Functional Ecology 2018321237ndash1250 wileyonlinelibrarycomjournalfec emsp|emsp1237copy 2018 The Authors Functional Ecology copy 2018 British Ecological Society
Social status mediates the fitness costs of infection with canine distemper virus in Serengeti spotted hyenas
Lucile Marescot1emsp|emspSarah Benhaiem1 emsp|emspOlivier Gimenez2 emsp|emspHeribert Hofer134emsp|emsp Jean-Dominique Lebreton2emsp|emspXimena A Olarte-Castillo1emsp|emspStephanie Kramer-Schadt1daggeremsp|emsp Marion L East1dagger
Abstract1 Theextenttowhichthefitnesscostsofinfectionaremediatedbykeylife-historytraits suchasageor social status is still unclearWithinpopulations individualheterogeneity in the outcomeof infection is the result of two successive pro-cessesthedegreeofcontactwiththepathogen(exposure)andtheimmunere-sponse to infection In socialmammals because individuals holdinghigh socialstatus typically interactmore frequentlywith groupmembers they should bemoreoften incontactwith infected individuals thanthoseof lowsocialstatusHoweverwhen access to resources is determined by social status individualswithahighsocialstatusareoftenbetternourishedhaveagreateropportunitytoallocate resources to immune processes and therefore should have a smallerchanceofsuccumbingtoinfectionthanindividualswithlowsocialstatus
2 Weinvestigatedtheriskandfitnesscostsofinfectionduringavirulentepidemicofcaninedistempervirus (CDV) inasocialcarnivorethespottedhyena intheSerengetiNationalParkWeanalysedtwodecadesofdetailed life-historydatafrom 625 females and 816males using amulti-event capturendashmarkndashrecapturemodel that accounts for uncertainty in the assignment of individual infectionstates
3 CubsofmotherswithahighsocialstatushadalowerprobabilityofCDVinfectionand were more likely to survive infection than those with low social statusSubadultandadultfemaleswithhighsocialstatushadahigherinfectionprobabil-itythanthosewithlowsocialstatusSubadultfemalesandpre-breedermalesthathadrecoveredfromCDVinfectionhadalowersurvivalthansusceptibleones
4 Our study disentangles the relative importance of individual exposure and re-sourceallocationto immuneprocessesdemonstrates fitnesscostsof infectionforjuvenilesparticularlyforthosewithlowsocialstatusshowsthatpatternsofinfectioncanbedrivenbydifferentmechanismsamongjuvenilesandadultsandestablishesanegativerelationshipbetweeninfectionandfitnessinafree-rangingmammal
1238emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
1emsp |emspINTRODUC TION
Infectious diseases pose a particular threat to high-density popu-lationsandgroup-livingspecieswithhighcontactrates (HawleyampAltizer2011)Theremaybesubstantialvariationamongmembersofagroupintheirdegreeofexposuretoagivenpathogenandintheoutcomeofinfection(BeldomenicoampBegon2010VanderWaalampEzenwa2016)Bodyconditionandtheabilitytoallocateresourcestoimmuneprocessescanprofoundlyaffecttheoutcomeofinfectionascansexageandsocialstatus(Eastetal2015Schmid-Hempel2003)Quantifying individualdifferences in theoutcomeof infec-tionanddeterminingtheimpactofinfectiononDarwinianfitnessinwildlifepopulationsmaybeachallengebecausediagnosingthein-fectionstatusforlargenumbersofindividualsisdifficultinpracticeparticularly if only non-invasive methods are available (GimenezLebreton Gaillard Choquet amp Pradel 2012 McClintock etal2010)Thisprobablyexplainswhylittle isknownaboutthesepro-cessesinnaturalenvironmentsObtainingsuchinformationishow-evercrucialtoimproveknowledgeofhostndashpathogendynamicsandpredictthelikelyimpactofdiseasesparticularlyduringepidemicsonthemostvulnerableclassesofindividualsandonpopulationlong-termviability(GervasiCivitelloKilvitisampMartin2015HawleyampAltizer2011KappelerCremerampNunn2015OliVenkataramanKleinWendlandampBrown2006)
In socialmammalswith stable dominance hierarchies an indi-vidualrsquossocialstatusregulates itsaccessto(food)resourcesandisthusoftenpositivelycorrelatedwithbothbodyconditionandfitness(Clutton-BrockampHuchard2013)Evensotherelationshipbetweenan individualrsquos social status and the outcome of infection with agivenpathogenislessstraightforwardSeveralstudiessuggestthatsociallydominantanimalsaremorefrequentlyexposedtopathogensbecausetheyareldquovaluablerdquosocialpartnerswhichexperiencehighercontact rates with conspecifics than subordinates for instancewhenformingandmaintainingsocialbonds (Seyfarth1977)Suchapositiverelationshipbetweensocialstatusandexposurehasbeenshowninseveralmammals(egMacIntoshetal2012)Ontheotherhandsubordinate individualsmaybe lessexposedbutmore likelytocontractdiseasesthandominantsandexperienceamoresevereoutcomewhen infected This is because subordinates whose ac-cesstoresourcesislimitedhaveahigherallostaticloadieahighercumulative energetic cost ofmaintaining homeostasis (Cavigelli ampChaudhry2012GoymannampWingfield2004Kappeleretal2015Sapolsky2005) and thus their allocationof resources to immuneprocesses is more often curtailed Despite considerable researchinto the influence of social processes on disease risk and spreadoftenwiththeuseofsocialnetworkanalyses(egCauchemezetal2011 Duboscq Romano V amp MacIntosh 2016 Kappeler etal
2015MacIntosh etal 2012Nunn JordaacutenMcCabe Verdolin ampFewell2015)toourknowledgefewstudiesonwildlifepopulationshaveinvestigatedtheeffectofsocialstatusonfitnessbyexplicitlyaccounting for the effect of both these processes (1) variation inexposuretoapathogen(ldquoexposurerdquohypothesis)and(2)variationintheoutcomeofinfectiondeterminedbytheopportunitytoallocateresourcestoimmuneprocesses(ldquoallocationrdquohypothesis)
Multi-event capturendashmarkndashrecapture (MECMR) models are arecent and powerful advance in statistical methods that make itpossible todisentangle theeffectofbothprocesseson the infec-tionprobabilityandtodeterminetheimpactofinfectiononsurvival(Chambertetal2012ConnampCooch2009Gimenezetal2012Pradel2005)HereweusedthisapproachtoassesstheeffectofsocialstatusinahighlysocialcarnivorethespottedhyenaCrocuta crocuta (hereafter ldquohyenardquo)oncaninedistempervirus (CDV) infec-tion during an epidemicwhen a strain pathogenic to this speciescirculated(Nikolinetal2017)CDVisahighlycontagiousvirusofa taxonomicallybroad rangeof carnivores (BeinekeBaumgaumlrtnerampWohlsein 2015 Deem Spelman Yates ampMontali 2000) TheoutcomeofCDV infection ranges fromsubclinical to fatal andaswithothermorbillivirusesindividualssurvivingtheinfectionacquirelifelongimmunity(AppelampSummers1995)AftertransmissiontoasusceptiblehostCDVtargetslymphocytesmacrophagesdendriticcells and lymphatic tissue and induces immunosuppressionwhichenhancesthespreadofCDVthroughthebloodstream(asymptom-aticandnon-contagiousstageTatsuoOnoampYanagi2001)Inthenext stageCDVenters epithelial cellswhich results in themani-festation of clinical disease and virus shedding (SawatskyWongHinkelmannCattaneoampvonMessling2012)andfinallyCDVat-tacksthecentralnervoussystemcausingneurologicalsigns(symp-tomaticandcontagiousstages)DuringallstagesCDVprofoundlysuppresseshost immune responsespredisposing infectedanimalstosecondaryinfections(Sawatskyetal2012)
In19931994avirulentCDVepidemiccausedthedeathofanestimated 30 of the African lion Panthera leo population in theSerengetiNationalPark(NP)(Roelke-Parkeretal1996)Inhyenasnoticeableldquohotspotsofinfectionrdquo(ieclinicaldiseaseandincreasedmortality)wereprimarilyobserved incubsstationedatcommunaldens(Haasetal1996)CDVstrainsthatinfectedlionsandhyenasduringthisepidemicweregeneticallydistinctfromthose infectingcanidsandencodeduniquemutationsthatmostlikelyincreasedthevirulenceofthe19931994epidemicfornon-canids(Nikolinetal2017)
In our study population low-ranking females and low-rankingmales spend a larger proportion of each year travelling long dis-tancesbetweentheclanterritoryanddistantareascontaininghighdensities of migratory prey a foraging tactic termed commuting
emspensp emsp | emsp1239Functional EcologyMARESCOT ET Al
(HoferampEast1993b)High-ranking females (HoferampEast2003)andmales(EastampHofer1991)arethuspresentmoreoftenintheclanterritorythanlow-rankingonesandhavehighintimatecontactwithclanmembersincludingcubsatthecommunalden(EastHoferampWickler1993)Furthermore themeanrateatwhichcubs sub-adults adult females and immigrant adultmales received friendlyoralcontactsaswellasbitesincreaseswiththeirsocialstatus(Eastetal2001)Similarly inanotherpopulationhigh-ranking femalesare also more gregarious than low-ranking ones forming morebonds and receivingmore frequent social support (Engh SiebertGreenberg ampHolekamp 2005 Ilany Booms ampHolekamp 2015SmithMemenisampHolekamp2007) The importanceof elevated
contact rates amonghigh-ranking clanmembers for the transmis-sion of infectious pathogens is illustrated by significantly higherseroprevalence to virus infections among high-ranking than low-rankinghyenasinourstudypopulation(Eastetal2001)aswellasin anotherone (Harrisonetal 2004)High-rankinghyenaswithintheseparatelineardominancehierarchiesamongadultfemales(plustheiroffspring)(HoferampEast2003)andamongadultreproductivelyactivemales (EastampHofer2001)havehigh ratesof contactwithclanmemberstherebyfacilitatingldquohyena-to-hyenardquoCDVtransmis-sionthroughcontactwithvirussheddingindividualsTheexposurehypothesisthereforepredictsthathigh-rankinghyenas females inparticulararemorelikelytogetinfectedwithCDVthanlow-rankingones(Figure1)
On theotherhand there is strongevidence that ahigh socialposition within the sex-specific linear dominance hierarchies hasmajorbenefitsforhyenasintermsoftheiraccesstoresourcesandfitness (Hoferamp East 2003Holekamp Smale amp Szykman 1996Houmlneretal2010)allostatic load(ldquostressrdquo) (Goymannetal2001)andallocationofresourcestoimmuneprocesses(Eastetal2015FliesMansfieldFliesGrantampHolekamp2016)Thusthealloca-tionhypothesispredictsthathigh-rankinghyenasare less likelytogetinfectedwithCDVandmorelikelytosurvivetheinfectionthanlow-rankinghyenas (Figure1) Toour knowledge our study is thefirst todisentangle the relative importanceof individual exposureandresourceallocationtoimmuneprocessesinawildlifepopulation
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy design and data collection
WecontinuouslymonitoredthreehyenaclanslocatedatthecentreoftheSerengetiNP(Eastetal2015HoferampEast1993b)between1990and2010Datawerecollectedfromallclanmembersandin-dividualswere identified by their unique spot patterns scars andothercharacteristicssuchasearnotchesClanscontainedphilopat-ricfemaleswhichbreedthroughouttheyear(HoferampEast1995)andtheiroffspringplusbreedingmalesthataremostlyimmigrants(EastampHofer2001)Femalesandtheiroffspringweresociallydomi-nantoverimmigrantmales(HoferampEast2003)Femalesandnatalmales were first detected and aged within their first few weeksof lifeaspreviouslydetailed (egHoferampEast1993a2003)Sexwasassessedatc3monthsofageusingthedimorphicglansmor-phology of the erect phallus following FrankGlickman and Licht(1991)Weaningoccursat12ndash20monthsofage(HoferampEast1995Holekampetal1996)
For healthmonitoring and disease diagnosis we recorded thestartandendofclinicalsignsofCDVForvirusscreeningwecol-lectedsalivafaecesandbloodfromknownindividualsandopportu-nisticallytissuesamplesfromdeadindividualsweencounteredthathaddiedofnaturalcausesorhadbeenhitbyvehicles
F IGURE 1emspSchematicrepresentationofhypothesespredictionsandstudydesignTopThetwohypotheses(ldquoHrdquohigh-rankingldquoLrdquolow-ranking)CentreProcessesunderlyingmodelconstructionwithinfectionprocessatthetopandobservationprocessatthebottomInfectionstates(solidcirclesS[blue]ldquosusceptiblerdquoI[orange]ldquoinfectedrdquoR[green]ldquorecoveredrdquo)andtransitionsbetweenstates(solidblackarrows)asafunctionoftheprobabilityofsurvivinginagivenstate(ϕiwithispecificforSIandR)andtheprobabilityofstayingsusceptible(1minusβ)orbecominginfected(β)Infectionstatesarelinked(dashedblackarrows)tofourevents(lefttoright)detectedindividualisassignedS(emptybluecircle)detectedindividualisassignedU(emptygreycircle)individualnotdetected(0emptyblackcircle)detectedindividualassignedI(emptyredcircle)anddetectedindividualassignedR(emptygreencircle)Withpthedetectionprobabilityδjtheprobabilityofassigninganinfectionstate( jbeingspecificforSIandR)p δjtheprobabilityofassigningadetectedindividualtoaninfectionstatep (1minusδj)theprobabilityofdetectinganindividualandassigningitUand 1 minus pjtheprobabilityofnotdetectinganindividualmdashonlyshownforSforsimplicityBottomThepredictionsofbothhypothesesintermsofprobabilityofinfection(β)andsurvival(ϕ)
H are more exposed to CDV than L because of higher contact rates with clan members
H allocate more resources to immunity than Lbecause of better access to food resources
S I RBiology
S I RObservation U 0
β φS φ I φ R
p δS
p(1-δS)
1-p
φ S (1- β)
Exposure Hypothesis Allocation Hypothesis
Model
PredictionsExposure hypothesis
- positive relationship between rank and infection probability (β) - no effect of rank on the survival probability (φ) of infected hyenas
Allocation hypothesis
- negative relationship between rank and infection probability (β) - positive relationship between rank and the survival probability (φ) of infected hyenas
H HLL L
1240emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
22emsp|emspDefinition of demographic social and infection states
Tomeettheassumptionsofcapturendashmarkndashrecapture(CMR)mod-elsonlysystematicobservationsofstudyclanmembersatcom-munal and birth dens were included For this purpose multipleobservationsof individualsduringagivenyearweresynthesizedintoasingleyearlysummaryanyclanmemberthatwasobservedat its clan communal andorbirthdensat leastonce throughouttheyearwassetasldquodetectedrdquothatyearThisdatasetincludesin-formationonthedetection(presence)ornon-detection(putativeabsence possibly death or in the case of males emigration) ofanyclanmember foreveryyearbetween1990and2010Whenan individual was detected in a given year (thereafter a ldquodetec-tionyearrdquo) itwasassigned toa specificdemographic social andinfection state accounting for uncertainty in the assignment ofthe infection state (see below ldquo223rdquo) Females andmalesweretreatedseparatelybecause thebehaviouralmechanismbywhichtheyacquireandmaintaintheirsocialstatesdifferedInadultfe-malehyenasthekeymechanismisbehaviouralsupportprovidedbycoalitionpartnersduringsocial interactions (Eastetal2009HoferampEast2003)Incontrastimmigrantmalesqueueforsocialstatus thustheirsocialstatus increaseswithclantenure (EastampHofer2001)
221emsp|emspDemographic states
Females (N = 625) were classified as cubs (C) subadults (SA)breeders (B) or non-breeders (NB) Age was determined fromdatesofwitnessedbirthsortoanaccuracyof1weekusingpel-agecharacteristicsbodysizethedegreetowhichearswereex-tended and the degree of coordination and mobility (eg EastBurkeWilhelmGreigampHofer2003HoferBenhaiemGollaampEast2016HoferampEast2003)Femalecubswereyoungerthan1yearSubadultfemaleswereagedbetween1and2yearsFemalebreedersgavebirthtoalitterduringagivenyearasdocumentedbyafreshlyrupturedclitoriscausedbyparturitions(HoferampEast1993b) andor subsequent lactationwhereas non-breeders didnotThevastmajorityoffemalebreederswerelactatingfemaleshencethisstaterepresentedtheelevatedenergeticcostoflacta-tion (Hoferetal2016)Males (N = 816)wereclassifiedascubs(C) pre-breeders (PB) or breeders (B)Male cubswere youngerthan1yearMalepre-breederswereolderthan1yearstillmem-bersoftheirnatalclanandhadnotyetstartedreproducingBothpre-breedermalesandsubadultfemalesspentmostoftheirtimeawayfromcommunaldensMalebreedersshowedreproductivebehaviour(EastampHofer2001)towardsfemaleclanmembersorwereverifiedbyDNAmicrosatelliteprofilingtohavefatheredatleastonecub(Houmlneretal2012)Breederswerepredominatelyimmigrantmalesaminorityofcases (12)were reproductivelyactivenatalmalesAsmalesdonotparticipate inparentalcarewe did not distinguish betweenmale breeder and non-breederstates
222emsp|emspSocial states
