A Comparative Analysis of Viral Richness and Viral Sharing in Cave-Roosting Bats


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A Comparative Analysis of Viral Richness and Viral Sharing in Cave-Roosting Bats

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Title:
A Comparative Analysis of Viral Richness and Viral Sharing in Cave-Roosting Bats
Series Title:
Diversity
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Willoughby, Anna R.
Phelps, Kendra L.
Consortium, PREDICT
Olival, Kevin J.
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English

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Chiroptera ( local )
Caves ( local )
Roosting Behavior ( local )
Viruses ( local )
Ecological Traits ( local )
Virus-Host Associations ( local )
Zoonosis ( local )
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serial ( sobekcm )

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Abstract:
Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or destroyed by human activities such as tourism and extractive industries. In addition to degrading the habitats of cave-roosting bats, such activities often promote contact between humans and bats, which may have potential impacts on human health. Cave-roosting bats are hosts to diverse viruses, some of which emerged in humans with severe consequences (e.g., severe acute respiratory syndrome coronavirus and Marburg virus). Characterizing patterns of viral richness and sharing among bat species are therefore important first steps for understanding bat-virus dynamics and mitigating future bat-human spillover. Here we compile a database of bat-virus associations and bat species ecological traits, and investigate the importance of roosting behavior as a determinant of viral richness and viral sharing among bat species. We show that cave-roosting species do not host greater viral richness, when accounting for publication bias, diet, body mass, and geographic range size. Our global analyses, however, show that cave-roosting bats do exhibit a greater likelihood of viral sharing, especially those documented in the literature as co-roosting in the same cave. We highlight the importance of caves as critical foci for bat conservation, as well as ideal sites for longitudinal surveillance of bat-virus dynamics.
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Diversity, Vol. 9, no. 3 (2017-08-28).

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K26-05211 ( USFLDC: LOCAL DOI )
k26.5211 ( USFLDC: LOCAL Handle )

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Article AComparativeAnalysisofViralRichnessandViral SharinginCave-RoostingBats AnnaR.Willoughby 1 ,KendraL.Phelps 2 ID ,PREDICTConsortium 3 andKevinJ.Olival 1, * 1 EcoHealthAlliance,460West34thStreet,17thFloor,NewYork,NY10001,USA; willoughby@ecohealthalliance.org 2DepartmentofBiologicalSciences,TexasTechUniversity,Lubbock,TX79409,USA;kendra.phelps@ttu.edu3OneHealthInstitute,SchoolofVeterinaryMedicine,UniversityofCaliforniaDavis,Davis,CA95616,USA;predict@ucdavis.edu * Correspondence:olival@ecohealthalliance.org;Tel.:+1-212-380-4460 Received:15July2017;Accepted:22August2017;Published:28August2017 Abstract:Cavesprovidecriticalroostinghabitatsforbatsglobally,butareincreasinglydisturbedordestroyedbyhumanactivitiessuchastourismandextractiveindustries.Inadditiontodegradingthehabitatsofcave-roostingbats,suchactivitiesoftenpromotecontactbetweenhumansandbats,whichmayhavepotentialimpactsonhumanhealth.Cave-roostingbatsarehoststodiverseviruses,someofwhichemergedinhumanswithsevereconsequencese.g.,severeacuterespiratorysyndromecoronavirusandMarburgvirus.Characterizingpatternsofviralrichnessandsharingamongbatspeciesarethereforeimportantrststepsforunderstandingbat-virusdynamicsandmitigatingfuturebat-humanspillover.Herewecompileadatabaseofbat-virusassociationsandbatspeciesecologicaltraits,andinvestigatetheimportanceofroostingbehaviorasadeterminantofviralrichnessandviralsharingamongbatspecies.Weshowthatcave-roostingspeciesdonothostgreaterviralrichness,whenaccountingforpublicationbias,diet,bodymass,andgeographicrangesize.Ourglobalanalyses,however,showthatcave-roostingbatsdoexhibitagreaterlikelihoodofviralsharing,especiallythosedocumentedintheliteratureasco-roostinginthesamecave.Wehighlighttheimportanceofcavesascriticalfociforbatconservation,aswellasidealsitesforlongitudinalsurveillanceofbat-virusdynamics. Keywords:Chiroptera;caves;roostingbehavior;viruses;ecologicaltraits;virus-hostassociations;zoonosis 1.Introduction 1.1.CavesasCriticalHabitatforBatsGloballyCavesrepresentcriticalroostingsitesforbatsonallcontinents,exceptAntarctica[1].Cavesprovidepermanentroostswithstablemicroclimaticconditionsoptimalforrearingyoungandaswinterhibernacula.Inaddition,cavesprovideshelterfrominclementweatherandpredators[2].Asaresult,caveshousesomeofthelargestaggregationsofbatsintheworld[3].Forexample,MonfortCaveinthePhilippineshousesacolonyoffrugivorousbatsRousettusamplexicaudatusestimatedat2millionindividualswitharoostingdensityof452.3individuals/m2[4],whileBrackenCaveintheUnitedStatesisoccupiedbyroughly20millioninsectivorousbatsTadaridabraziliensis[5].Cavesareoftenstructurallycomplexe.g.,passageways,cracksandcrevices,chambers,providingarangeofroostingopportunitiesthatcanaccommodatespecies-specicpreferencesandsupportaggregationsofahighdiversityofcave-roostingspecies[6].Particularlyinthetropics,caveshavebeenreportedtohousebatsofmorethan10species[3,7,8].Consequently,inmanycountries,asignicantproportionofDiversity 2017 , 9 ,35;doi:10.3390/d9030035www.mdpi.com/journal/diversity

