWellingtonZoocolony(Ch.3) 135 Table14.Menstrualcycleparameters(Ch.3) 142 Table15.Ovariansynchronypermuationtestresults 144 Table16.DemographicprofileofmembersofWellingtonZoocolony(Ch.4) 166 Table17.Menstrualcycleparameters(Ch.4) 172 Table18.Mensestoturgescentphaseinterval 176 vi Acknowledgements Thisthesisistheproductofapproximatelytwoyearsofearnestlabour.Followingayear ofdatacollectionattheWellingtonZoo,Ispentanotheryearinputtingandanalysingthe 250+hoursofdataandwritingthefinaldocument.Severalpeoplewereintegraltothis process, providing me with the advice and encouragement necessary to complete this document.TothesepeopleIamforeverindebted,andIwouldliketothankthemhere.I amparticularlygratefultomyprimarysupervisor,WayneLinklater,whoseideaitwasto study the Wellington Zoo hamadryas baboon colony and without whose wisdom and guidancethisthesiswouldhavebeenmuchthepoorer.Iamsimilarlyindebtedtomy secondarysupervisor,AlanDixson,whosuggestedthatIfocusontheovariancyclesof femalesandwhoseseminalworkonprimatesexualityservedasatemplateformyown endeavours,andtoShirleyPledger,whoconceivedanddesignedthepermutationmodels in chapters 3 and 4 and enlightened me to the power and importance of statistical modelling. Furthermore, this project would have been impossible without permission from the Wellington Zoo community to conduct my research there. The support and companionship that I received from the Wellington Zoo staff made my time there a pleasureandsomethingthatIshallalwaysrememberfondly.InparticularIwishtothank PaulHorton,whohelpedtofamiliarisemewiththeindividualbaboonsandprovidedme with a detailed history of the colony. Thanks also goes to my closest friend and confidant,RebeccaPaxton,whospentmanyhourstirelesslyinputtingdataforlittlemore thantheoddbitofliquoriceandmanyvaguepromises.Lastbutnotleast,Imustthank the baboons themselves, whose trials and tribulations were always educational, often amusing, occasionally perplexing, and which provide the basis for this thesis. vii Chapter1:Generalintroduction Rhythmicalchangesinreproductivestatusarecommonfeaturesofbiologicalorganisms, both across and withingenerations. The lifecycle of each individual follows a passage from fertilisation and embryonic development, through to immaturity, maturity and finally senescence, which is repeated in successivegenerationsofoffspring.Similarly, upon reaching sexual maturity many organisms exhibit cyclical reproductive patterns throughouttheiradultlives.Forinstance,inmanyorganismsfertilityisrestrictedtoa relatively limited time period within each year, a pattern which is replicated at approximately the same time over successive years. Indoingsofemalesmayimprove their reproductive success by coordinating future reproductive events with favourable environmentalconditions(Baker,1938;Bronson,1985;BronsonandHeideman,1994; Nelsonetal.,1990),orbylimitingtheirfecunditytocertaintimesoftheyearwherethere are sufficient resources to support reproductive functions (Asa, 1996; Bronson and Heideman,1994;Nelsonetal.,1990). Many females also experience even finer-scale cyclical patterns called ovarian cyclesthatareassociatedwithperiodicreleaseofgametes(i.e.,ova)inthefemalegonads (i.e.,theovaries).Thesevarygreatlyintheirbasicfeaturesandlengthacrosstheanimal kingdom,andarelikelytohavealsobeenshapedtosomedegreebyevolution.Inthe remainderofthissection,Iwilloutlinethearchetypalfeaturesofthemammalianovarian cycleanddiscussitspossibleevolution,firstlyformammalsingeneralandthenforthe most researched order in this respect, the primates. Next I discuss the evolution of exaggerated perineal swellings in primates and the possibility of individual female controloftheovariancycleinmammals.Finally,informationonthefocalspeciesofthe study, the hamadryas baboon ( Papio h. hamadryas ), is provided, before the research questionsandgeneralsynopsisofthethesisareoutlined.
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