Femalesandmaleswereclassifiedaseitherhigh-ranking(H)orlow-ranking(L)basedontheirpositionsinthe(strictlylinear)adultfemaleand adult male dominance hierarchies respectivelyWe recordedsubmissivebehavioursduringdyadicadultfemalendashfemaleandadultmalendashmale interactions (egEastetal2003HoferampEast2003)andconstructedstrictlylineardominancehierarchiesforeachclanInteractionswererecordedadlibitumduringfrequentobservationperiods of c 3hr duration at bothdawn andduskmostly at clandensandduringall-nightobservationsDominancehierarchieswereadjustedaftereach lossorrecruitmentofadultsandwhendyadicinteractiondatarevealedthananindividualhadincreasedorfalleninrankTopermit thecomparisonof theranksheldby individualswithin hierarchies containing different numbers of animals withinandacrossclansandyearswecomputedforeachrankheldbyanin-dividualduringitslifetimeastandardizedrankThismeasureplacestherankswithinagivenhierarchyevenlybetweenthehighest(stand-ardizedrank+1)andthe lowest (standardizedrankminus1)rank (Eastetal 2003 Goymann etal 2001) For breeder and non-breederfemalesandbreederandpre-breedersmalesolderthan2yearsthesocialstateswerehigh-ranking(Haveragestandardizedrankrang-ingfrom001to+1)andlow-ranking(Laveragestandardizedrankrangingfromminus1to0)Ifdifferentsocialstateswereobservedforanindividualwithinayearweassignedthemostfrequentlyobservedstate(ieHorL)duringthatyearforthatindividualTheyearlypro-portionsofHandLstatesamongfemalesandamongmaleswerenotexactly50ndash50ineachclanbecause(1)wecalculatedstandard-izedranksforeachstableperiod(iewhennolossesorrecruitmentofadultstothehierarchyoccurredandtheranksheldbyindividualsdidnotchange)andeachyearwasconstitutedbyavariablenumberofsuchperiodsandbecause(2)weassignedthesocialstateofthegeneticmothertofemaleandmalecubsfemalesubadultsandmalepre-breedersyoungerthan2yearsfornon-adoptedoffspringandthatofthesurrogatemotherforadoptedoffspring(asoffspringtypi-callyacquirearankimmediatelybelowthatofthefemalethatrearedthemHoferampEast2003Eastetal2009)
223emsp|emspInfection states
Infectionstatesinbothfemalesandmaleswereassignedusingthreediagnosticprocedures(1)RT-PCRscreeningforthepresenceorab-senceofCDVRNAinsamples(seeabove)resultswereclassifiedasldquoviropositiverdquoorldquovironegativerdquorespectively(2)CDVantibodytitresinseraresultswereclassifiedldquoseropositiverdquowhenserumcontaineda significant antibody titre against CDV and ldquoseronegativerdquo whennot and (3) the observation of clinical signs associatedwithCDVinfection inhyenas and the secondary infections it causes in thisspecies(Haasetal1996alsoseeSupportingInformationsection2c)hereaftertermedldquoclinicalsignsrdquoIndividualswereassignedas
1Susceptible(S)individualswithaseronegativeresultunlessclin-ical signsandoraviropositive resultwereobservedduring the
emspensp emsp | emsp1241Functional EcologyMARESCOT ET Al
23emsp|emspMulti- event capturendashmarkndashrecapture model
Weusedamulti-eventCMR (MECMR)model (Pradel2005) fittedinE-SURGE190(ChoquetampNogue2011)toestimatesurvivalandstatetransitionprobabilities(theldquobiologicalprocessesrdquo)Thismodelpermits the estimation of such parameters whilst simultaneouslyaccountingforpotentialmethodologicalbiasesThese includegapsbetween monitoring periods left-censored data when individualswereobservedfirstasadultsatthebeginningofthestudyandright-censoreddatawhen individualswere still alive but not necessarilydetectedat theendof the study (the ldquoobservationprocessesrdquo seeSchaubGimenezSchmidtampPradel2004LebretonNicholsBarkerPradelampSpendelow2009Gimenezetal2012andFigure1foragraphicalrepresentationofthebiologicalandobservationprocesses)Thismodelalsoaccountsforthepotentially imperfectdetectionofmale hyenas that have temporarily or permanently dispersed fe-malesraisingtheiroffspringoutsidecommunaldensorfemalesstay-ingwiththemigratorypreyherdsforperiodsexceeding1year(MLEastpersonalobs)Individualsdetected(ldquocapturedrdquo)inagivenyearwereassignedan(S IorR) infectionstateifdatawereavailableoranunknowninfectionstateifdatawereunavailable(ConnampCooch2009)Moreclassicalmodelswouldnormallydiscardindividualswithunknowninfectionstatesbutthiswouldmostlikelyresultinbiases
Wefittedtwosetsofcandidatemodelsseparatelyforfemalesand males The biological processes were the product of foursquared matrices representing transitions between demographicstatessocialstatesinfectionstatesandsurvival
231emsp|emspTransitions between demographic states
ThematrixDemo(Equation1)considersthetransitionsoffemalesto three demographic states subadults (SA) breeders (B) or non-breeders(NB)
withΨthetransitionprobabilitytotheBstateaccessiblefromSAB andNB females andwith 1 minus Ψ its complement Each entry inDemoistheprobabilityoftransitionfromaldquostartingrdquodemographicstate(fourrowscorrespondingtothedemographicstatesCSABNBontheleftsideofthematrix)totheldquofollowingrdquodemographicstate(fourcolumnscorrespondingtothedemographicstatesCSABNBnotshownforsimplicity)Hereforexamplesurvivingcubs(C) (ldquostarting staterdquo) have a transition probability to the subadultstate(SA)(ldquofollowingstaterdquo)thatisequalto1Theequivalentma-trixformales ispresented intheSupporting Informationsection2fPleasenotethatΨisasymbolicnotationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
1242emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
thesocialstatesLandHnotshownforsimplicity)Pleasenotethatr is a symbolic notationhere This parameter could vary betweenstatesdependingonthemodelbeingtested
233emsp|emspTransitions between infection states
The matrix Infection (Equation3) considers the transitions of fe-malesormalestothreeinfectionstatessusceptible(S)infected(I)andrecovered(R)
withβ the infection probability (ie the probability of transitionfromasusceptibletoaninfectedstate)and1minus βitscomplementEach entry in Infection is the probability of transition from aldquostartingrdquo infection state category (three rows corresponding tothe infectionstatesS IR)toaldquofollowingrdquo infectionstate(threecolumnscorrespondingtheinfectionstatesSIRnotshownforsimplicity)PleasenotethatβisasymbolicnotationhereThispa-rametercouldvarybetweenstatesdependingonthemodelbeingtested
234emsp|emspSurvival
The matrix Survival (Equation4) accounts for the annual survivalprobabilitiesof females showsannualapparentsurvivalprobabili-tiesandis
withϕ thesurvivalprobabilityEachentry inSurvival is theprob-abilityof surviving froma ldquostartingrdquodemographicstate (four rowscorrespondingto thedemographicstatesCSABNBonthe leftsideofthematrix)DdrepresentsthetransitiontotheldquodeadrdquostateThe equivalent matrix for males is presented in the SupportingInformation section 2f Please note thatϕ is a symbolic notationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
Torepresentallpossibletransitionsbetweendemographicso-cialandinfectionstatesofsurvivingindividualswethencombinedthese matrices in a way that is fully described in the SupportingInformation
235emsp|emspGoodness- of- fit
Prior to model selection we performed a goodness-of-fit test to(1)determinewhetherourdatamettheassumptionsofCMRmod-els and (2) validate ourmodel (Grosbois etal 2008) The results
on themodel fitarepresented in theSupporting Information seesection2f
236emsp|emspModel selection
Wefitted twosetsof candidatemodels separately for femalesand males It is often recommended to parameterize the ob-servationprocess (here detection and assignment) before thebiologicalone(egCulinaLachishPradelChoquetampSheldon2013)Startingwithaconstant-onlymodelwesequentiallypa-rameterizedthe(1)assignmentofinfectionstates(2)detection(3) survival (4) infection (5) social transitions and (6) breedingtransitionstestingforeffectsofsocialdemographicandinfec-tionstatesonthoseprocessesTotestourtwomainhypothesesanddisentangletheimportanceofexposureandallocationinaf-fectingtheoutcomeofCDVinfectionwetestedfortheeffectof social states on infection probability and on the survival ofindividuals indifferent infectionstatesconfrontingour resultswith the predictions derived from each hypothesis as summa-rizedinFigure1
For the observation processes we chose models with thelowestvalueofthequasi-Akaike informationcriterioncorrectedforsmallsamplesize(QAICcHannanampQuinn1979)QAICcwasusedratherthanthecommonAICtocorrectforpotentiallyauto-correlated andoverdisperseddata (HannanampQuinn1979) Forthe biological processes bestmodelswere thosewith the larg-estnumberofparameterswithina rangeof twoQAICcunitsofdifferencefromthemodelwiththelowestQAICcvalueinordertoavoiddismissingpotentiallyimportantbiologicalpredictorsofinterest We considered that fully identifiable models differingbylt2QAICcunitsfromthemodelwiththelowestQAICcmighthavesubstantialempiricalsupportforexplainingvariationintheresponsevariable(BurnhamampAnderson2003)andreportthesealso in Table 1
3emsp |emspRESULTS
Duringthestudyperiodhyenaswereidentifiedin90ofencoun-teroccasionsThesexdemographicstateandsocialstatewereas-signedto82ofindividualsTheremainingindividuals(notdetectedatcommunaldensorwithat leastoneunclearorunknowndemo-graphicorsocialstateduringtheirencounterhistory)wereexcludedOur finaldatasetswerecomposedof625 femalesand816malesFor43offemalesand44ofmalesinformationontheirinfectionstatewasavailableonatleastoneoccasionduringtheirencounterhistoryAmongstfemales189werecubs149subadults346non-breedersand316breedersamongstmales222werecubs182pre-breedersand596breedersHigh-rankingfemalesandmaleswereslightlymorecommonlyobservedthanlow-rankingones(1542high-rankingvs1306low-rankingstatesforfemales1463high-rankingvs1167 low-rankingstates formales)Fifty-four fe-maleswere infectedwith CDV between 1991 and 1997 (86 of
(3)Infection=
S
I
R
⎡⎢⎢⎢⎣
1minusβ β 0
0 0 1
0 0 1
⎤⎥⎥⎥⎦
(4)Survival=
C
SA
B
NB
Dd
⎡⎢⎢⎢⎢⎢⎢⎣
ϕ 0 0 0 1minusϕ
0 ϕ 0 0 1minusϕ
0 0 ϕ 0 1minusϕ
0 0 0 ϕ 1minusϕ
0 0 0 0 1
⎤⎥⎥⎥⎥⎥⎥⎦
emspensp emsp | emsp1243Functional EcologyMARESCOT ET Al
321emsp|emspEffect of social status on infection probability
Social status influenced the infectionprobability of cubs andof olderindividuals (pooled subadults breeders and non-breeders) in opposite
directions(Table1)Infectionprobabilitywaslowerforhigh-rankingthanlow-ranking cubs (Table2 Figure3a) and higher for high-ranking sub-adultsbreederandnon-breederfemalesthanlow-rankingones(Table2)
322emsp|emspEffect of social status on survival of susceptible and infected females
Social status affected the survival probability of susceptible andinfected cubs (Table1)with susceptible high-ranking female cubssurviving better than susceptible low-ranking ones and infectedhigh-rankingfemalecubssurvivingbetterthaninfectedlow-rankingones (Table2 Figure3b) Similarly susceptible high-ranking sub-adultshadahighersurvivalthansusceptiblelow-rankingonesandpooled infected and recovered high-ranking subadults a slightlyhighersurvivalthanpooledinfectedandrecoveredlow-rankingsub-adults (Table2Figure3b)Bothhigh-rankingand low-rankingsus-ceptible subadults had a substantially higher survival than pooledinfected and recoveredones (Table2 Figure3b)Breeder survival
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
1238emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
1emsp |emspINTRODUC TION
Infectious diseases pose a particular threat to high-density popu-lationsandgroup-livingspecieswithhighcontactrates (HawleyampAltizer2011)Theremaybesubstantialvariationamongmembersofagroupintheirdegreeofexposuretoagivenpathogenandintheoutcomeofinfection(BeldomenicoampBegon2010VanderWaalampEzenwa2016)Bodyconditionandtheabilitytoallocateresourcestoimmuneprocessescanprofoundlyaffecttheoutcomeofinfectionascansexageandsocialstatus(Eastetal2015Schmid-Hempel2003)Quantifying individualdifferences in theoutcomeof infec-tionanddeterminingtheimpactofinfectiononDarwinianfitnessinwildlifepopulationsmaybeachallengebecausediagnosingthein-fectionstatusforlargenumbersofindividualsisdifficultinpracticeparticularly if only non-invasive methods are available (GimenezLebreton Gaillard Choquet amp Pradel 2012 McClintock etal2010)Thisprobablyexplainswhylittle isknownaboutthesepro-cessesinnaturalenvironmentsObtainingsuchinformationishow-evercrucialtoimproveknowledgeofhostndashpathogendynamicsandpredictthelikelyimpactofdiseasesparticularlyduringepidemicsonthemostvulnerableclassesofindividualsandonpopulationlong-termviability(GervasiCivitelloKilvitisampMartin2015HawleyampAltizer2011KappelerCremerampNunn2015OliVenkataramanKleinWendlandampBrown2006)
In socialmammalswith stable dominance hierarchies an indi-vidualrsquossocialstatusregulates itsaccessto(food)resourcesandisthusoftenpositivelycorrelatedwithbothbodyconditionandfitness(Clutton-BrockampHuchard2013)Evensotherelationshipbetweenan individualrsquos social status and the outcome of infection with agivenpathogenislessstraightforwardSeveralstudiessuggestthatsociallydominantanimalsaremorefrequentlyexposedtopathogensbecausetheyareldquovaluablerdquosocialpartnerswhichexperiencehighercontact rates with conspecifics than subordinates for instancewhenformingandmaintainingsocialbonds (Seyfarth1977)Suchapositiverelationshipbetweensocialstatusandexposurehasbeenshowninseveralmammals(egMacIntoshetal2012)Ontheotherhandsubordinate individualsmaybe lessexposedbutmore likelytocontractdiseasesthandominantsandexperienceamoresevereoutcomewhen infected This is because subordinates whose ac-cesstoresourcesislimitedhaveahigherallostaticloadieahighercumulative energetic cost ofmaintaining homeostasis (Cavigelli ampChaudhry2012GoymannampWingfield2004Kappeleretal2015Sapolsky2005) and thus their allocationof resources to immuneprocesses is more often curtailed Despite considerable researchinto the influence of social processes on disease risk and spreadoftenwiththeuseofsocialnetworkanalyses(egCauchemezetal2011 Duboscq Romano V amp MacIntosh 2016 Kappeler etal
2015MacIntosh etal 2012Nunn JordaacutenMcCabe Verdolin ampFewell2015)toourknowledgefewstudiesonwildlifepopulationshaveinvestigatedtheeffectofsocialstatusonfitnessbyexplicitlyaccounting for the effect of both these processes (1) variation inexposuretoapathogen(ldquoexposurerdquohypothesis)and(2)variationintheoutcomeofinfectiondeterminedbytheopportunitytoallocateresourcestoimmuneprocesses(ldquoallocationrdquohypothesis)
Multi-event capturendashmarkndashrecapture (MECMR) models are arecent and powerful advance in statistical methods that make itpossible todisentangle theeffectofbothprocesseson the infec-tionprobabilityandtodeterminetheimpactofinfectiononsurvival(Chambertetal2012ConnampCooch2009Gimenezetal2012Pradel2005)HereweusedthisapproachtoassesstheeffectofsocialstatusinahighlysocialcarnivorethespottedhyenaCrocuta crocuta (hereafter ldquohyenardquo)oncaninedistempervirus (CDV) infec-tion during an epidemicwhen a strain pathogenic to this speciescirculated(Nikolinetal2017)CDVisahighlycontagiousvirusofa taxonomicallybroad rangeof carnivores (BeinekeBaumgaumlrtnerampWohlsein 2015 Deem Spelman Yates ampMontali 2000) TheoutcomeofCDV infection ranges fromsubclinical to fatal andaswithothermorbillivirusesindividualssurvivingtheinfectionacquirelifelongimmunity(AppelampSummers1995)AftertransmissiontoasusceptiblehostCDVtargetslymphocytesmacrophagesdendriticcells and lymphatic tissue and induces immunosuppressionwhichenhancesthespreadofCDVthroughthebloodstream(asymptom-aticandnon-contagiousstageTatsuoOnoampYanagi2001)Inthenext stageCDVenters epithelial cellswhich results in themani-festation of clinical disease and virus shedding (SawatskyWongHinkelmannCattaneoampvonMessling2012)andfinallyCDVat-tacksthecentralnervoussystemcausingneurologicalsigns(symp-tomaticandcontagiousstages)DuringallstagesCDVprofoundlysuppresseshost immune responsespredisposing infectedanimalstosecondaryinfections(Sawatskyetal2012)
In19931994avirulentCDVepidemiccausedthedeathofanestimated 30 of the African lion Panthera leo population in theSerengetiNationalPark(NP)(Roelke-Parkeretal1996)Inhyenasnoticeableldquohotspotsofinfectionrdquo(ieclinicaldiseaseandincreasedmortality)wereprimarilyobserved incubsstationedatcommunaldens(Haasetal1996)CDVstrainsthatinfectedlionsandhyenasduringthisepidemicweregeneticallydistinctfromthose infectingcanidsandencodeduniquemutationsthatmostlikelyincreasedthevirulenceofthe19931994epidemicfornon-canids(Nikolinetal2017)
In our study population low-ranking females and low-rankingmales spend a larger proportion of each year travelling long dis-tancesbetweentheclanterritoryanddistantareascontaininghighdensities of migratory prey a foraging tactic termed commuting
emspensp emsp | emsp1239Functional EcologyMARESCOT ET Al