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Diversity 2017 , 9 ,35 2of16nativebatsdependoncavesasroostsites.Forexample,roughly80%ofallbatspeciesinPuertoRicoroostincaves[9],while101of131%batspeciesinChinadependoncavesasroosts[10]. 1.2.ViralDiversityinCave-andNon-Cave-RoostingBatsAllmammalsharborviruses,butviralrichnessisnotuniformamongspeciesormammalianorders.Bats,rodents,primates,andtwoungulateordersareeachhosttoanoverallgreatertotalnumberofvirusesperspeciesascomparedtoothermammalianorders,aftercontrollingforresearcheffortandotherspecies-specicfactors[11].However,batshavethegreatestproportionofzoonoticvirusesi.e.,virusesthatcaninfectanimalsandhumansperspeciesascomparedtoothermammalianorders[11],potentiallyduetotheiruniquelife-historytraitsorinnateimmunesystem[12,13].WithintheorderChiroptera,severalstudieshaveexaminedtheecologicalandlife-historytraitsassociatedwithviralrichnessperspecies[11,14–18].Ecologicaltraitsknowntoincreaseviralrichnessinbatsincludelargegeographicrangesizeandhighnumberofsympatricspecies.Highlevelsofpopulationgeneticstructure,largecolonysize,lowconservationthreatlevel,heavierhostbodymass,anddietarybreadtharesomeofthechiropteranlife-historytraitsthathavebeenassociatedwithhighpathogenrichness.Luisetal.[14]includedpropensitytoroostincavesasanexplanatoryvariableforviralsharingamongasubsetof52batspecies,butroostingbehaviorotherwisehasnotbeenexplicitlytestedasadeterminantofviralrichnessorviralsharing.Cave-roostingbatspeciesarespecicallyknowntobereservoirsforseveralzoonoticvirusesincludingsevereacuterespiratorysyndromeSARScoronavirusandMarburgvirus[19,20],aswellashosttonovelvirusescloselyrelatedtoEbolavirus[21,22].Speciccladesofvirusesareoftenprimarilyassociatedwithcloselyrelatedbattaxa;forexample,theSARScoronavirusesareprimarilyfoundinthegenusRhinolophus,whichincludesanumberofcave-roostingspecies[23,24].Otherviralgroupsappeartobesharedmorewidelyacrossbattaxawithvaryingecologicalandlife-historytraits,particularlygeneralistvirusessuchaslyssavirusesandmosquito-borneaviviruses[25]. 1.3.DiseaseEcologyandUniqueTraitsofCave-RoostingBatSpeciesSeveraltraitsuniquetocave-roostingspeciesmayhelpinmaintainingagreaterpoolofvirusesgreaterviralrichnessand/orhelpfacilitateviralsharingamongspecies.Closecontactbetweenconspecicindividualsroostinginconnedcavescouldfacilitatesustainedviralmaintenanceandpotentiallygreaterviralrichness,thoughthereareconictingndingsintheliteratureabouttheimportanceofgregariousnessinbat-virusdynamics[14,16].Densematernitycoloniesincavescouldenhanceintraspecictransmission.Synchronousandseasonalbreedinginhigh-densitybatcoloniesintroducesapulseofsusceptibleindividualsi.e.,offspringthatcouldincreaseratesofviraltransmissionandcirculation,withapeaktypically3monthsafterbirth,whenmaternalantibodieshavewaned[26,27].Diversebatassemblagesfoundco-roostingincaveswillalsolikelypromoteviralcirculationandmaintenancebetweenbatsofdifferentspeciesthattypicallywouldnotinteractwhileforaging,orotherwise,outsideoftheroost.Interspeciccontactbetweenindividualsincavescouldalsofacilitatehostswitchingofvirusesbetweenbatspecies.Successfulviralestablishmentinanovelpreviouslyuninfectedspecies,however,dependsinpartonotherbehavioralfactorsandonthephylogeneticrelatednessofspecies[11,28].Justascavesprovidestablemicroclimaticconditionsandsheltertobats,theymayprovideoptimalenvironmentsthatpromoteviralpersistenceoutsidethehost.Cavestypicallymaintainconsistenttemperatureandhumidityprolesandlackultravioletradiation,allofwhichareimportantenvironmentalfactorsinuencingviraldecay[29,30].Theseabioticfactors,inpart,contributetothelong-termpersistenceofthefungalpathogenPseudogymnoascusdestructans,thecausativeagentofwhitenosesyndromeinbatcoloniesacrossNorthAmerica,andpotentiallyotherhumanpathogenicbacteriaincaves[31,32].Theroleofcaveenvironmentsonviralsurvivalneedsfurtherinvestigationthroughbothenvironmentalsamplingandexperimentalstudies.RecentdetectionofGroupCBetacoronavirusRNAinbatguanofromcaveoorsinThailand,however,demonstratesthepotentialforindirectviraltransmissionincaves[33].