(HoferampEast1993b)High-ranking females (HoferampEast2003)andmales(EastampHofer1991)arethuspresentmoreoftenintheclanterritorythanlow-rankingonesandhavehighintimatecontactwithclanmembersincludingcubsatthecommunalden(EastHoferampWickler1993)Furthermore themeanrateatwhichcubs sub-adults adult females and immigrant adultmales received friendlyoralcontactsaswellasbitesincreaseswiththeirsocialstatus(Eastetal2001)Similarly inanotherpopulationhigh-ranking femalesare also more gregarious than low-ranking ones forming morebonds and receivingmore frequent social support (Engh SiebertGreenberg ampHolekamp 2005 Ilany Booms ampHolekamp 2015SmithMemenisampHolekamp2007) The importanceof elevated
contact rates amonghigh-ranking clanmembers for the transmis-sion of infectious pathogens is illustrated by significantly higherseroprevalence to virus infections among high-ranking than low-rankinghyenasinourstudypopulation(Eastetal2001)aswellasin anotherone (Harrisonetal 2004)High-rankinghyenaswithintheseparatelineardominancehierarchiesamongadultfemales(plustheiroffspring)(HoferampEast2003)andamongadultreproductivelyactivemales (EastampHofer2001)havehigh ratesof contactwithclanmemberstherebyfacilitatingldquohyena-to-hyenardquoCDVtransmis-sionthroughcontactwithvirussheddingindividualsTheexposurehypothesisthereforepredictsthathigh-rankinghyenas females inparticulararemorelikelytogetinfectedwithCDVthanlow-rankingones(Figure1)
On theotherhand there is strongevidence that ahigh socialposition within the sex-specific linear dominance hierarchies hasmajorbenefitsforhyenasintermsoftheiraccesstoresourcesandfitness (Hoferamp East 2003Holekamp Smale amp Szykman 1996Houmlneretal2010)allostatic load(ldquostressrdquo) (Goymannetal2001)andallocationofresourcestoimmuneprocesses(Eastetal2015FliesMansfieldFliesGrantampHolekamp2016)Thusthealloca-tionhypothesispredictsthathigh-rankinghyenasare less likelytogetinfectedwithCDVandmorelikelytosurvivetheinfectionthanlow-rankinghyenas (Figure1) Toour knowledge our study is thefirst todisentangle the relative importanceof individual exposureandresourceallocationtoimmuneprocessesinawildlifepopulation
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy design and data collection
WecontinuouslymonitoredthreehyenaclanslocatedatthecentreoftheSerengetiNP(Eastetal2015HoferampEast1993b)between1990and2010Datawerecollectedfromallclanmembersandin-dividualswere identified by their unique spot patterns scars andothercharacteristicssuchasearnotchesClanscontainedphilopat-ricfemaleswhichbreedthroughouttheyear(HoferampEast1995)andtheiroffspringplusbreedingmalesthataremostlyimmigrants(EastampHofer2001)Femalesandtheiroffspringweresociallydomi-nantoverimmigrantmales(HoferampEast2003)Femalesandnatalmales were first detected and aged within their first few weeksof lifeaspreviouslydetailed (egHoferampEast1993a2003)Sexwasassessedatc3monthsofageusingthedimorphicglansmor-phology of the erect phallus following FrankGlickman and Licht(1991)Weaningoccursat12ndash20monthsofage(HoferampEast1995Holekampetal1996)
For healthmonitoring and disease diagnosis we recorded thestartandendofclinicalsignsofCDVForvirusscreeningwecol-lectedsalivafaecesandbloodfromknownindividualsandopportu-nisticallytissuesamplesfromdeadindividualsweencounteredthathaddiedofnaturalcausesorhadbeenhitbyvehicles
F IGURE 1emspSchematicrepresentationofhypothesespredictionsandstudydesignTopThetwohypotheses(ldquoHrdquohigh-rankingldquoLrdquolow-ranking)CentreProcessesunderlyingmodelconstructionwithinfectionprocessatthetopandobservationprocessatthebottomInfectionstates(solidcirclesS[blue]ldquosusceptiblerdquoI[orange]ldquoinfectedrdquoR[green]ldquorecoveredrdquo)andtransitionsbetweenstates(solidblackarrows)asafunctionoftheprobabilityofsurvivinginagivenstate(ϕiwithispecificforSIandR)andtheprobabilityofstayingsusceptible(1minusβ)orbecominginfected(β)Infectionstatesarelinked(dashedblackarrows)tofourevents(lefttoright)detectedindividualisassignedS(emptybluecircle)detectedindividualisassignedU(emptygreycircle)individualnotdetected(0emptyblackcircle)detectedindividualassignedI(emptyredcircle)anddetectedindividualassignedR(emptygreencircle)Withpthedetectionprobabilityδjtheprobabilityofassigninganinfectionstate( jbeingspecificforSIandR)p δjtheprobabilityofassigningadetectedindividualtoaninfectionstatep (1minusδj)theprobabilityofdetectinganindividualandassigningitUand 1 minus pjtheprobabilityofnotdetectinganindividualmdashonlyshownforSforsimplicityBottomThepredictionsofbothhypothesesintermsofprobabilityofinfection(β)andsurvival(ϕ)
H are more exposed to CDV than L because of higher contact rates with clan members
H allocate more resources to immunity than Lbecause of better access to food resources
S I RBiology
S I RObservation U 0
β φS φ I φ R
p δS
p(1-δS)
1-p
φ S (1- β)
Exposure Hypothesis Allocation Hypothesis
Model
PredictionsExposure hypothesis
- positive relationship between rank and infection probability (β) - no effect of rank on the survival probability (φ) of infected hyenas
Allocation hypothesis
- negative relationship between rank and infection probability (β) - positive relationship between rank and the survival probability (φ) of infected hyenas
H HLL L
1240emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
22emsp|emspDefinition of demographic social and infection states
Tomeettheassumptionsofcapturendashmarkndashrecapture(CMR)mod-elsonlysystematicobservationsofstudyclanmembersatcom-munal and birth dens were included For this purpose multipleobservationsof individualsduringagivenyearweresynthesizedintoasingleyearlysummaryanyclanmemberthatwasobservedat its clan communal andorbirthdensat leastonce throughouttheyearwassetasldquodetectedrdquothatyearThisdatasetincludesin-formationonthedetection(presence)ornon-detection(putativeabsence possibly death or in the case of males emigration) ofanyclanmember foreveryyearbetween1990and2010Whenan individual was detected in a given year (thereafter a ldquodetec-tionyearrdquo) itwasassigned toa specificdemographic social andinfection state accounting for uncertainty in the assignment ofthe infection state (see below ldquo223rdquo) Females andmalesweretreatedseparatelybecause thebehaviouralmechanismbywhichtheyacquireandmaintaintheirsocialstatesdifferedInadultfe-malehyenasthekeymechanismisbehaviouralsupportprovidedbycoalitionpartnersduringsocial interactions (Eastetal2009HoferampEast2003)Incontrastimmigrantmalesqueueforsocialstatus thustheirsocialstatus increaseswithclantenure (EastampHofer2001)
221emsp|emspDemographic states
Females (N = 625) were classified as cubs (C) subadults (SA)breeders (B) or non-breeders (NB) Age was determined fromdatesofwitnessedbirthsortoanaccuracyof1weekusingpel-agecharacteristicsbodysizethedegreetowhichearswereex-tended and the degree of coordination and mobility (eg EastBurkeWilhelmGreigampHofer2003HoferBenhaiemGollaampEast2016HoferampEast2003)Femalecubswereyoungerthan1yearSubadultfemaleswereagedbetween1and2yearsFemalebreedersgavebirthtoalitterduringagivenyearasdocumentedbyafreshlyrupturedclitoriscausedbyparturitions(HoferampEast1993b) andor subsequent lactationwhereas non-breeders didnotThevastmajorityoffemalebreederswerelactatingfemaleshencethisstaterepresentedtheelevatedenergeticcostoflacta-tion (Hoferetal2016)Males (N = 816)wereclassifiedascubs(C) pre-breeders (PB) or breeders (B)Male cubswere youngerthan1yearMalepre-breederswereolderthan1yearstillmem-bersoftheirnatalclanandhadnotyetstartedreproducingBothpre-breedermalesandsubadultfemalesspentmostoftheirtimeawayfromcommunaldensMalebreedersshowedreproductivebehaviour(EastampHofer2001)towardsfemaleclanmembersorwereverifiedbyDNAmicrosatelliteprofilingtohavefatheredatleastonecub(Houmlneretal2012)Breederswerepredominatelyimmigrantmalesaminorityofcases (12)were reproductivelyactivenatalmalesAsmalesdonotparticipate inparentalcarewe did not distinguish betweenmale breeder and non-breederstates
222emsp|emspSocial states
Femalesandmaleswereclassifiedaseitherhigh-ranking(H)orlow-ranking(L)basedontheirpositionsinthe(strictlylinear)adultfemaleand adult male dominance hierarchies respectivelyWe recordedsubmissivebehavioursduringdyadicadultfemalendashfemaleandadultmalendashmale interactions (egEastetal2003HoferampEast2003)andconstructedstrictlylineardominancehierarchiesforeachclanInteractionswererecordedadlibitumduringfrequentobservationperiods of c 3hr duration at bothdawn andduskmostly at clandensandduringall-nightobservationsDominancehierarchieswereadjustedaftereach lossorrecruitmentofadultsandwhendyadicinteractiondatarevealedthananindividualhadincreasedorfalleninrankTopermit thecomparisonof theranksheldby individualswithin hierarchies containing different numbers of animals withinandacrossclansandyearswecomputedforeachrankheldbyanin-dividualduringitslifetimeastandardizedrankThismeasureplacestherankswithinagivenhierarchyevenlybetweenthehighest(stand-ardizedrank+1)andthe lowest (standardizedrankminus1)rank (Eastetal 2003 Goymann etal 2001) For breeder and non-breederfemalesandbreederandpre-breedersmalesolderthan2yearsthesocialstateswerehigh-ranking(Haveragestandardizedrankrang-ingfrom001to+1)andlow-ranking(Laveragestandardizedrankrangingfromminus1to0)Ifdifferentsocialstateswereobservedforanindividualwithinayearweassignedthemostfrequentlyobservedstate(ieHorL)duringthatyearforthatindividualTheyearlypro-portionsofHandLstatesamongfemalesandamongmaleswerenotexactly50ndash50ineachclanbecause(1)wecalculatedstandard-izedranksforeachstableperiod(iewhennolossesorrecruitmentofadultstothehierarchyoccurredandtheranksheldbyindividualsdidnotchange)andeachyearwasconstitutedbyavariablenumberofsuchperiodsandbecause(2)weassignedthesocialstateofthegeneticmothertofemaleandmalecubsfemalesubadultsandmalepre-breedersyoungerthan2yearsfornon-adoptedoffspringandthatofthesurrogatemotherforadoptedoffspring(asoffspringtypi-callyacquirearankimmediatelybelowthatofthefemalethatrearedthemHoferampEast2003Eastetal2009)
223emsp|emspInfection states
Infectionstatesinbothfemalesandmaleswereassignedusingthreediagnosticprocedures(1)RT-PCRscreeningforthepresenceorab-senceofCDVRNAinsamples(seeabove)resultswereclassifiedasldquoviropositiverdquoorldquovironegativerdquorespectively(2)CDVantibodytitresinseraresultswereclassifiedldquoseropositiverdquowhenserumcontaineda significant antibody titre against CDV and ldquoseronegativerdquo whennot and (3) the observation of clinical signs associatedwithCDVinfection inhyenas and the secondary infections it causes in thisspecies(Haasetal1996alsoseeSupportingInformationsection2c)hereaftertermedldquoclinicalsignsrdquoIndividualswereassignedas
1Susceptible(S)individualswithaseronegativeresultunlessclin-ical signsandoraviropositive resultwereobservedduring the
emspensp emsp | emsp1241Functional EcologyMARESCOT ET Al
23emsp|emspMulti- event capturendashmarkndashrecapture model
Weusedamulti-eventCMR (MECMR)model (Pradel2005) fittedinE-SURGE190(ChoquetampNogue2011)toestimatesurvivalandstatetransitionprobabilities(theldquobiologicalprocessesrdquo)Thismodelpermits the estimation of such parameters whilst simultaneouslyaccountingforpotentialmethodologicalbiasesThese includegapsbetween monitoring periods left-censored data when individualswereobservedfirstasadultsatthebeginningofthestudyandright-censoreddatawhen individualswere still alive but not necessarilydetectedat theendof the study (the ldquoobservationprocessesrdquo seeSchaubGimenezSchmidtampPradel2004LebretonNicholsBarkerPradelampSpendelow2009Gimenezetal2012andFigure1foragraphicalrepresentationofthebiologicalandobservationprocesses)Thismodelalsoaccountsforthepotentially imperfectdetectionofmale hyenas that have temporarily or permanently dispersed fe-malesraisingtheiroffspringoutsidecommunaldensorfemalesstay-ingwiththemigratorypreyherdsforperiodsexceeding1year(MLEastpersonalobs)Individualsdetected(ldquocapturedrdquo)inagivenyearwereassignedan(S IorR) infectionstateifdatawereavailableoranunknowninfectionstateifdatawereunavailable(ConnampCooch2009)Moreclassicalmodelswouldnormallydiscardindividualswithunknowninfectionstatesbutthiswouldmostlikelyresultinbiases
Wefittedtwosetsofcandidatemodelsseparatelyforfemalesand males The biological processes were the product of foursquared matrices representing transitions between demographicstatessocialstatesinfectionstatesandsurvival
231emsp|emspTransitions between demographic states
ThematrixDemo(Equation1)considersthetransitionsoffemalesto three demographic states subadults (SA) breeders (B) or non-breeders(NB)
withΨthetransitionprobabilitytotheBstateaccessiblefromSAB andNB females andwith 1 minus Ψ its complement Each entry inDemoistheprobabilityoftransitionfromaldquostartingrdquodemographicstate(fourrowscorrespondingtothedemographicstatesCSABNBontheleftsideofthematrix)totheldquofollowingrdquodemographicstate(fourcolumnscorrespondingtothedemographicstatesCSABNBnotshownforsimplicity)Hereforexamplesurvivingcubs(C) (ldquostarting staterdquo) have a transition probability to the subadultstate(SA)(ldquofollowingstaterdquo)thatisequalto1Theequivalentma-trixformales ispresented intheSupporting Informationsection2fPleasenotethatΨisasymbolicnotationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
1242emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
thesocialstatesLandHnotshownforsimplicity)Pleasenotethatr is a symbolic notationhere This parameter could vary betweenstatesdependingonthemodelbeingtested
233emsp|emspTransitions between infection states
The matrix Infection (Equation3) considers the transitions of fe-malesormalestothreeinfectionstatessusceptible(S)infected(I)andrecovered(R)
withβ the infection probability (ie the probability of transitionfromasusceptibletoaninfectedstate)and1minus βitscomplementEach entry in Infection is the probability of transition from aldquostartingrdquo infection state category (three rows corresponding tothe infectionstatesS IR)toaldquofollowingrdquo infectionstate(threecolumnscorrespondingtheinfectionstatesSIRnotshownforsimplicity)PleasenotethatβisasymbolicnotationhereThispa-rametercouldvarybetweenstatesdependingonthemodelbeingtested
234emsp|emspSurvival
The matrix Survival (Equation4) accounts for the annual survivalprobabilitiesof females showsannualapparentsurvivalprobabili-tiesandis
withϕ thesurvivalprobabilityEachentry inSurvival is theprob-abilityof surviving froma ldquostartingrdquodemographicstate (four rowscorrespondingto thedemographicstatesCSABNBonthe leftsideofthematrix)DdrepresentsthetransitiontotheldquodeadrdquostateThe equivalent matrix for males is presented in the SupportingInformation section 2f Please note thatϕ is a symbolic notationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
Torepresentallpossibletransitionsbetweendemographicso-cialandinfectionstatesofsurvivingindividualswethencombinedthese matrices in a way that is fully described in the SupportingInformation
235emsp|emspGoodness- of- fit
Prior to model selection we performed a goodness-of-fit test to(1)determinewhetherourdatamettheassumptionsofCMRmod-els and (2) validate ourmodel (Grosbois etal 2008) The results
on themodel fitarepresented in theSupporting Information seesection2f
236emsp|emspModel selection
Wefitted twosetsof candidatemodels separately for femalesand males It is often recommended to parameterize the ob-servationprocess (here detection and assignment) before thebiologicalone(egCulinaLachishPradelChoquetampSheldon2013)Startingwithaconstant-onlymodelwesequentiallypa-rameterizedthe(1)assignmentofinfectionstates(2)detection(3) survival (4) infection (5) social transitions and (6) breedingtransitionstestingforeffectsofsocialdemographicandinfec-tionstatesonthoseprocessesTotestourtwomainhypothesesanddisentangletheimportanceofexposureandallocationinaf-fectingtheoutcomeofCDVinfectionwetestedfortheeffectof social states on infection probability and on the survival ofindividuals indifferent infectionstatesconfrontingour resultswith the predictions derived from each hypothesis as summa-rizedinFigure1