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Diversity 2017 , 9 ,35 3of16 1.4.Human-CaveBatInteractionsNearlyhalfofallbatspeciesthatusecavesasroostsarethreatenedorendangered[15].Thishighlightstheincreasingpressurethatcaveecosystems,andcave-roostingbats,areunderfromamultitudeofhumandisturbances.Anthropogenicstressorscouldalsoleadtoanincreaseinviralsheddinginbatpopulations,thusmakinghuman-batinteractionsmorehazardous[15].Increasingevidencesupportstheassumptionthathabitatqualityandbathealthareinherentlylinked.Forexample,inpaleotropicalforestswithintenseloggingandfragmentation,batswithpoorbodyconditionsweremorelikelytoshedastrovirusesinfeces[34].Seltmannetal.[34]speculatedthatincreasedsusceptibilityofindividualstoacquireandshedvirusesmayhaveresultedfromstress-inducedimmunosuppression.Humanvisitationtocavesfortourism,religiousceremonies,bathunting,quarryingoflimestoneandphosphate,andharvestingotherbiologicalresourcesincavescanpotentiateinteractionsbetweenhumansandcave-roostingbats.Quarryingposesthegreatestthreattocave-roostingbats,resultinginthedirectandirreversiblelossofpermanentroostsites[35,36].SpecieslossismagniedfurtherbyoverexploitationthroughunregulatedhuntingforhumanconsumptionaswellaspurportedtraditionalChineseremediese.g.,asthma[37].Frequentandregularvisitsbytouristsincaveshasbeenshowntoincreasecarbondioxidelevelsandaltertemperatureandhumidityprolesincavechambers,causingbatstoabandonroosts[38].Extractionofbiologicalresourcesincaves,particularlytheharvestingofbatguanoforfertilizer,caveswiftletnestsforbird'snestsoup,andmineralformationsforsouvenirse.g.,stalactites,oftendisturbsroostingbats[8,35,36].Theseactivitiestypicallyputlocalworkersinfrequentcontactwithbatexcreta,providingopportunitiesforexposuretovirusesthatmaybeshedinfeces,urine,orsaliva.Forexample,Marburgvirusspilloverfromcave-roostingbatshasbeenlinkedtogoldmining[39,40]andtourism[41]incavesfromDemocraticRepublicofCongoandUganda.Inaddition,destructionofforagingsitessurroundingcavescanserveasanadditionalstressortocave-roostingbatsthatmaypromotesusceptibilitytoinfection.Urbanandagriculturalexpansion,inadditiontocommerciallogging,oftenresultsinextensivedeteriorationanddestructionofforestedhabitatsthatserveascriticalforagingsitesforcave-roostingbats[4,36].Collectively,suchthreatsrepresentinescapablestressorstobatsthatmayalsoincreasethesusceptibilityofindividualbatstoviralinfections,promotecontactbetweencave-roostingbatsandhumans,and/orprovideopportunitiesforviralspillover. 1.5.StudyObjectivesCave-roostingbatspeciescompriseasignicantproportionofglobalbatdiversity,yetareunderincreasinganthropogenicpressurethatcouldleadtofutureviralspilloverevents.Giventhesetwocriticalissues,ourprimarystudyobjectiveistoaggregateexistingdataanddevelopcomparativeanalysestobetterunderstandpatternsofviralrichnessandviralsharingwithincave-roostingbatspeciesandbetweencave-andnon-cave-roostingbatspecies.Specically,weaimtodeterminetherelativeimportanceofroostingbehavioronbothviralrichnesswithinandviralsharingamongbatspecies.Weaddressthefollowingthreequestions:Iscave-roostingbehavioradriverofviralrichnesswhenconsideredtogetherwithasuiteofotherecologicalandlife-historytraits?Whatfactorsarethemostimportantdeterminantsofviralsharingbetweenbatspecies?Istheregreaterviralsharingbetweenco-roostingspeciesthanspecieswithoutdocumentedco-roostingbehaviorincaves? 2.MaterialsandMethods 2.1.DatabaseofViralAssociationsandHostTraitsWecompiledadatabaseof595virus-hostassociationsfor114viralspeciesand205batspecies.VirusnamesweresynonymizedtotheInternationalCommitteeontheTaxonomyofVirusesICTV2016version1[42],andonlyvirusesassignedaspeciesnamewereincludedinourdatabase.Batspecies

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Diversity 2017 , 9 ,35 4of16weresynonymizedaccordingtotheInternationalUnionforConservationofNatureandNaturalResourcesIUCNRedListofThreatenedSpeciesversion2017[43].Amajorityoftheassociationsn=509werecollectedfromarecentlypublishedmammalianvirusdatabase[11],withadditionalassociationsaddedfromanupdatedliteraturesearchfromthisstudyn=49,aswellaspubliclyavailablehost-virusassociationsfromthePREDICTglobalsurveillanceprogram,n =37,forvirusandhostspeciesthatmetourabovetaxonomiccriteriaSupplementaryTableS1andItemS1[44].WealsoanalyzedasubsetofthedatalimitedtoviraldetectionobtainedthroughPCRorvirusisolation—a`stringent'databaseexcludingserologicalantibodyandantigendetection—tocontrolforpotentialbiasesfromcross-reactivityofrelatedviruses.Thestringentdatabaseincludes153batspecies,82viruses,and277virus-hostassociations.Viralrichness,denedasthenumberofICTV—recognizedvirusesdetectedineachbatspecies,wascalculatedseparatelyforthemainandstringentdatabases.Todetermineroostingbehaviorforeachbatspecies,weperformedaliteraturesearchusingkeywordsinWebofScienceandGoogleScholar.LiteraturesearchesincludedeachspeciesbinomialplusrecenttaxonomicsynonymsAND“roost”.Additionalliteraturesourcestocategorizeroostingbehaviorwerefoundinthereferencesectionofpublicationsobtainedfromtheinitialliteraturesearch.Roostingbehaviorwascategorizedasobligatecave-roostingifaspecieswasdocumentedtoexclusivelyusecavesasroostsites,facultativecave-roostingwhenaspeciesroostsincavesaswellasotherroostsitese.g.,hollowtrees,abandonedbuildings,termitenests,ornon-cave-roostingifaspecieshasnotbeenrecordedtoroostincavesSupplementaryItemS2.Wecollectedadditionalhostlife-historyandecologicaltraitsthatmaybeimportantforexplainingobservedviralrichness.Hosttaxonomy,threatstatus,dieti.e.,frugivore,insectivore,orother,andspatialrangeinformationwereextractedfromIUCN[43].FromtheIUCNspatialshapeles,wecalculatedgeographicrangesizelog10km2andsympatricviralhostspeciesi.e.,countofbatspeciesinbothmainandstringentvirusdatabasesthathaveoverlappingspatialrangeswiththergeospackageinR.SpeciesbodymasswasextractedfromPanTHERIA[45].Asmorecloselyrelatedspecieswillhavesimilarbodymassduetosharedevolutionaryhistory,wecontrolledforthisbycalculatingtheresidualsfromaphylogeneticeigenvectorregressionPVRonbodymass[46,47].AsdescribedinOlivaletal.[11],wecalculatedPVRforbodymassusingtheRpackagePVRandaprunedmammaliansupertreethatonlyincludedbatspeciesinourviraldatabase[48,49].ArtibeusplanirostriswasmanuallyinsertedinthetreenexttoArtibeusjamaicensisperSimmons[50].Toplotviralrichnessfromourmaindatabaseandroostingbehaviorontothephylogeny,thepicanteRpackagewasused.Toaddressresearchbiasamongbatspecies,weextractedthetotalpublicationcountforeachspeciesandknownsynonymsfromPubMedusingtherentrezRpackage.ThezoonoticstatusofvirusesfollowedOlivaletal.[11],butwasupdatedthroughliteraturesearchesofviralbinomialAND“case”OR“human”usingGoogleScholarandPubMed.With205batspeciesinourmaindatabase,thereare20,910uniquespecies-pairswiththepotentialforviralsharingand11,628uniquespecies-pairsforthe153batspeciesinourstringentdatabase.Here,wedeneviralsharingasthedualdetectionofavirusintwobatspecies.Wecreatedseveralsharedtraitsperspecies-pairtotesttheirrelationshipwithviralsharing.Duringliteraturesearchestocategorizeroostingbehavior,iftwoormorespeciesweredocumentedasroostinginthesamecave,wenotedthemasco-roostingspeciesseeSupplementaryTableS3.Forthe201specieswithIUCNrangeinformation,wecalculatedspatialandsympatricspeciesoverlapbetweeneachspecies-pairasproxiesforpotentialinterspeciccontact.Todothis,wecalculatedsquarekilometersofoverlapbetweeneachspecies-pairfromtheirIUCNspatialleusinggIntersectionfunctioninthergeosRpackage.Sympatricspeciesoverlapwascalculatedasthenumberofhostsinourdatabasewhoserangeintersectswithbothspeciesofthepair.Fromourhosttraits,wedeterminedabinarycave-roostingbehaviortrait:“Yes”ifbothspecieswereobligateorfacultativecave-roostingand“No”ifonlyoneorneitherspecieswereobligateorfacultativecave-roosting.Similarly,ashareddietbinarytraitwasdetermined:“Yes”ifbothspecieshadthesamedietarynichee.g.,bothfrugivoresor“No”iftheyhaddifferentdietse.g.,oneafrugivoreandoneaninsectivore.Toaccountforresearchbiasindual