For the observation processes we chose models with thelowestvalueofthequasi-Akaike informationcriterioncorrectedforsmallsamplesize(QAICcHannanampQuinn1979)QAICcwasusedratherthanthecommonAICtocorrectforpotentiallyauto-correlated andoverdisperseddata (HannanampQuinn1979) Forthe biological processes bestmodelswere thosewith the larg-estnumberofparameterswithina rangeof twoQAICcunitsofdifferencefromthemodelwiththelowestQAICcvalueinordertoavoiddismissingpotentiallyimportantbiologicalpredictorsofinterest We considered that fully identifiable models differingbylt2QAICcunitsfromthemodelwiththelowestQAICcmighthavesubstantialempiricalsupportforexplainingvariationintheresponsevariable(BurnhamampAnderson2003)andreportthesealso in Table 1
3emsp |emspRESULTS
Duringthestudyperiodhyenaswereidentifiedin90ofencoun-teroccasionsThesexdemographicstateandsocialstatewereas-signedto82ofindividualsTheremainingindividuals(notdetectedatcommunaldensorwithat leastoneunclearorunknowndemo-graphicorsocialstateduringtheirencounterhistory)wereexcludedOur finaldatasetswerecomposedof625 femalesand816malesFor43offemalesand44ofmalesinformationontheirinfectionstatewasavailableonatleastoneoccasionduringtheirencounterhistoryAmongstfemales189werecubs149subadults346non-breedersand316breedersamongstmales222werecubs182pre-breedersand596breedersHigh-rankingfemalesandmaleswereslightlymorecommonlyobservedthanlow-rankingones(1542high-rankingvs1306low-rankingstatesforfemales1463high-rankingvs1167 low-rankingstates formales)Fifty-four fe-maleswere infectedwith CDV between 1991 and 1997 (86 of
(3)Infection=
S
I
R
⎡⎢⎢⎢⎣
1minusβ β 0
0 0 1
0 0 1
⎤⎥⎥⎥⎦
(4)Survival=
C
SA
B
NB
Dd
⎡⎢⎢⎢⎢⎢⎢⎣
ϕ 0 0 0 1minusϕ
0 ϕ 0 0 1minusϕ
0 0 ϕ 0 1minusϕ
0 0 0 ϕ 1minusϕ
0 0 0 0 1
⎤⎥⎥⎥⎥⎥⎥⎦
emspensp emsp | emsp1243Functional EcologyMARESCOT ET Al
321emsp|emspEffect of social status on infection probability
Social status influenced the infectionprobability of cubs andof olderindividuals (pooled subadults breeders and non-breeders) in opposite
directions(Table1)Infectionprobabilitywaslowerforhigh-rankingthanlow-ranking cubs (Table2 Figure3a) and higher for high-ranking sub-adultsbreederandnon-breederfemalesthanlow-rankingones(Table2)
322emsp|emspEffect of social status on survival of susceptible and infected females
Social status affected the survival probability of susceptible andinfected cubs (Table1)with susceptible high-ranking female cubssurviving better than susceptible low-ranking ones and infectedhigh-rankingfemalecubssurvivingbetterthaninfectedlow-rankingones (Table2 Figure3b) Similarly susceptible high-ranking sub-adultshadahighersurvivalthansusceptiblelow-rankingonesandpooled infected and recovered high-ranking subadults a slightlyhighersurvivalthanpooledinfectedandrecoveredlow-rankingsub-adults (Table2Figure3b)Bothhigh-rankingand low-rankingsus-ceptible subadults had a substantially higher survival than pooledinfected and recoveredones (Table2 Figure3b)Breeder survival
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
emspensp emsp | emsp1239Functional EcologyMARESCOT ET Al
(HoferampEast1993b)High-ranking females (HoferampEast2003)andmales(EastampHofer1991)arethuspresentmoreoftenintheclanterritorythanlow-rankingonesandhavehighintimatecontactwithclanmembersincludingcubsatthecommunalden(EastHoferampWickler1993)Furthermore themeanrateatwhichcubs sub-adults adult females and immigrant adultmales received friendlyoralcontactsaswellasbitesincreaseswiththeirsocialstatus(Eastetal2001)Similarly inanotherpopulationhigh-ranking femalesare also more gregarious than low-ranking ones forming morebonds and receivingmore frequent social support (Engh SiebertGreenberg ampHolekamp 2005 Ilany Booms ampHolekamp 2015SmithMemenisampHolekamp2007) The importanceof elevated
contact rates amonghigh-ranking clanmembers for the transmis-sion of infectious pathogens is illustrated by significantly higherseroprevalence to virus infections among high-ranking than low-rankinghyenasinourstudypopulation(Eastetal2001)aswellasin anotherone (Harrisonetal 2004)High-rankinghyenaswithintheseparatelineardominancehierarchiesamongadultfemales(plustheiroffspring)(HoferampEast2003)andamongadultreproductivelyactivemales (EastampHofer2001)havehigh ratesof contactwithclanmemberstherebyfacilitatingldquohyena-to-hyenardquoCDVtransmis-sionthroughcontactwithvirussheddingindividualsTheexposurehypothesisthereforepredictsthathigh-rankinghyenas females inparticulararemorelikelytogetinfectedwithCDVthanlow-rankingones(Figure1)
On theotherhand there is strongevidence that ahigh socialposition within the sex-specific linear dominance hierarchies hasmajorbenefitsforhyenasintermsoftheiraccesstoresourcesandfitness (Hoferamp East 2003Holekamp Smale amp Szykman 1996Houmlneretal2010)allostatic load(ldquostressrdquo) (Goymannetal2001)andallocationofresourcestoimmuneprocesses(Eastetal2015FliesMansfieldFliesGrantampHolekamp2016)Thusthealloca-tionhypothesispredictsthathigh-rankinghyenasare less likelytogetinfectedwithCDVandmorelikelytosurvivetheinfectionthanlow-rankinghyenas (Figure1) Toour knowledge our study is thefirst todisentangle the relative importanceof individual exposureandresourceallocationtoimmuneprocessesinawildlifepopulation
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy design and data collection
WecontinuouslymonitoredthreehyenaclanslocatedatthecentreoftheSerengetiNP(Eastetal2015HoferampEast1993b)between1990and2010Datawerecollectedfromallclanmembersandin-dividualswere identified by their unique spot patterns scars andothercharacteristicssuchasearnotchesClanscontainedphilopat-ricfemaleswhichbreedthroughouttheyear(HoferampEast1995)andtheiroffspringplusbreedingmalesthataremostlyimmigrants(EastampHofer2001)Femalesandtheiroffspringweresociallydomi-nantoverimmigrantmales(HoferampEast2003)Femalesandnatalmales were first detected and aged within their first few weeksof lifeaspreviouslydetailed (egHoferampEast1993a2003)Sexwasassessedatc3monthsofageusingthedimorphicglansmor-phology of the erect phallus following FrankGlickman and Licht(1991)Weaningoccursat12ndash20monthsofage(HoferampEast1995Holekampetal1996)
For healthmonitoring and disease diagnosis we recorded thestartandendofclinicalsignsofCDVForvirusscreeningwecol-lectedsalivafaecesandbloodfromknownindividualsandopportu-nisticallytissuesamplesfromdeadindividualsweencounteredthathaddiedofnaturalcausesorhadbeenhitbyvehicles
F IGURE 1emspSchematicrepresentationofhypothesespredictionsandstudydesignTopThetwohypotheses(ldquoHrdquohigh-rankingldquoLrdquolow-ranking)CentreProcessesunderlyingmodelconstructionwithinfectionprocessatthetopandobservationprocessatthebottomInfectionstates(solidcirclesS[blue]ldquosusceptiblerdquoI[orange]ldquoinfectedrdquoR[green]ldquorecoveredrdquo)andtransitionsbetweenstates(solidblackarrows)asafunctionoftheprobabilityofsurvivinginagivenstate(ϕiwithispecificforSIandR)andtheprobabilityofstayingsusceptible(1minusβ)orbecominginfected(β)Infectionstatesarelinked(dashedblackarrows)tofourevents(lefttoright)detectedindividualisassignedS(emptybluecircle)detectedindividualisassignedU(emptygreycircle)individualnotdetected(0emptyblackcircle)detectedindividualassignedI(emptyredcircle)anddetectedindividualassignedR(emptygreencircle)Withpthedetectionprobabilityδjtheprobabilityofassigninganinfectionstate( jbeingspecificforSIandR)p δjtheprobabilityofassigningadetectedindividualtoaninfectionstatep (1minusδj)theprobabilityofdetectinganindividualandassigningitUand 1 minus pjtheprobabilityofnotdetectinganindividualmdashonlyshownforSforsimplicityBottomThepredictionsofbothhypothesesintermsofprobabilityofinfection(β)andsurvival(ϕ)
H are more exposed to CDV than L because of higher contact rates with clan members
H allocate more resources to immunity than Lbecause of better access to food resources
S I RBiology
S I RObservation U 0
β φS φ I φ R
p δS
p(1-δS)
1-p
φ S (1- β)
Exposure Hypothesis Allocation Hypothesis
Model
PredictionsExposure hypothesis
- positive relationship between rank and infection probability (β) - no effect of rank on the survival probability (φ) of infected hyenas
Allocation hypothesis
- negative relationship between rank and infection probability (β) - positive relationship between rank and the survival probability (φ) of infected hyenas
H HLL L
1240emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
22emsp|emspDefinition of demographic social and infection states
Tomeettheassumptionsofcapturendashmarkndashrecapture(CMR)mod-elsonlysystematicobservationsofstudyclanmembersatcom-munal and birth dens were included For this purpose multipleobservationsof individualsduringagivenyearweresynthesizedintoasingleyearlysummaryanyclanmemberthatwasobservedat its clan communal andorbirthdensat leastonce throughouttheyearwassetasldquodetectedrdquothatyearThisdatasetincludesin-formationonthedetection(presence)ornon-detection(putativeabsence possibly death or in the case of males emigration) ofanyclanmember foreveryyearbetween1990and2010Whenan individual was detected in a given year (thereafter a ldquodetec-tionyearrdquo) itwasassigned toa specificdemographic social andinfection state accounting for uncertainty in the assignment ofthe infection state (see below ldquo223rdquo) Females andmalesweretreatedseparatelybecause thebehaviouralmechanismbywhichtheyacquireandmaintaintheirsocialstatesdifferedInadultfe-malehyenasthekeymechanismisbehaviouralsupportprovidedbycoalitionpartnersduringsocial interactions (Eastetal2009HoferampEast2003)Incontrastimmigrantmalesqueueforsocialstatus thustheirsocialstatus increaseswithclantenure (EastampHofer2001)
221emsp|emspDemographic states
Females (N = 625) were classified as cubs (C) subadults (SA)breeders (B) or non-breeders (NB) Age was determined fromdatesofwitnessedbirthsortoanaccuracyof1weekusingpel-agecharacteristicsbodysizethedegreetowhichearswereex-tended and the degree of coordination and mobility (eg EastBurkeWilhelmGreigampHofer2003HoferBenhaiemGollaampEast2016HoferampEast2003)Femalecubswereyoungerthan1yearSubadultfemaleswereagedbetween1and2yearsFemalebreedersgavebirthtoalitterduringagivenyearasdocumentedbyafreshlyrupturedclitoriscausedbyparturitions(HoferampEast1993b) andor subsequent lactationwhereas non-breeders didnotThevastmajorityoffemalebreederswerelactatingfemaleshencethisstaterepresentedtheelevatedenergeticcostoflacta-tion (Hoferetal2016)Males (N = 816)wereclassifiedascubs(C) pre-breeders (PB) or breeders (B)Male cubswere youngerthan1yearMalepre-breederswereolderthan1yearstillmem-bersoftheirnatalclanandhadnotyetstartedreproducingBothpre-breedermalesandsubadultfemalesspentmostoftheirtimeawayfromcommunaldensMalebreedersshowedreproductivebehaviour(EastampHofer2001)towardsfemaleclanmembersorwereverifiedbyDNAmicrosatelliteprofilingtohavefatheredatleastonecub(Houmlneretal2012)Breederswerepredominatelyimmigrantmalesaminorityofcases (12)were reproductivelyactivenatalmalesAsmalesdonotparticipate inparentalcarewe did not distinguish betweenmale breeder and non-breederstates
222emsp|emspSocial states
Femalesandmaleswereclassifiedaseitherhigh-ranking(H)orlow-ranking(L)basedontheirpositionsinthe(strictlylinear)adultfemaleand adult male dominance hierarchies respectivelyWe recordedsubmissivebehavioursduringdyadicadultfemalendashfemaleandadultmalendashmale interactions (egEastetal2003HoferampEast2003)andconstructedstrictlylineardominancehierarchiesforeachclanInteractionswererecordedadlibitumduringfrequentobservationperiods of c 3hr duration at bothdawn andduskmostly at clandensandduringall-nightobservationsDominancehierarchieswereadjustedaftereach lossorrecruitmentofadultsandwhendyadicinteractiondatarevealedthananindividualhadincreasedorfalleninrankTopermit thecomparisonof theranksheldby individualswithin hierarchies containing different numbers of animals withinandacrossclansandyearswecomputedforeachrankheldbyanin-dividualduringitslifetimeastandardizedrankThismeasureplacestherankswithinagivenhierarchyevenlybetweenthehighest(stand-ardizedrank+1)andthe lowest (standardizedrankminus1)rank (Eastetal 2003 Goymann etal 2001) For breeder and non-breederfemalesandbreederandpre-breedersmalesolderthan2yearsthesocialstateswerehigh-ranking(Haveragestandardizedrankrang-ingfrom001to+1)andlow-ranking(Laveragestandardizedrankrangingfromminus1to0)Ifdifferentsocialstateswereobservedforanindividualwithinayearweassignedthemostfrequentlyobservedstate(ieHorL)duringthatyearforthatindividualTheyearlypro-portionsofHandLstatesamongfemalesandamongmaleswerenotexactly50ndash50ineachclanbecause(1)wecalculatedstandard-izedranksforeachstableperiod(iewhennolossesorrecruitmentofadultstothehierarchyoccurredandtheranksheldbyindividualsdidnotchange)andeachyearwasconstitutedbyavariablenumberofsuchperiodsandbecause(2)weassignedthesocialstateofthegeneticmothertofemaleandmalecubsfemalesubadultsandmalepre-breedersyoungerthan2yearsfornon-adoptedoffspringandthatofthesurrogatemotherforadoptedoffspring(asoffspringtypi-callyacquirearankimmediatelybelowthatofthefemalethatrearedthemHoferampEast2003Eastetal2009)
223emsp|emspInfection states
Infectionstatesinbothfemalesandmaleswereassignedusingthreediagnosticprocedures(1)RT-PCRscreeningforthepresenceorab-senceofCDVRNAinsamples(seeabove)resultswereclassifiedasldquoviropositiverdquoorldquovironegativerdquorespectively(2)CDVantibodytitresinseraresultswereclassifiedldquoseropositiverdquowhenserumcontaineda significant antibody titre against CDV and ldquoseronegativerdquo whennot and (3) the observation of clinical signs associatedwithCDVinfection inhyenas and the secondary infections it causes in thisspecies(Haasetal1996alsoseeSupportingInformationsection2c)hereaftertermedldquoclinicalsignsrdquoIndividualswereassignedas
1Susceptible(S)individualswithaseronegativeresultunlessclin-ical signsandoraviropositive resultwereobservedduring the
emspensp emsp | emsp1241Functional EcologyMARESCOT ET Al
23emsp|emspMulti- event capturendashmarkndashrecapture model
Weusedamulti-eventCMR (MECMR)model (Pradel2005) fittedinE-SURGE190(ChoquetampNogue2011)toestimatesurvivalandstatetransitionprobabilities(theldquobiologicalprocessesrdquo)Thismodelpermits the estimation of such parameters whilst simultaneouslyaccountingforpotentialmethodologicalbiasesThese includegapsbetween monitoring periods left-censored data when individualswereobservedfirstasadultsatthebeginningofthestudyandright-censoreddatawhen individualswere still alive but not necessarilydetectedat theendof the study (the ldquoobservationprocessesrdquo seeSchaubGimenezSchmidtampPradel2004LebretonNicholsBarkerPradelampSpendelow2009Gimenezetal2012andFigure1foragraphicalrepresentationofthebiologicalandobservationprocesses)Thismodelalsoaccountsforthepotentially imperfectdetectionofmale hyenas that have temporarily or permanently dispersed fe-malesraisingtheiroffspringoutsidecommunaldensorfemalesstay-ingwiththemigratorypreyherdsforperiodsexceeding1year(MLEastpersonalobs)Individualsdetected(ldquocapturedrdquo)inagivenyearwereassignedan(S IorR) infectionstateifdatawereavailableoranunknowninfectionstateifdatawereunavailable(ConnampCooch2009)Moreclassicalmodelswouldnormallydiscardindividualswithunknowninfectionstatesbutthiswouldmostlikelyresultinbiases
Wefittedtwosetsofcandidatemodelsseparatelyforfemalesand males The biological processes were the product of foursquared matrices representing transitions between demographicstatessocialstatesinfectionstatesandsurvival
231emsp|emspTransitions between demographic states
ThematrixDemo(Equation1)considersthetransitionsoffemalesto three demographic states subadults (SA) breeders (B) or non-breeders(NB)
withΨthetransitionprobabilitytotheBstateaccessiblefromSAB andNB females andwith 1 minus Ψ its complement Each entry inDemoistheprobabilityoftransitionfromaldquostartingrdquodemographicstate(fourrowscorrespondingtothedemographicstatesCSABNBontheleftsideofthematrix)totheldquofollowingrdquodemographicstate(fourcolumnscorrespondingtothedemographicstatesCSABNBnotshownforsimplicity)Hereforexamplesurvivingcubs(C) (ldquostarting staterdquo) have a transition probability to the subadultstate(SA)(ldquofollowingstaterdquo)thatisequalto1Theequivalentma-trixformales ispresented intheSupporting Informationsection2fPleasenotethatΨisasymbolicnotationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
1242emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
thesocialstatesLandHnotshownforsimplicity)Pleasenotethatr is a symbolic notationhere This parameter could vary betweenstatesdependingonthemodelbeingtested
233emsp|emspTransitions between infection states
The matrix Infection (Equation3) considers the transitions of fe-malesormalestothreeinfectionstatessusceptible(S)infected(I)andrecovered(R)
withβ the infection probability (ie the probability of transitionfromasusceptibletoaninfectedstate)and1minus βitscomplementEach entry in Infection is the probability of transition from aldquostartingrdquo infection state category (three rows corresponding tothe infectionstatesS IR)toaldquofollowingrdquo infectionstate(threecolumnscorrespondingtheinfectionstatesSIRnotshownforsimplicity)PleasenotethatβisasymbolicnotationhereThispa-rametercouldvarybetweenstatesdependingonthemodelbeingtested
234emsp|emspSurvival
The matrix Survival (Equation4) accounts for the annual survivalprobabilitiesof females showsannualapparentsurvivalprobabili-tiesandis
withϕ thesurvivalprobabilityEachentry inSurvival is theprob-abilityof surviving froma ldquostartingrdquodemographicstate (four rowscorrespondingto thedemographicstatesCSABNBonthe leftsideofthematrix)DdrepresentsthetransitiontotheldquodeadrdquostateThe equivalent matrix for males is presented in the SupportingInformation section 2f Please note thatϕ is a symbolic notationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
Torepresentallpossibletransitionsbetweendemographicso-cialandinfectionstatesofsurvivingindividualswethencombinedthese matrices in a way that is fully described in the SupportingInformation
235emsp|emspGoodness- of- fit
Prior to model selection we performed a goodness-of-fit test to(1)determinewhetherourdatamettheassumptionsofCMRmod-els and (2) validate ourmodel (Grosbois etal 2008) The results
on themodel fitarepresented in theSupporting Information seesection2f
236emsp|emspModel selection
Wefitted twosetsof candidatemodels separately for femalesand males It is often recommended to parameterize the ob-servationprocess (here detection and assignment) before thebiologicalone(egCulinaLachishPradelChoquetampSheldon2013)Startingwithaconstant-onlymodelwesequentiallypa-rameterizedthe(1)assignmentofinfectionstates(2)detection(3) survival (4) infection (5) social transitions and (6) breedingtransitionstestingforeffectsofsocialdemographicandinfec-tionstatesonthoseprocessesTotestourtwomainhypothesesanddisentangletheimportanceofexposureandallocationinaf-fectingtheoutcomeofCDVinfectionwetestedfortheeffectof social states on infection probability and on the survival ofindividuals indifferent infectionstatesconfrontingour resultswith the predictions derived from each hypothesis as summa-rizedinFigure1
For the observation processes we chose models with thelowestvalueofthequasi-Akaike informationcriterioncorrectedforsmallsamplesize(QAICcHannanampQuinn1979)QAICcwasusedratherthanthecommonAICtocorrectforpotentiallyauto-correlated andoverdisperseddata (HannanampQuinn1979) Forthe biological processes bestmodelswere thosewith the larg-estnumberofparameterswithina rangeof twoQAICcunitsofdifferencefromthemodelwiththelowestQAICcvalueinordertoavoiddismissingpotentiallyimportantbiologicalpredictorsofinterest We considered that fully identifiable models differingbylt2QAICcunitsfromthemodelwiththelowestQAICcmighthavesubstantialempiricalsupportforexplainingvariationintheresponsevariable(BurnhamampAnderson2003)andreportthesealso in Table 1
3emsp |emspRESULTS
Duringthestudyperiodhyenaswereidentifiedin90ofencoun-teroccasionsThesexdemographicstateandsocialstatewereas-signedto82ofindividualsTheremainingindividuals(notdetectedatcommunaldensorwithat leastoneunclearorunknowndemo-graphicorsocialstateduringtheirencounterhistory)wereexcludedOur finaldatasetswerecomposedof625 femalesand816malesFor43offemalesand44ofmalesinformationontheirinfectionstatewasavailableonatleastoneoccasionduringtheirencounterhistoryAmongstfemales189werecubs149subadults346non-breedersand316breedersamongstmales222werecubs182pre-breedersand596breedersHigh-rankingfemalesandmaleswereslightlymorecommonlyobservedthanlow-rankingones(1542high-rankingvs1306low-rankingstatesforfemales1463high-rankingvs1167 low-rankingstates formales)Fifty-four fe-maleswere infectedwith CDV between 1991 and 1997 (86 of
(3)Infection=
S
I
R
⎡⎢⎢⎢⎣
1minusβ β 0
0 0 1
0 0 1
⎤⎥⎥⎥⎦
(4)Survival=
C
SA
B
NB
Dd
⎡⎢⎢⎢⎢⎢⎢⎣
ϕ 0 0 0 1minusϕ
0 ϕ 0 0 1minusϕ
0 0 ϕ 0 1minusϕ
0 0 0 ϕ 1minusϕ
0 0 0 0 1
⎤⎥⎥⎥⎥⎥⎥⎦
emspensp emsp | emsp1243Functional EcologyMARESCOT ET Al
321emsp|emspEffect of social status on infection probability
Social status influenced the infectionprobability of cubs andof olderindividuals (pooled subadults breeders and non-breeders) in opposite
directions(Table1)Infectionprobabilitywaslowerforhigh-rankingthanlow-ranking cubs (Table2 Figure3a) and higher for high-ranking sub-adultsbreederandnon-breederfemalesthanlow-rankingones(Table2)
322emsp|emspEffect of social status on survival of susceptible and infected females
Social status affected the survival probability of susceptible andinfected cubs (Table1)with susceptible high-ranking female cubssurviving better than susceptible low-ranking ones and infectedhigh-rankingfemalecubssurvivingbetterthaninfectedlow-rankingones (Table2 Figure3b) Similarly susceptible high-ranking sub-adultshadahighersurvivalthansusceptiblelow-rankingonesandpooled infected and recovered high-ranking subadults a slightlyhighersurvivalthanpooledinfectedandrecoveredlow-rankingsub-adults (Table2Figure3b)Bothhigh-rankingand low-rankingsus-ceptible subadults had a substantially higher survival than pooledinfected and recoveredones (Table2 Figure3b)Breeder survival
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
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emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
1240emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
22emsp|emspDefinition of demographic social and infection states
Tomeettheassumptionsofcapturendashmarkndashrecapture(CMR)mod-elsonlysystematicobservationsofstudyclanmembersatcom-munal and birth dens were included For this purpose multipleobservationsof individualsduringagivenyearweresynthesizedintoasingleyearlysummaryanyclanmemberthatwasobservedat its clan communal andorbirthdensat leastonce throughouttheyearwassetasldquodetectedrdquothatyearThisdatasetincludesin-formationonthedetection(presence)ornon-detection(putativeabsence possibly death or in the case of males emigration) ofanyclanmember foreveryyearbetween1990and2010Whenan individual was detected in a given year (thereafter a ldquodetec-tionyearrdquo) itwasassigned toa specificdemographic social andinfection state accounting for uncertainty in the assignment ofthe infection state (see below ldquo223rdquo) Females andmalesweretreatedseparatelybecause thebehaviouralmechanismbywhichtheyacquireandmaintaintheirsocialstatesdifferedInadultfe-malehyenasthekeymechanismisbehaviouralsupportprovidedbycoalitionpartnersduringsocial interactions (Eastetal2009HoferampEast2003)Incontrastimmigrantmalesqueueforsocialstatus thustheirsocialstatus increaseswithclantenure (EastampHofer2001)
221emsp|emspDemographic states
Females (N = 625) were classified as cubs (C) subadults (SA)breeders (B) or non-breeders (NB) Age was determined fromdatesofwitnessedbirthsortoanaccuracyof1weekusingpel-agecharacteristicsbodysizethedegreetowhichearswereex-tended and the degree of coordination and mobility (eg EastBurkeWilhelmGreigampHofer2003HoferBenhaiemGollaampEast2016HoferampEast2003)Femalecubswereyoungerthan1yearSubadultfemaleswereagedbetween1and2yearsFemalebreedersgavebirthtoalitterduringagivenyearasdocumentedbyafreshlyrupturedclitoriscausedbyparturitions(HoferampEast1993b) andor subsequent lactationwhereas non-breeders didnotThevastmajorityoffemalebreederswerelactatingfemaleshencethisstaterepresentedtheelevatedenergeticcostoflacta-tion (Hoferetal2016)Males (N = 816)wereclassifiedascubs(C) pre-breeders (PB) or breeders (B)Male cubswere youngerthan1yearMalepre-breederswereolderthan1yearstillmem-bersoftheirnatalclanandhadnotyetstartedreproducingBothpre-breedermalesandsubadultfemalesspentmostoftheirtimeawayfromcommunaldensMalebreedersshowedreproductivebehaviour(EastampHofer2001)towardsfemaleclanmembersorwereverifiedbyDNAmicrosatelliteprofilingtohavefatheredatleastonecub(Houmlneretal2012)Breederswerepredominatelyimmigrantmalesaminorityofcases (12)were reproductivelyactivenatalmalesAsmalesdonotparticipate inparentalcarewe did not distinguish betweenmale breeder and non-breederstates
222emsp|emspSocial states
Femalesandmaleswereclassifiedaseitherhigh-ranking(H)orlow-ranking(L)basedontheirpositionsinthe(strictlylinear)adultfemaleand adult male dominance hierarchies respectivelyWe recordedsubmissivebehavioursduringdyadicadultfemalendashfemaleandadultmalendashmale interactions (egEastetal2003HoferampEast2003)andconstructedstrictlylineardominancehierarchiesforeachclanInteractionswererecordedadlibitumduringfrequentobservationperiods of c 3hr duration at bothdawn andduskmostly at clandensandduringall-nightobservationsDominancehierarchieswereadjustedaftereach lossorrecruitmentofadultsandwhendyadicinteractiondatarevealedthananindividualhadincreasedorfalleninrankTopermit thecomparisonof theranksheldby individualswithin hierarchies containing different numbers of animals withinandacrossclansandyearswecomputedforeachrankheldbyanin-dividualduringitslifetimeastandardizedrankThismeasureplacestherankswithinagivenhierarchyevenlybetweenthehighest(stand-ardizedrank+1)andthe lowest (standardizedrankminus1)rank (Eastetal 2003 Goymann etal 2001) For breeder and non-breederfemalesandbreederandpre-breedersmalesolderthan2yearsthesocialstateswerehigh-ranking(Haveragestandardizedrankrang-ingfrom001to+1)andlow-ranking(Laveragestandardizedrankrangingfromminus1to0)Ifdifferentsocialstateswereobservedforanindividualwithinayearweassignedthemostfrequentlyobservedstate(ieHorL)duringthatyearforthatindividualTheyearlypro-portionsofHandLstatesamongfemalesandamongmaleswerenotexactly50ndash50ineachclanbecause(1)wecalculatedstandard-izedranksforeachstableperiod(iewhennolossesorrecruitmentofadultstothehierarchyoccurredandtheranksheldbyindividualsdidnotchange)andeachyearwasconstitutedbyavariablenumberofsuchperiodsandbecause(2)weassignedthesocialstateofthegeneticmothertofemaleandmalecubsfemalesubadultsandmalepre-breedersyoungerthan2yearsfornon-adoptedoffspringandthatofthesurrogatemotherforadoptedoffspring(asoffspringtypi-callyacquirearankimmediatelybelowthatofthefemalethatrearedthemHoferampEast2003Eastetal2009)
223emsp|emspInfection states
Infectionstatesinbothfemalesandmaleswereassignedusingthreediagnosticprocedures(1)RT-PCRscreeningforthepresenceorab-senceofCDVRNAinsamples(seeabove)resultswereclassifiedasldquoviropositiverdquoorldquovironegativerdquorespectively(2)CDVantibodytitresinseraresultswereclassifiedldquoseropositiverdquowhenserumcontaineda significant antibody titre against CDV and ldquoseronegativerdquo whennot and (3) the observation of clinical signs associatedwithCDVinfection inhyenas and the secondary infections it causes in thisspecies(Haasetal1996alsoseeSupportingInformationsection2c)hereaftertermedldquoclinicalsignsrdquoIndividualswereassignedas
1Susceptible(S)individualswithaseronegativeresultunlessclin-ical signsandoraviropositive resultwereobservedduring the
emspensp emsp | emsp1241Functional EcologyMARESCOT ET Al
23emsp|emspMulti- event capturendashmarkndashrecapture model
Weusedamulti-eventCMR (MECMR)model (Pradel2005) fittedinE-SURGE190(ChoquetampNogue2011)toestimatesurvivalandstatetransitionprobabilities(theldquobiologicalprocessesrdquo)Thismodelpermits the estimation of such parameters whilst simultaneouslyaccountingforpotentialmethodologicalbiasesThese includegapsbetween monitoring periods left-censored data when individualswereobservedfirstasadultsatthebeginningofthestudyandright-censoreddatawhen individualswere still alive but not necessarilydetectedat theendof the study (the ldquoobservationprocessesrdquo seeSchaubGimenezSchmidtampPradel2004LebretonNicholsBarkerPradelampSpendelow2009Gimenezetal2012andFigure1foragraphicalrepresentationofthebiologicalandobservationprocesses)Thismodelalsoaccountsforthepotentially imperfectdetectionofmale hyenas that have temporarily or permanently dispersed fe-malesraisingtheiroffspringoutsidecommunaldensorfemalesstay-ingwiththemigratorypreyherdsforperiodsexceeding1year(MLEastpersonalobs)Individualsdetected(ldquocapturedrdquo)inagivenyearwereassignedan(S IorR) infectionstateifdatawereavailableoranunknowninfectionstateifdatawereunavailable(ConnampCooch2009)Moreclassicalmodelswouldnormallydiscardindividualswithunknowninfectionstatesbutthiswouldmostlikelyresultinbiases
Wefittedtwosetsofcandidatemodelsseparatelyforfemalesand males The biological processes were the product of foursquared matrices representing transitions between demographicstatessocialstatesinfectionstatesandsurvival
231emsp|emspTransitions between demographic states
ThematrixDemo(Equation1)considersthetransitionsoffemalesto three demographic states subadults (SA) breeders (B) or non-breeders(NB)
withΨthetransitionprobabilitytotheBstateaccessiblefromSAB andNB females andwith 1 minus Ψ its complement Each entry inDemoistheprobabilityoftransitionfromaldquostartingrdquodemographicstate(fourrowscorrespondingtothedemographicstatesCSABNBontheleftsideofthematrix)totheldquofollowingrdquodemographicstate(fourcolumnscorrespondingtothedemographicstatesCSABNBnotshownforsimplicity)Hereforexamplesurvivingcubs(C) (ldquostarting staterdquo) have a transition probability to the subadultstate(SA)(ldquofollowingstaterdquo)thatisequalto1Theequivalentma-trixformales ispresented intheSupporting Informationsection2fPleasenotethatΨisasymbolicnotationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
1242emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
thesocialstatesLandHnotshownforsimplicity)Pleasenotethatr is a symbolic notationhere This parameter could vary betweenstatesdependingonthemodelbeingtested
233emsp|emspTransitions between infection states
The matrix Infection (Equation3) considers the transitions of fe-malesormalestothreeinfectionstatessusceptible(S)infected(I)andrecovered(R)
withβ the infection probability (ie the probability of transitionfromasusceptibletoaninfectedstate)and1minus βitscomplementEach entry in Infection is the probability of transition from aldquostartingrdquo infection state category (three rows corresponding tothe infectionstatesS IR)toaldquofollowingrdquo infectionstate(threecolumnscorrespondingtheinfectionstatesSIRnotshownforsimplicity)PleasenotethatβisasymbolicnotationhereThispa-rametercouldvarybetweenstatesdependingonthemodelbeingtested
234emsp|emspSurvival
The matrix Survival (Equation4) accounts for the annual survivalprobabilitiesof females showsannualapparentsurvivalprobabili-tiesandis
withϕ thesurvivalprobabilityEachentry inSurvival is theprob-abilityof surviving froma ldquostartingrdquodemographicstate (four rowscorrespondingto thedemographicstatesCSABNBonthe leftsideofthematrix)DdrepresentsthetransitiontotheldquodeadrdquostateThe equivalent matrix for males is presented in the SupportingInformation section 2f Please note thatϕ is a symbolic notationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
Torepresentallpossibletransitionsbetweendemographicso-cialandinfectionstatesofsurvivingindividualswethencombinedthese matrices in a way that is fully described in the SupportingInformation
235emsp|emspGoodness- of- fit
Prior to model selection we performed a goodness-of-fit test to(1)determinewhetherourdatamettheassumptionsofCMRmod-els and (2) validate ourmodel (Grosbois etal 2008) The results
on themodel fitarepresented in theSupporting Information seesection2f
236emsp|emspModel selection