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Diversity 2017 , 9 ,35 5of16virusdetectioninthespecies-pair,theminimumpublicationcountfromthetwospecieswasusedasdescribedinG mezetal.[51]. 2.2.ViralRichnessandSharingAnalysesGenerallinearmodelsGLMswereusedtoidentifysignicantpredictorsofviralrichnessandviralsharingforspeciesinbothourmainandstringentdatabases.Variablesfortheviralrichnessmodelsincludedroostingbehavioranddietascategoricalpredictors,andrangesize,phylogenetically-correctedmass,researchefforti.e.,publicationcount,andthenumberofsympatricspeciesascontinuouscovariatesSupplementaryTableS2.Asrangesizeandsympatricspecieswerehighlycorrelatedp<0.001,r=0.60,thesecollinearvariableswerealternatedinourmodelselection.Onlyelevenspecies%wereobligatecave-roosting,sotheobligateandfacultativecategoriesweremergedtocreatebinaryroostingbehaviorvariableof“caving”or“noncaving”.Covariateswerenormalizedtoaccountforscalingdifferences,whileresearcheffortandrangesizewerelog10-transformed.Forviralrichness,wecalculatedcountdataofvirusesperspeciesandusedaPoissondistribution.ForbestviralrichnessGLMs,weconrmedvariablesignicancewhilecontrollingforphylogeneticsignalbyincludinghostfamilyasarandomeffectSupplementaryTableS4.VariablesincludedinourGLMstoassessviralsharingincludedroostingbehaviorcave-ornon-cave-roosting,documentationofco-roostingfromtheliterature,andshareddietasbinarypredictors,andphylogeneticrelatedness,researchefforti.e.,minimumnumberofpublicationsforeachspeciespair,andspatialoverlapkm2ascontinuouscovariatesSupplementaryTableS3.Tocalculatephylogeneticrelatednessbetweenbatspecies,weusedthecopheneticfunctionintheRpackageapetocalculatebranchdistancebetweeneachspeciespaironaversionofthemammaliansupertreeprunedtoonlyincludethespeciesinourdatabase[49].Covariateswerenormalizedtoaccountforscalingdifferences.Numericvariablespublicationcount,phylogeneticdistance,andrangeoverlapsizewerelog10-transformed,asabove.Viralsharingwascalculatedasabinomialdistribution:detectionofatleastonevirusinbothspeciesornovirusdetectedinbothspecies.Forboththeviralrichnessandviralsharingmodels,westartedwithamodelthatincludedonlyroostingbehaviorcave-vs.non-cave-roostingandresearcheffort.Wethenperformedadditionalmodelrunsbasedonaprioriecologicalandlife-historyhypothesesandusedAkaikeInformationCriterionAICvaluestoselectthebestmodelSupplementaryTablesS4andS5.Allanalysesweretestedonthemaindatabaseaswellasourstringentdatabase.Fortheviralsharingmodel,wealsousedadatabaselimitedtospecieswithliteratureveriedco-roosting,meaningtheyco-roostwithatleastoneotherspeciesinourmaindatabasen=74hosts,n=2701species-pairs.CoefcientplotswerevisualizedusingthearmpackageinR.UsingtheigraphpackageinR,weconstructedabipartitenetworktovisualizehost-virusassociationsamongcave-andnon-cave-roostingbatspecies.Weadditionallyforcedaunipartitehostnetworkandcalculatednetwork-levelmetricscomponentsandmodularitytodescribeviralsharingamongbathosts. 3.Results 3.1.DatabaseSummaryandDescriptiveStatisticsOurdatabasecontains205batspeciesassociatedwithatleastonevirusfrom12taxonomicfamilies.Only5ofthe12batfamilies%containbothcave-andnon-cave-roostingspeciesEmballonuridae,Molossidae,Phyllostomidae,Pteropodidae,Vespertilionidae.Theother7familiesarecomprisedofonlycave-roostingspeciesHipposideridae,Megadermatidae,Miniopteridae,Mormoopidae,Natalidae,Nycteridae,Rhinolophidae.Cave-roostingspeciesmakeupthemajority%,146of205speciesofspeciesinourviralhostdatabase.Theglobaldistributionofcave-roostingspecieswithviralinformationwasdistinctfromthenon-cave-roostingspecies,withgreaterrichnessofcave-roostingspeciesatnorthernlatitudesandinSoutheastAsiaandChinaFigure1.BasedonPubMedarticlecounts,batsofcave-roostingspeciesmean=26.7articleshavebeenstudiedmoreextensivelythan