Wefitted twosetsof candidatemodels separately for femalesand males It is often recommended to parameterize the ob-servationprocess (here detection and assignment) before thebiologicalone(egCulinaLachishPradelChoquetampSheldon2013)Startingwithaconstant-onlymodelwesequentiallypa-rameterizedthe(1)assignmentofinfectionstates(2)detection(3) survival (4) infection (5) social transitions and (6) breedingtransitionstestingforeffectsofsocialdemographicandinfec-tionstatesonthoseprocessesTotestourtwomainhypothesesanddisentangletheimportanceofexposureandallocationinaf-fectingtheoutcomeofCDVinfectionwetestedfortheeffectof social states on infection probability and on the survival ofindividuals indifferent infectionstatesconfrontingour resultswith the predictions derived from each hypothesis as summa-rizedinFigure1
For the observation processes we chose models with thelowestvalueofthequasi-Akaike informationcriterioncorrectedforsmallsamplesize(QAICcHannanampQuinn1979)QAICcwasusedratherthanthecommonAICtocorrectforpotentiallyauto-correlated andoverdisperseddata (HannanampQuinn1979) Forthe biological processes bestmodelswere thosewith the larg-estnumberofparameterswithina rangeof twoQAICcunitsofdifferencefromthemodelwiththelowestQAICcvalueinordertoavoiddismissingpotentiallyimportantbiologicalpredictorsofinterest We considered that fully identifiable models differingbylt2QAICcunitsfromthemodelwiththelowestQAICcmighthavesubstantialempiricalsupportforexplainingvariationintheresponsevariable(BurnhamampAnderson2003)andreportthesealso in Table 1
3emsp |emspRESULTS
Duringthestudyperiodhyenaswereidentifiedin90ofencoun-teroccasionsThesexdemographicstateandsocialstatewereas-signedto82ofindividualsTheremainingindividuals(notdetectedatcommunaldensorwithat leastoneunclearorunknowndemo-graphicorsocialstateduringtheirencounterhistory)wereexcludedOur finaldatasetswerecomposedof625 femalesand816malesFor43offemalesand44ofmalesinformationontheirinfectionstatewasavailableonatleastoneoccasionduringtheirencounterhistoryAmongstfemales189werecubs149subadults346non-breedersand316breedersamongstmales222werecubs182pre-breedersand596breedersHigh-rankingfemalesandmaleswereslightlymorecommonlyobservedthanlow-rankingones(1542high-rankingvs1306low-rankingstatesforfemales1463high-rankingvs1167 low-rankingstates formales)Fifty-four fe-maleswere infectedwith CDV between 1991 and 1997 (86 of
(3)Infection=
S
I
R
⎡⎢⎢⎢⎣
1minusβ β 0
0 0 1
0 0 1
⎤⎥⎥⎥⎦
(4)Survival=
C
SA
B
NB
Dd
⎡⎢⎢⎢⎢⎢⎢⎣
ϕ 0 0 0 1minusϕ
0 ϕ 0 0 1minusϕ
0 0 ϕ 0 1minusϕ
0 0 0 ϕ 1minusϕ
0 0 0 0 1
⎤⎥⎥⎥⎥⎥⎥⎦
emspensp emsp | emsp1243Functional EcologyMARESCOT ET Al
321emsp|emspEffect of social status on infection probability
Social status influenced the infectionprobability of cubs andof olderindividuals (pooled subadults breeders and non-breeders) in opposite
directions(Table1)Infectionprobabilitywaslowerforhigh-rankingthanlow-ranking cubs (Table2 Figure3a) and higher for high-ranking sub-adultsbreederandnon-breederfemalesthanlow-rankingones(Table2)
322emsp|emspEffect of social status on survival of susceptible and infected females
Social status affected the survival probability of susceptible andinfected cubs (Table1)with susceptible high-ranking female cubssurviving better than susceptible low-ranking ones and infectedhigh-rankingfemalecubssurvivingbetterthaninfectedlow-rankingones (Table2 Figure3b) Similarly susceptible high-ranking sub-adultshadahighersurvivalthansusceptiblelow-rankingonesandpooled infected and recovered high-ranking subadults a slightlyhighersurvivalthanpooledinfectedandrecoveredlow-rankingsub-adults (Table2Figure3b)Bothhigh-rankingand low-rankingsus-ceptible subadults had a substantially higher survival than pooledinfected and recoveredones (Table2 Figure3b)Breeder survival
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
emspensp emsp | emsp1241Functional EcologyMARESCOT ET Al
23emsp|emspMulti- event capturendashmarkndashrecapture model
Weusedamulti-eventCMR (MECMR)model (Pradel2005) fittedinE-SURGE190(ChoquetampNogue2011)toestimatesurvivalandstatetransitionprobabilities(theldquobiologicalprocessesrdquo)Thismodelpermits the estimation of such parameters whilst simultaneouslyaccountingforpotentialmethodologicalbiasesThese includegapsbetween monitoring periods left-censored data when individualswereobservedfirstasadultsatthebeginningofthestudyandright-censoreddatawhen individualswere still alive but not necessarilydetectedat theendof the study (the ldquoobservationprocessesrdquo seeSchaubGimenezSchmidtampPradel2004LebretonNicholsBarkerPradelampSpendelow2009Gimenezetal2012andFigure1foragraphicalrepresentationofthebiologicalandobservationprocesses)Thismodelalsoaccountsforthepotentially imperfectdetectionofmale hyenas that have temporarily or permanently dispersed fe-malesraisingtheiroffspringoutsidecommunaldensorfemalesstay-ingwiththemigratorypreyherdsforperiodsexceeding1year(MLEastpersonalobs)Individualsdetected(ldquocapturedrdquo)inagivenyearwereassignedan(S IorR) infectionstateifdatawereavailableoranunknowninfectionstateifdatawereunavailable(ConnampCooch2009)Moreclassicalmodelswouldnormallydiscardindividualswithunknowninfectionstatesbutthiswouldmostlikelyresultinbiases
Wefittedtwosetsofcandidatemodelsseparatelyforfemalesand males The biological processes were the product of foursquared matrices representing transitions between demographicstatessocialstatesinfectionstatesandsurvival
231emsp|emspTransitions between demographic states
ThematrixDemo(Equation1)considersthetransitionsoffemalesto three demographic states subadults (SA) breeders (B) or non-breeders(NB)
withΨthetransitionprobabilitytotheBstateaccessiblefromSAB andNB females andwith 1 minus Ψ its complement Each entry inDemoistheprobabilityoftransitionfromaldquostartingrdquodemographicstate(fourrowscorrespondingtothedemographicstatesCSABNBontheleftsideofthematrix)totheldquofollowingrdquodemographicstate(fourcolumnscorrespondingtothedemographicstatesCSABNBnotshownforsimplicity)Hereforexamplesurvivingcubs(C) (ldquostarting staterdquo) have a transition probability to the subadultstate(SA)(ldquofollowingstaterdquo)thatisequalto1Theequivalentma-trixformales ispresented intheSupporting Informationsection2fPleasenotethatΨisasymbolicnotationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
1242emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
thesocialstatesLandHnotshownforsimplicity)Pleasenotethatr is a symbolic notationhere This parameter could vary betweenstatesdependingonthemodelbeingtested
233emsp|emspTransitions between infection states
The matrix Infection (Equation3) considers the transitions of fe-malesormalestothreeinfectionstatessusceptible(S)infected(I)andrecovered(R)
withβ the infection probability (ie the probability of transitionfromasusceptibletoaninfectedstate)and1minus βitscomplementEach entry in Infection is the probability of transition from aldquostartingrdquo infection state category (three rows corresponding tothe infectionstatesS IR)toaldquofollowingrdquo infectionstate(threecolumnscorrespondingtheinfectionstatesSIRnotshownforsimplicity)PleasenotethatβisasymbolicnotationhereThispa-rametercouldvarybetweenstatesdependingonthemodelbeingtested
234emsp|emspSurvival
The matrix Survival (Equation4) accounts for the annual survivalprobabilitiesof females showsannualapparentsurvivalprobabili-tiesandis
withϕ thesurvivalprobabilityEachentry inSurvival is theprob-abilityof surviving froma ldquostartingrdquodemographicstate (four rowscorrespondingto thedemographicstatesCSABNBonthe leftsideofthematrix)DdrepresentsthetransitiontotheldquodeadrdquostateThe equivalent matrix for males is presented in the SupportingInformation section 2f Please note thatϕ is a symbolic notationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
Torepresentallpossibletransitionsbetweendemographicso-cialandinfectionstatesofsurvivingindividualswethencombinedthese matrices in a way that is fully described in the SupportingInformation
235emsp|emspGoodness- of- fit
Prior to model selection we performed a goodness-of-fit test to(1)determinewhetherourdatamettheassumptionsofCMRmod-els and (2) validate ourmodel (Grosbois etal 2008) The results
on themodel fitarepresented in theSupporting Information seesection2f
236emsp|emspModel selection
Wefitted twosetsof candidatemodels separately for femalesand males It is often recommended to parameterize the ob-servationprocess (here detection and assignment) before thebiologicalone(egCulinaLachishPradelChoquetampSheldon2013)Startingwithaconstant-onlymodelwesequentiallypa-rameterizedthe(1)assignmentofinfectionstates(2)detection(3) survival (4) infection (5) social transitions and (6) breedingtransitionstestingforeffectsofsocialdemographicandinfec-tionstatesonthoseprocessesTotestourtwomainhypothesesanddisentangletheimportanceofexposureandallocationinaf-fectingtheoutcomeofCDVinfectionwetestedfortheeffectof social states on infection probability and on the survival ofindividuals indifferent infectionstatesconfrontingour resultswith the predictions derived from each hypothesis as summa-rizedinFigure1
For the observation processes we chose models with thelowestvalueofthequasi-Akaike informationcriterioncorrectedforsmallsamplesize(QAICcHannanampQuinn1979)QAICcwasusedratherthanthecommonAICtocorrectforpotentiallyauto-correlated andoverdisperseddata (HannanampQuinn1979) Forthe biological processes bestmodelswere thosewith the larg-estnumberofparameterswithina rangeof twoQAICcunitsofdifferencefromthemodelwiththelowestQAICcvalueinordertoavoiddismissingpotentiallyimportantbiologicalpredictorsofinterest We considered that fully identifiable models differingbylt2QAICcunitsfromthemodelwiththelowestQAICcmighthavesubstantialempiricalsupportforexplainingvariationintheresponsevariable(BurnhamampAnderson2003)andreportthesealso in Table 1
3emsp |emspRESULTS
Duringthestudyperiodhyenaswereidentifiedin90ofencoun-teroccasionsThesexdemographicstateandsocialstatewereas-signedto82ofindividualsTheremainingindividuals(notdetectedatcommunaldensorwithat leastoneunclearorunknowndemo-graphicorsocialstateduringtheirencounterhistory)wereexcludedOur finaldatasetswerecomposedof625 femalesand816malesFor43offemalesand44ofmalesinformationontheirinfectionstatewasavailableonatleastoneoccasionduringtheirencounterhistoryAmongstfemales189werecubs149subadults346non-breedersand316breedersamongstmales222werecubs182pre-breedersand596breedersHigh-rankingfemalesandmaleswereslightlymorecommonlyobservedthanlow-rankingones(1542high-rankingvs1306low-rankingstatesforfemales1463high-rankingvs1167 low-rankingstates formales)Fifty-four fe-maleswere infectedwith CDV between 1991 and 1997 (86 of
(3)Infection=
S
I
R
⎡⎢⎢⎢⎣
1minusβ β 0
0 0 1
0 0 1
⎤⎥⎥⎥⎦
(4)Survival=
C
SA
B
NB
Dd
⎡⎢⎢⎢⎢⎢⎢⎣
ϕ 0 0 0 1minusϕ
0 ϕ 0 0 1minusϕ
0 0 ϕ 0 1minusϕ
0 0 0 ϕ 1minusϕ
0 0 0 0 1
⎤⎥⎥⎥⎥⎥⎥⎦
emspensp emsp | emsp1243Functional EcologyMARESCOT ET Al
321emsp|emspEffect of social status on infection probability
Social status influenced the infectionprobability of cubs andof olderindividuals (pooled subadults breeders and non-breeders) in opposite
directions(Table1)Infectionprobabilitywaslowerforhigh-rankingthanlow-ranking cubs (Table2 Figure3a) and higher for high-ranking sub-adultsbreederandnon-breederfemalesthanlow-rankingones(Table2)
322emsp|emspEffect of social status on survival of susceptible and infected females
Social status affected the survival probability of susceptible andinfected cubs (Table1)with susceptible high-ranking female cubssurviving better than susceptible low-ranking ones and infectedhigh-rankingfemalecubssurvivingbetterthaninfectedlow-rankingones (Table2 Figure3b) Similarly susceptible high-ranking sub-adultshadahighersurvivalthansusceptiblelow-rankingonesandpooled infected and recovered high-ranking subadults a slightlyhighersurvivalthanpooledinfectedandrecoveredlow-rankingsub-adults (Table2Figure3b)Bothhigh-rankingand low-rankingsus-ceptible subadults had a substantially higher survival than pooledinfected and recoveredones (Table2 Figure3b)Breeder survival
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
1242emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
thesocialstatesLandHnotshownforsimplicity)Pleasenotethatr is a symbolic notationhere This parameter could vary betweenstatesdependingonthemodelbeingtested
233emsp|emspTransitions between infection states
The matrix Infection (Equation3) considers the transitions of fe-malesormalestothreeinfectionstatessusceptible(S)infected(I)andrecovered(R)
withβ the infection probability (ie the probability of transitionfromasusceptibletoaninfectedstate)and1minus βitscomplementEach entry in Infection is the probability of transition from aldquostartingrdquo infection state category (three rows corresponding tothe infectionstatesS IR)toaldquofollowingrdquo infectionstate(threecolumnscorrespondingtheinfectionstatesSIRnotshownforsimplicity)PleasenotethatβisasymbolicnotationhereThispa-rametercouldvarybetweenstatesdependingonthemodelbeingtested
234emsp|emspSurvival
The matrix Survival (Equation4) accounts for the annual survivalprobabilitiesof females showsannualapparentsurvivalprobabili-tiesandis
withϕ thesurvivalprobabilityEachentry inSurvival is theprob-abilityof surviving froma ldquostartingrdquodemographicstate (four rowscorrespondingto thedemographicstatesCSABNBonthe leftsideofthematrix)DdrepresentsthetransitiontotheldquodeadrdquostateThe equivalent matrix for males is presented in the SupportingInformation section 2f Please note thatϕ is a symbolic notationhereThisparametercouldvarybetweenstatesdependingonthemodelbeingtested
Torepresentallpossibletransitionsbetweendemographicso-cialandinfectionstatesofsurvivingindividualswethencombinedthese matrices in a way that is fully described in the SupportingInformation
235emsp|emspGoodness- of- fit
Prior to model selection we performed a goodness-of-fit test to(1)determinewhetherourdatamettheassumptionsofCMRmod-els and (2) validate ourmodel (Grosbois etal 2008) The results
on themodel fitarepresented in theSupporting Information seesection2f
236emsp|emspModel selection
Wefitted twosetsof candidatemodels separately for femalesand males It is often recommended to parameterize the ob-servationprocess (here detection and assignment) before thebiologicalone(egCulinaLachishPradelChoquetampSheldon2013)Startingwithaconstant-onlymodelwesequentiallypa-rameterizedthe(1)assignmentofinfectionstates(2)detection(3) survival (4) infection (5) social transitions and (6) breedingtransitionstestingforeffectsofsocialdemographicandinfec-tionstatesonthoseprocessesTotestourtwomainhypothesesanddisentangletheimportanceofexposureandallocationinaf-fectingtheoutcomeofCDVinfectionwetestedfortheeffectof social states on infection probability and on the survival ofindividuals indifferent infectionstatesconfrontingour resultswith the predictions derived from each hypothesis as summa-rizedinFigure1
For the observation processes we chose models with thelowestvalueofthequasi-Akaike informationcriterioncorrectedforsmallsamplesize(QAICcHannanampQuinn1979)QAICcwasusedratherthanthecommonAICtocorrectforpotentiallyauto-correlated andoverdisperseddata (HannanampQuinn1979) Forthe biological processes bestmodelswere thosewith the larg-estnumberofparameterswithina rangeof twoQAICcunitsofdifferencefromthemodelwiththelowestQAICcvalueinordertoavoiddismissingpotentiallyimportantbiologicalpredictorsofinterest We considered that fully identifiable models differingbylt2QAICcunitsfromthemodelwiththelowestQAICcmighthavesubstantialempiricalsupportforexplainingvariationintheresponsevariable(BurnhamampAnderson2003)andreportthesealso in Table 1
3emsp |emspRESULTS
Duringthestudyperiodhyenaswereidentifiedin90ofencoun-teroccasionsThesexdemographicstateandsocialstatewereas-signedto82ofindividualsTheremainingindividuals(notdetectedatcommunaldensorwithat leastoneunclearorunknowndemo-graphicorsocialstateduringtheirencounterhistory)wereexcludedOur finaldatasetswerecomposedof625 femalesand816malesFor43offemalesand44ofmalesinformationontheirinfectionstatewasavailableonatleastoneoccasionduringtheirencounterhistoryAmongstfemales189werecubs149subadults346non-breedersand316breedersamongstmales222werecubs182pre-breedersand596breedersHigh-rankingfemalesandmaleswereslightlymorecommonlyobservedthanlow-rankingones(1542high-rankingvs1306low-rankingstatesforfemales1463high-rankingvs1167 low-rankingstates formales)Fifty-four fe-maleswere infectedwith CDV between 1991 and 1997 (86 of
(3)Infection=
S
I
R
⎡⎢⎢⎢⎣
1minusβ β 0
0 0 1
0 0 1
⎤⎥⎥⎥⎦
(4)Survival=
C
SA
B
NB
Dd
⎡⎢⎢⎢⎢⎢⎢⎣
ϕ 0 0 0 1minusϕ
0 ϕ 0 0 1minusϕ
0 0 ϕ 0 1minusϕ
0 0 0 ϕ 1minusϕ
0 0 0 0 1
⎤⎥⎥⎥⎥⎥⎥⎦
emspensp emsp | emsp1243Functional EcologyMARESCOT ET Al
321emsp|emspEffect of social status on infection probability
Social status influenced the infectionprobability of cubs andof olderindividuals (pooled subadults breeders and non-breeders) in opposite
directions(Table1)Infectionprobabilitywaslowerforhigh-rankingthanlow-ranking cubs (Table2 Figure3a) and higher for high-ranking sub-adultsbreederandnon-breederfemalesthanlow-rankingones(Table2)
322emsp|emspEffect of social status on survival of susceptible and infected females
Social status affected the survival probability of susceptible andinfected cubs (Table1)with susceptible high-ranking female cubssurviving better than susceptible low-ranking ones and infectedhigh-rankingfemalecubssurvivingbetterthaninfectedlow-rankingones (Table2 Figure3b) Similarly susceptible high-ranking sub-adultshadahighersurvivalthansusceptiblelow-rankingonesandpooled infected and recovered high-ranking subadults a slightlyhighersurvivalthanpooledinfectedandrecoveredlow-rankingsub-adults (Table2Figure3b)Bothhigh-rankingand low-rankingsus-ceptible subadults had a substantially higher survival than pooledinfected and recoveredones (Table2 Figure3b)Breeder survival
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
emspensp emsp | emsp1243Functional EcologyMARESCOT ET Al
321emsp|emspEffect of social status on infection probability
Social status influenced the infectionprobability of cubs andof olderindividuals (pooled subadults breeders and non-breeders) in opposite
directions(Table1)Infectionprobabilitywaslowerforhigh-rankingthanlow-ranking cubs (Table2 Figure3a) and higher for high-ranking sub-adultsbreederandnon-breederfemalesthanlow-rankingones(Table2)
322emsp|emspEffect of social status on survival of susceptible and infected females
Social status affected the survival probability of susceptible andinfected cubs (Table1)with susceptible high-ranking female cubssurviving better than susceptible low-ranking ones and infectedhigh-rankingfemalecubssurvivingbetterthaninfectedlow-rankingones (Table2 Figure3b) Similarly susceptible high-ranking sub-adultshadahighersurvivalthansusceptiblelow-rankingonesandpooled infected and recovered high-ranking subadults a slightlyhighersurvivalthanpooledinfectedandrecoveredlow-rankingsub-adults (Table2Figure3b)Bothhigh-rankingand low-rankingsus-ceptible subadults had a substantially higher survival than pooledinfected and recoveredones (Table2 Figure3b)Breeder survival
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
1244emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
331emsp|emspEffect of social status on infection probability
Social status influenced the infection probability amongst cubs(Table1)High-rankingcubshada lower infectionprobability thanlow-rankingonesasforfemales(Table2Figure3c)
332emsp|emspEffect of social status on survival of susceptible and infected
As for females susceptible high-ranking male cubs survived bet-terthansusceptiblelow-rankingones(Tables1and2)andinfectedhigh-rankingmale cubs survived better than infected low-rankingones (Table2 Figure3d) Susceptible pre-breeders survived bet-terthanpooledinfectedandrecoveredonesandwithinthispooledgrouphigh-rankingpre-breederssurvivedbetterthanlow-rankingones(Table2Figure3d)High-rankingbreedershadalowersurvivalthanlow-rankingones(Table2)
4emsp |emspDISCUSSION
The impact of the 19931994 CDV epidemic on hyenas in theSerengetiNPwas substantial particularly among young animalsMaternalsocialstatushadasubstantial impactontheprobabilityofcubinfectionanditsoutcomeHigh-borncubswerelesslikelyto
beinfectedandincurredasmallerreductionintheirsurvivalonceinfected(femalecubs16malecubs20)thanlow-borncubs(fe-malecubs31malecubs36Table2Figure3bd)Thesefindingsareconsistentwiththeideathathigh-borncubsallocatesubstan-tiallymoreresourcestoimmuneprocessesthanlow-bornonesbe-causetheirmilkintakeissignificantlyhigher(HoferampEast1993b2003Hoferetal2016)Thissuggeststhattherank-relatedabil-ity to allocate resources to immuneprocesses ismore importantindeterminingtheoutcomeofinfectionindependenthyenacubsthandifferencesinCDVexposureOurresultsareconsistentwithother studies on hyenas that provide evidence that social statusaffects the allocationof resources to immuneprocesses and theoutcomeofinfectionDuringlactationlow-rankingfemalehyenashavesignificantlyhigherhelmintheggburdensandaremorelikelytohaveconcurrentprotozoanparasiteinfectionsthanhigh-rankingfemales(Eastetal2015)Similarlynutritionallydisadvantagedhy-enassufferedhighermortalityduringanoutbreakofapathogenicbacterium(Houmlneretal2012)HigherserumconcentrationsoftheimmunoglobulinIgMinhigh-rankingfemalesmayreflectagreaterallocation of resources to immune processes (Flies etal 2016)Rank-relateddifferencesintheexpressionofimmunegeneshavebeenreportedinanon-humanprimate(Tungetal2012)
High-rankinghyenacubsmayalsohaveagreaterabilitythanlow-rankingcubs to invest in the repairofcellsandtissuesdamagedbyCDVandimmuneprocessestocombatsecondaryinfectionsthattyp-ically accompanyCDV infection (Beineke etal 2009)whichwouldhaveaided their recoveryEvensowecannotexclude thepossibil-itythathigh-andlow-rankingcubsdifferintheirimmuneresponsesbecauseofdifferences intheiralleliccompositionof immunegenesThecostofmate-choice ishigher for low-rankingthanhigh-rankingfemales(Eastetal2003)andhenceageneticcomponentmayinpartexplainthemoresevereoutcomeofCDVinfectionlow-rankingcubs
Incontrasttofemalecubshigh-rankingfemalesubadultsweremore likely tobe infectedwithCDVthan low-rankingones (con-sistentwiththeexposurehypothesis)butonceinfectedtheirsur-vivalwasbetterthanthatoflow-rankingones(Figure3bTable2)(consistentwiththeallocationhypothesis)Interestinglythereduc-tioninsurvivalwassimilarbetweensocialstates(high-born30low-born28Table2)AsweaningusuallytakesplaceduringthesecondyearoflifethedemographicclassofsubadultscomprisedbothunweanedandweanedlifestagesVariationinthecontribu-tionofmilkandsolidfoodtothedietofsubadultsmayexplainwhydifferencesinthesurvivalofhigh-rankingandlow-rankinginfectedandrecoveredfemalesubadultswerelessclear-cutthanforcubswhosesurvivalcompletelydependsonmaternalmilk(HoferampEast1993b) Among pre-breedermales therewas no effect of socialstatusandnodifferenceinthesurvivalofinfectedhigh-rankingandlow-rankingindividualsThereductioninsurvivalforpre-breedermaleswassubstantialandofasimilarmagnitudetothatinsubadultfemales(high-born27low-born33Table2Figure3d)
We found clear evidence of a delayed detrimental effect onthe survival of subadult females and pre-breeding males that re-covered from infection suggesting a longer term fitness cost of
F IGURE 2emspConditionalprobabilitydistributionofthethreeinfectionstatesldquosusceptiblerdquoldquoinfectedrdquoandldquorecoveredrdquoduringthestudyperiod1990ndash2010TheseprobabilitydensitiesareobtainedwiththecdplotfunctioninRwhichcomputesasmoothingkerneldensityfunctionSolidlinesfemalesdashedlinesmalesTheprobabilitydensitiesofldquoinfectedrdquoarerepresentedbytheareabelowtheorangelinesthoseofldquosusceptiblerdquocovertheareabetweentheorangeandthebluelinesandthoseofldquorecoveredrdquocovertheareabetweenthebluelinesand1thegreendottedhorizontallineThevirulentcaninedistempervirus(CDV)epidemic(1993ndash1994)isindicatedinorangeonthex-axisAninterpolationfactorwasusedtosmooththelinesbetweendatapoints
1990 93 2000 201093 94
00
02
04
06
08
10
Con
ditio
nal d
ensi
ty
Study period
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
emspensp emsp | emsp1245Functional EcologyMARESCOT ET Al
CDV infection in termsof reduced survival (Figure3c d Table2)CDVsubstantiallydepletes lymphoidorgansand lymphocytes re-duces responsesof immunomodulatorycytokinesandupregulatesinflammatory cytokines Direct virus-mediated damage and pro-inflammatory cytokine-induced damage to the central nervoussystemcanalsooccur(Beinekeetal2009)TheCDVstrainthatin-fectedhyenasinthe19931994epidemicencodedonenovelaminoacidintheV-protein(Nikolinetal2017)TheV-proteinisknowntodisrupthostinterferonsignalling(vonMesslingSvitekampCattaneo2006Roumlthlisbergeretal 2010) hence rendering theoutcomeof
infectionparticularlysevereAsrepairingCDV-damagedtissuesandmountingimmuneresponsestoinfectionarecostlyintermsofbodyresourceshoststhatdonotmeetthesecostsarepronetosecond-aryinfectionsthatthenfuelthisldquoviciouscirclerdquo(Beinekeetal2009Beldomenico amp Begon 2010) The hitherto unsuspected delayedanddetrimentaleffectofCDVinfectioninfemalesubadultandmalepre-breederhyenasmostlikelyresultedfromtheseverepathologiescausedbyanon-canidadaptedCDVstrain
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
1246emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
casefor infectionofhyenaswithAlphacoronavirus (GollerFickelHofer Beier amp East 2013) Hepatozoon (East etal 2008) andDipylidium helminths (East Kurze Wilhelm Benhaiem amp Hofer2013) in our study populationAlthough adults exposed toCDVbefore the19931994epidemicpresumablyhadprotective anti-body titres the lack of clinical canine distemper in adult hyenasduringthisepidemicwasprobablyduetoothercomponentsoftheimmunesystemHyenaslikethedomesticcatFelis catus(Beinekeetal2015)canhaveCDVreplicating in leucocyteswithoutde-veloping clinical disease (Nikolin etal 2017) Since in long-livedspeciesadult survival isacritical fitnesscomponentnatural se-lectionmayalsofavourthedevelopmentofstrongeradultimmunedefencestominimizetheimpactofinfections(BootsBestMillerampWhite2009)
The outcome of CDV infection in terms of reduced survivalwasmoresevereamongmalesthanamongfemaleswhichisalsosupportedbyourresultsoninfectionprobabilities(Table2)Thesesuggestthatimmuneresponsesmaybemoreefficaciousinfemalethaninmalehyenasasfoundinmanymammalsbirdsandreptiles(reviewedinKleinampFlanagan2016)Rank-relateddifferences insocial contactamong femalesprobablyexplainwhyhigh-rankingfemalesaremorelikelytobecomeinfectedthanlow-rankingones(Table2)This result isconsistentwiththefindingsofapreviousstudyinthesamehyenapopulationwherethehighercontactratesofhigh-rankingadult femalessignificantly increased theirproba-bilityofexposuretorabies(Eastetal2001) Interestinglymorefrequent (asymptomatic) exposure to CDV among high-rankingadult femaleswould induce protectiveCDV titres andmayhave
benefitted their cubs through the transfer of these antibodiesduring lactation an idea consistent with our finding that high-ranking cubs had a lower infection probability than low-rankingones The effect of social status amongmales was not identifi-able Interestinglymales had a higher infection probability thanfemalesdespitethelowerprobabilityofassigninganinfectedstatetomales (see Supporting Information section 3b) Because ourMECMRmodelallowedustoaccountforsuchuncertaintywecon-siderthisarobustresult
Our results suggest that CDV transmission mostly occurredbetween virus shedding cubs at communal dens and susceptibleclanmembersvisitingthesesocialcentresHencecommunaldenswouldhavepromotedahighlevelofexposureamongclanmembersduringtheepidemicSimilarlythetransmissionofairbornevirusesinclustersofsusceptible individualswith intensesocialcontactssuchasinschoolsandkindergartensisknowntodriveepidemicsofmeasles(Garenneetal1991Paunioetal1998)andtheH1N1strain of avian influenza (Cauchemez etal 2011) The impact oftheseviruseson the fitnessofsusceptible (non-vaccinated) juve-nileswasnotquantifiedOurstudydoesquantifythelethalimpactof an infectious juvenile viral disease in a fissionndashfusion societysimilartothatinhumansandwithtransmissionhotspots(commu-naldens)similartoschoolsandkindergartensHenceourresultsmayprovideusefulinsightsintoinfectiousjuvenilediseasesinhu-mans aswell as those in othermammalian specieswith a similarsocialstructure
Therehasbeenconsiderableandvaluableresearchontherela-tionshipsbetweensocialityanddiseasebasedonnetworkanalysesThis research demonstrates that social contact rates (eg groom-ing)could influencediseasetransmissionorburdenandvice-versa(egBansalReadPourbohloulampMeyers2010Chenetal2014Duboscqetal 2016) Social networks are increasingly integratingdiseasedynamicsintheiranalyses(egSpringerKappelerampNunn2017Vazquez-Prokopecetal2013VolzampMeyers2007)buttoour knowledge no network-based study has ever considered dy-namicprocessesinboththepathogenandthehostThemainchal-lengeofsocialnetworkanalysesmostlikelyliesinthedifficultyofdescribing feedback dynamics between host social networks anddisease-related fitness costs in the host (Van Segbroeck Santosamp Pacheco 2010 VolzampMeyers 2007) As an alternative to so-cial network analysis other studies including ours use surrogatevariablesforcontactratesWeusedclassesofsocialstatusothersusedthenumberofanimalsencounteredsimultaneouslyinthesamearea(Crossetal2004)breedingstatus(Gentonetal2015)orin-directmeasuresofsocio-economicstatusinmanyhumansocieties(Sapolsky2005)
Manystudiesincludingdetailedclinicalsurveysontheinfectionhistoriesofpatientsasdeterminedbyrepeatedvirusscreeningandserologicalanalysesfocusonallocationofresourcestoimmunepro-cesses andheterogeneityon theoutcomeof infection yet neglecttoconsiderthepotentialcontributionofvariationinhostexposureTherefore such studies do not disentangle the effect of variationinexposureintermsofcontactrateswithinfectedindividualsfrom
F IGURE 3emspMaximumlikelihoodestimate(MLE)(plusmnSE)probabilitiesofannualinfectionwithcaninedistempervirus(CDV)((a)and(c)dashedlines)andsurvival((b)and(d)solidlines)ofSerengetispottedhyenasasafunctionofdemographicsocialandinfectionstatesasdetectedbythebest-rankedmodel(a)and(b)Highandlow-rankingfemalecubsandsubadults(c)and(d)Highandlow-rankingmalecubsandpre-breedersInfectionstatesweresusceptible(paleblue)infected(orange)andrecovered(green)
02
04
06
08
10
High Low High LowCub Subadult
High Low High Low
High Low High Low High Low High Low
Cub Subadult
Infe
ctio
n pr
obab
ility
(a)
02
04
06
08
10
Sur
viva
l pro
babi
lity
(b)
04
06
08
10(c)
Cub Pre-breeder
Infe
ctio
n pr
obab
ility
04
06
08
10(d)
Cub Pre-breeder
Sur
viva
l pro
babi
lity
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
emspensp emsp | emsp1247Functional EcologyMARESCOT ET Al
immunocompetence(Kappeleretal2015)Neverthelesssomeem-pirical studieshaveused statistical inference todisentangle theef-fects of exposure from thoseof immune responses to exposure inthepropagationofinfectiousdisease(CivitelloampRohr2014)orde-scribepotentialmethodologicalapproachestoachievethis(RhodesHalloranampLongini1996)Thesemethodologicalapproachesmaybeapplicabletoexperimentalstudiesbutnottonon-invasivestudiesonfree-rangingspeciesthatincludeuncertaintyintheinfectionstatusofthehostModelsthataccountforunavoidableuncertaintyinthein-fectionstateofindividualseitherlumpthesetwoprocesses(ieexpo-sureandallocation)orconsideronlyoneofthesetwoprocesses(egChambertetal2012ChoquetCarrieacuteChambertampBoulinier2013)
In our study the detection probability of individuals was onaverageveryhighanddidnotvarywithinfectionstatesThusweare not dealingwith any heterogeneity in state-specific detectionprobabilities(suchasalowerdetectionofinfectedanimalsascom-paredtosusceptibleoneswhichcanbiasestimationscfJennelleCoochConroyamp Senar 2007)However one potential limitationofourstudyandpossiblyofotherstudiesbasedonnon-invasiveoropportunistic sample collections is the risk ofmisclassification ofinfectionstatesduetodiagnosticinaccuracyandimperfectstateob-servationBuzduganVergneGrosboisDelahayandDrewe(2017)proposed the first approach to estimate probabilities associatedwithanindividualrsquosinfectionstateatanygivenpointdependingonprior and current knowledge about that individualrsquos health statusAlthoughthisapproach ispromising it isnotapplicabletostudiessuchasours thatdonot routinely runmultiplediagnostic tests inseriesorparallelWechosetomodeluncertaintyontheassignmentof infectionstatesotherschosetomodeltheriskofnotcorrectlyassigningthosestates(Buzduganetal2017)Toourknowledgenostudyhasevermodelledbothtypesofuncertaintysimultaneouslyprobablybecausethiswouldrequireextensivedataonhealthstatus
Ourmodelling approach permits the separation of the influenceof variation in virus exposure and resource allocation to immuneprocessesonCDVinfectionprobabilityWithourapproach it isalsopossibletotestforaneffectofsocialstatusonboththelikelihoodofpathogenexposureandcontractingthediseaseFurthermorewewereabletotestforaninteractioneffectbetweensocialandinfectionstatesonsurvivalWethereforecouldquantifytheoutcomeofCDVinfec-tionindifferentdemographicandsocialclassesanddemonstratethatdemographicandsocialstatesmediatedthepositiverelationshipbe-tweenCDVinfectionandmortalityFinallytheparametersestimatedbythisapproachcaneasilybecombinedwithmatrixmodelstoprovideahighlypowerfultooltoexaminethelong-termconsequencesofepi-demicsatthepopulationlevel(Olietal2006)
ACKNOWLEDG EMENTS
We are grateful to the Commission for Science and Technologyof Tanzania (COSTECH) the Tanzania Wildlife Research Institute(TAWIRI)andTanzaniaNationalParks(TANAPA)fortheirsupportofourresearchWethanktheDeutscheForschungsgemeinschaft(grantsEA53-1KR42662-1DFG-Grako1121)theLeibniz-InstituteforZoo
andWildlifeResearch theFritz-Thyssen-Stiftung theStifterverbandderdeutschenWissenschaftand theMax-Planck-Gesellschaft for fi-nancialassistanceWethankReacutemiChoquetSarahCubaynesMatthiasFranzandSylvainGandonfordiscussionsandAnnieFrancisThomasShabaniMalvinaAndrisNellyBoyerRobertFyumagwaTraudiGollaKatjaGollerNicoleGusset-BurgenerRichardHoareKarinHoumlnigMarkJago Stephan Karl Berit Kostka Michelle Lindson Sonja MetzgerMelodyRoelke-ParkerDagmarThiererAgnesTuumlrkHaraldWiikandKerstinWilhelmforassistanceWethankJDuboscqandthreeanony-mousreviewersfortheirhelpfulsuggestions
AUTHORSrsquo CONTRIBUTIONS
SKSMLE and JDL designed the initial researchMLE HHXAOCandSBperformedthefieldandorlaboratoryworkLMandSBconstructedthemodelsunderthesupervisionofOGSKSJDL and HH and SB LMMLE HH and SKS wrote thepaperAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
The data are archived in figshare httpsdoiorg106084m9figshare5840970(Benhaiemetal2018)
BansalSReadJPourbohloulBampMeyersLA(2010)Thedynamicnature of contact networks in infectious disease epidemiologyJournal of Biological Dynamics4 478ndash489 httpsdoiorg101080175137582010503376
Beineke A Baumgaumlrtner W amp Wohlsein P (2015) Cross-speciestransmission of canine distemper virusmdashan updateOne Health 149ndash59httpsdoiorg101016jonehlt201509002
Beineke A Puff C Seehusen F amp Baumgaumlrtner W (2009)PathogenesisandimmunopathologyofsystemicandnervouscaninedistemperVeterinary Immunology and Immunopathology127 1ndash18httpsdoiorg101016jvetimm200809023
BeldomenicoPMampBegonM (2010)DiseasespreadsusceptibilityandinfectionintensityViciouscirclesTrends in Ecology amp Evolution2521ndash27httpsdoiorg101016jtree200906015
BenhaiemSMarescotLGimenezOHoferHLebretonJ-DOlarte-CastilloXAhellipEastML(2018)Capture-Mark-Recapture(CMR)datasets of Serengeti spotted hyenas infected with CDV figshare httpsdoiorg106084m9figshare5840970
BootsMBestAMillerMRampWhiteA(2009)TheroleofecologicalfeedbacksintheevolutionofhostdefenceWhatdoestheorytellusPhilosophical Transactions of the Royal Society of London B Biological Sciences36427ndash36httpsdoiorg101098rstb20080160
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
1248emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
BurnhamKPampAndersonDR(2003)Model selection and multimodel inference A practical information-theoretic approachBerlinGermanyNewYorkNYSpringerScienceampBusinessMedia
BuzduganSNVergneTGrosboisVDelahayRJampDreweJA(2017) Inferenceof the infection statusof individualsusing longi-tudinal testing data from cryptic populations Towards a probabi-listic approach to diagnosis Scientific Reports7 1111 httpsdoiorg101038s41598-017-00806-4
CauchemezSBhattaraiAMarchbanksTLFaganRPOstroffSFergusonNMhellipAnguloF J (2011)Roleof socialnetworks inshapingdiseasetransmissionduringacommunityoutbreakof2009H1N1 pandemic influenza Proceedings of the National Academy of Sciences of the United States of America1082825ndash2830httpsdoiorg101073pnas1008895108
CavigelliSAampChaudhryHS(2012)Socialstatusglucocorticoidsimmune function and health Can animal studies help us under-stand human socioeconomic-status-related health disparitiesHormones and Behavior 62 295ndash313 httpsdoiorg101016jyhbeh201207006
Chambert T Staszewski V Lobato E Choquet R CarrieC McCoy K D hellip Boulinier T (2012) Exposure of black-legged kittiwakes to Lyme disease spirochetes Dynamics ofthe immune status of adult hosts and effects on their sur-vival Journal of Animal Ecology 81 986ndash995 httpsdoiorg101111j1365-2656201201979x
ChoquetRCarrieacuteCChambertTampBoulinierT (2013)Estimatingtransitions between states using measurements with imperfectdetectionApplication to serologicaldataEcology94 2160ndash2165httpsdoiorg10189012-18491
CivitelloD JampRohr JR (2014)Disentangling theeffectsofexpo-sure and susceptibility on transmission of the zoonotic parasiteSchistosoma mansoni Journal of Animal Ecology 83 1379ndash1386httpsdoiorg1011111365-265612222
Clutton-BrockTHampHuchardE (2013)Social competitionandse-lection inmalesandfemalesPhilosophical Transactions of the Royal Society of London B Biological Sciences36820130074httpsdoiorg101098rstb20130074
ConnPBampCoochEG (2009)Multistatecapturendashrecaptureanal-ysis under imperfect state observation An application to dis-ease models Journal of Applied Ecology 46 486ndash492 httpsdoiorg101111j1365-2664200801597x
CulinaALachishSPradelRChoquetRampSheldonBC(2013)Amultieventapproachtoestimatingpairfidelityandheterogeneityinstate transitionsEcology and Evolution3 4326ndash4338 httpsdoiorg101002ece3729
DeemSLSpelmanLHYatesRAampMontaliRJ(2000)Caninedistemper in terrestrial carnivores A review Journal of Zoo and Wildlife Medicine31441ndash451
DesprezMMcMahonCRHindellMAHarcourtRampGimenezO (2013) Known unknowns in an imperfect world Incorporatinguncertainty inrecruitmentestimatesusingmulti-eventcapturendashre-capture models Ecology and Evolution 3 4658ndash4668 httpsdoiorg101002ece3846
East M L Burke T Wilhelm K Greig C amp Hofer H (2003)Sexual conflicts in spotted hyenasMale and femalemating tac-tics and their reproductive outcome with respect to age socialstatusandtenureProceedings of the Royal Sociely of London Series B Biological Sciences 270 1247ndash1254 httpsdoiorg101098rspb20032363
EastMLHoferHCoxJHWulleUWiikHampPitraC(2001)Regular exposure to rabies virus and lack of symptomatic diseaseinSerengetispottedhyenasProceedings of the National Academy of Sciences of the United States of America98 15026ndash15031httpsdoiorg101073pnas261411898
EastM L Hofer H ampWicklerW (1993) The erect lsquopenisrsquo is aflag of submission in a female-dominated society Greetings inSerengeti spotted hyenas Behavioral Ecology and Sociobiology33355ndash370
East M L Kurze CWilhelm K Benhaiem S amp Hofer H (2013)Factors influencingDipylidium sp infection ina free-ranging socialcarnivorethespottedhyaena(Crocuta crocuta)International Journal for Parasitology Parasites and Wildlife2257ndash265
EastMLOttoEHelmsJThiererDCableJampHoferH(2015)Doeslactationleadtoresourceallocationtrade-offsinthespottedhyaena Behavioral Ecology and Sociobiology 69 805ndash814 httpsdoiorg101007s00265-015-1897-x
EastMLWibbeltGLieckfeldtDLudwigAGollerKWilhelmK hellip Hofer H (2008) A Hepatozoon species genetically distinctfrom H canis infecting spotted hyenas in the Serengeti ecosys-tem Tanzania Journal of Wildlife Diseases 44 45ndash52 httpsdoiorg1075890090-3558-44145
Flies A SMansfield L S Flies E J Grant C K ampHolekamp KE (2016) Socioecological predictors of immune defenses in wildspotted hyenas Functional Ecology 30 1549ndash1557 httpsdoiorg1011111365-243512638
FrankLGGlickmanSEampLichtP (1991)Fatalsiblingaggres-sion precocial development and androgens in neonatal spot-ted hyenas Science 252 702ndash704 httpsdoiorg101126science2024122
Genton C Pierre A Cristescu R Leacutevreacutero F Gatti S Pierre J ShellipLeGouarP (2015)HowEbola impactssocialdynamics ingoril-lasAmultistatemodellingapproachJournal of Animal Ecology84166ndash176httpsdoiorg1011111365-265612268
GervasiSSCivitelloDJKilvitisHJampMartinLB(2015)Thecon-textofhostcompetenceAroleforplasticityinhostndashparasitedynam-ics Trends in Parasitology 31 419ndash425 httpsdoiorg101016jpt201505002
GimenezO Lebreton J-DGaillard J-M Choquet R amp Pradel R(2012) Estimating demographic parameters using hidden processdynamic models Theoretical Population Biology82307ndash316httpsdoiorg101016jtpb201202001
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
emspensp emsp | emsp1249Functional EcologyMARESCOT ET Al
GollerVKFickelJHoferHBeierSampEastML(2013)CoronavirusgenotypeandinfectionprevalenceinwildcarnivoresintheSerengetiNationalParkTanzaniaAchives of Virology158729ndash734
GoymannWEastMLWachterBHoumlnerOPMostlEVanrsquotHofT JampHoferH (2001)Social state-dependentandenvironmen-talmodulationoffaecalcorticosteroidlevelsinfree-rangingfemalespotted hyenas Proceedings of the Royal Sociely of London Series B Biological Sciences 268 2453ndash2459 httpsdoiorg101098rspb20011828
GrosboisVGimenezOGaillardJMPradelRBarbraudCClobertJhellipWeimerskirchH(2008)Assessingtheimpactofclimatevari-ation on survival in vertebrate populationsBiological Reviews 83357ndash399httpsdoiorg101111j1469-185X200800047x
Haas L Hofer H East M Wohlsein P Liess B amp Barrett T(1996) Canine distemper virus infection in Serengeti spot-ted hyaenas Veterinary Microbiology 49 147ndash152 httpsdoiorg1010160378-1135(95)00180-8
HannanEJampQuinnBG(1979)ThedeterminationoftheorderofanautoregressionJournal of the Royal Statistical Society Series B41190ndash195
Harrison TMMazet JKHolekampK EDubovi E EnghA LNelson K hellip Munson L (2004) Antibodies to canine and fe-line viruses in spotted hyenas (Crocuta crocuta) in theMasaiMaraNationalReserveJournal of Wildlife Diseases401ndash10httpsdoiorg1075890090-3558-4011
Hofer H amp EastM L (1993b) The commuting system of Serengetispotted hyaenas ndash How a predator copes with migratory prey IIAttendance and maternal care Animal Behaviour 46 575ndash589httpsdoiorg101006anbe19931224
HoferHampEastML(1995)Populationdynamicspopulationsizeand the commuting system of Serengeti spotted hyenas In ASinclairampPArcese(Eds)Serengeti II dynamics management and conservation of an ecosystem(pp332ndash363)ChicagoILUniversityofChigagoPress
Hofer H amp East M L (2003) Behavioral processes and costsof co-existence in female spotted hyenas A life history per-spective Evolutionary Ecology 17 315ndash331 httpsdoiorg101023A1027352517231
HolekampKESmaleLampSzykmanM(1996)Rankandreproductionin the female spotted hyaena Journal of Reproduction and Fertility108229ndash237httpsdoiorg101530jrf01080229
HoumlnerOPWachterBGollerKVHoferHRunyoroVThiererDhellipEastML(2012)TheimpactofapathogenicbacteriumonasocialcarnivorepopulationJournal of Animal Ecology8136ndash46httpsdoiorg101111j1365-2656201101873x
Jennelle C S Cooch E G Conroy M J amp Senar J C (2007)State-specific detection probabilities and disease prev-alence Ecological Applications 17 154ndash167 httpsdoiorg1018901051-0761(2007)017[0154SDPADP]20CO2
KappelerPMCremerSampNunnCL (2015)SocialityandhealthImpacts of sociality on disease susceptibility and transmission inanimal and human societiesPhilosophical Transactions of the Royal Society of London B Biological Sciences37020140116httpsdoiorg101098rstb20140116
Lebreton J D Nichols J D Barker R J Pradel R amp SpendelowJ A (2009) Chapter 3 modeling individual animal histories withmultistate capturendashrecapture models Advances in Ecological Research pp 87ndash173 Academic Press httpsdoiorg101016S0065-2504(09)00403-6
MacIntosh A J J Jacobs A Garcia C Shimizu K Mouri KHuffmanMAampHernandezAD (2012)Monkeysinthemid-dle Parasite transmission through the social network of a wildprimate PLoS ONE 7 e51144 httpsdoiorg101371journalpone0051144
NikolinVNOlarte-CastilloXAOsterriederNHoferHDuboviEMazzoniCJhellipEastML(2017)CaninedistempervirusintheSerengeti ecosystem Molecular adaptation to different carnivorespeciesMolecular Ecology262111ndash2130httpsdoiorg101111mec13902
NunnC L Jordaacuten FMcCabeCM Verdolin J L amp Fewell JH(2015) Infectious disease and group size More than just a num-bersgamePhilosophical Transactions of the Royal Society of London B Biological Sciences 370 20140111 httpsdoiorg101098rstb20140111
PaunioMPeltolaHValleMDavidkinIVirtanenMampHeinonenO P (1998) Explosive school-based measles outbreak Intenseexposuremayhave resulted in high risk even among revaccineesAmerican Journal of Epidemiology 148 1103ndash1110 httpsdoiorg101093oxfordjournalsajea009588
RhodesPHHalloranMEampLonginiJrIM(1996)CountingprocessmodelsforinfectiousdiseasedataDistinguishingexposuretoinfec-tionfromsusceptibilityJournal of the Royal Statistical Society Series B58751ndash762
Roelke-ParkerM EMunson L Packer C Kock R Cleaveland SCarpenterMhellipAppelMJ (1996)Acaninedistempervirusepi-demicinSerengetilions(Panthera leo)Nature379441ndash445httpsdoiorg101038379441a0
RoumlthlisbergerAWienerDSchweizerMPeterhansEZurbriggenAampPlattetP(2010)TwodomainsoftheVproteinofvirulentca-nine distemper virus selectively inhibit STAT1 and STAT2 nuclearimportJournal of Virology846328ndash6343httpsdoiorg101128JVI01878-09
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
1250emsp |emsp emspenspFunctional Ecology MARESCOT ET Al
SawatskyBWongXXHinkelmannSCattaneoRampvonMesslingV (2012) Canine distemper virus epithelial cell infection is re-quiredforclinicaldiseasebutnotforimmunosuppressionJournal of Virology863658ndash3666httpsdoiorg101128JVI06414-11
SchaubMGimenezOSchmidtBRampPradelR(2004)Estimatingsurvival and temporary emigration in the multistate capture-recapture framework Ecology 85 2107ndash2113 httpsdoiorg10189003-3110
Schmid-HempelP (2003)Variation in immunedefenceas aquestionof evolutionary ecologyProceedings of the Royal Sociely of London Series B Biological Sciences270357ndash366httpsdoiorg101098rspb20022265
SeyfarthRM(1977)Amodelofsocialgroomingamongadultfemalemonkeys Journal of Theoretical Biology 65 671ndash698 httpsdoiorg1010160022-5193(77)90015-7
SmithJEMemenisSKampHolekampKE(2007)Rank-relatedpart-nerchoiceinthefissionndashfusionsocietyofthespottedhyena(Crocuta crocuta) Behavioral Ecology and Sociobiology 61 753ndash765 httpsdoiorg101007s00265-006-0305-y
SpringerA Kappeler PMampNunnC L (2017)Dynamic vs staticsocial networks in models of parasite transmission PredictingCryptosporidiumspreadinwildlemursJournal of Animal Ecology86419ndash433httpsdoiorg1011111365-265612617
Tatsuo H Ono N amp Yanagi Y (2001) Morbilliviruses use signal-ing lymphocyte activation molecules (CD150) as cellular recep-tors Journal of Virology 75 5842ndash5850 httpsdoiorg101128JVI75135842-58502001
TungJBarreiroLBJohnsonZPHansenKDMichopoulosVToufexis D hellip Gilad Y (2012) Social environment is associatedwithgeneregulatoryvariation intherhesusmacaqueimmunesys-tem Proceedings of the National Academy of Sciences of the United States of America 109 6490ndash6495 httpsdoiorg101073pnas1202734109
von Messling V Svitek N amp Cattaneo R (2006) Receptor (SLAM[CD150]) recognition and theV protein sustain swift lymphocyte-basedinvasionofmucosaltissueandlymphaticorgansbyamorbil-livirus Journal of Virology806084ndash6092httpsdoiorg101128jvi00357-06
Vazquez-ProkopecGMBisanzioD Stoddard S T Paz-SoldanVMorrisonACElderJPhellipKitronU(2013)UsingGPStechnol-ogytoquantifyhumanmobilitydynamiccontactsandinfectiousdis-easedynamicsinaresource-poorurbanenvironmentPLoS ONE8e58802httpsdoiorg101371journalpone0058802
Volz E amp Meyers L A (2007) Susceptiblendashinfectedndashrecovered ep-idemics in dynamic contact networks Proceedings of the Royal Society of London B Biological Sciences2742925ndash2934httpsdoiorg101098rspb20071159
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleMarescotLBenhaiemSGimenezOetalSocialstatusmediatesthefitnesscostsofinfectionwithcaninedistempervirusinSerengetispottedhyenasFunct Ecol 2018321237ndash1250 httpsdoiorg1011111365-243513059
![Biografie Florian Hofer [Deutsch]](https://static.documents.pub/doc/80x56/568c3b971a28ab0235aab3bb/biografie-florian-hofer-deutsch.jpg)