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Diversity 2017 , 9 ,35 6of16non-cave-roostingspeciesmean=9.2articles;t=3.3921,df=191.79,p<0.001.Twenty-sixspecieshadnosearchresultsfortheirscienticnameinPubMed.Batsofthreespecieshavebeenmoreextensivelystudied>300articlesforeachthanbatsofallotherspecies:Eptesicusfuscus,Myotislucifugus,andDesmodusrotundus . Figure1.Hostdistributionmapsforbatspeciesintheviraldatabaseforacave-roostingbatsn =142andbnon-cave-roostingbatsn=59.Batspeciesrichness,regardlessofroostingbehavior,ishighestinSouthandCentralAmerica,butrichnessofcave-roostingspeciesisalsohighinSoutheastAsia,westernNorthAmerica,andsouthernEurope.FourbatspeciesinourdatabasewithoutIUCNspatiallesarenotincludedinthisgureorourgeographictraitanalyses.ThemostrepresentedbatgenerainourdatabasewereMyotisn=25species,Rhinolophusn=16,allcave-roosting,Pteropusn=12,allnon-cave-roosting,andHipposiderosn=12,Figure2.SpeciesinthegenusPteropusareimportantnaturalreservoirsforNipah[52]andHendra[53]viruses,andtheonlygenuslistedabovewithoutrepresentedspeciesusingcavesasroostsites.SomeimportantviralgeneraareexclusivetothebatgeneraRhinolophus,Hipposideros,Miniopterus,Natalus,andPipistrellus,whicharelargelycomprisedofcave-roostingspecies,whileotherviralgeneraareexclusivetobatsofnon-cave-roostinggeneraPteropusandCynomopsorArtibeus,Eptesicus,Lasiurus,andMyotis,whichincludebothcave-andnon-cave-roostingspecies.Eachbatspecieswasobservedtohostonaverage2.90uniquevirusesincludingserologicaldetectionsand1.35virusesusingstringentdetectionsonly.Fifty-threebatspecieshaveonlyhadserologicalviraldetectioncave-roostingand18non-cave-roostingspecies.EidolonhelvumandArtibeuslituratushadthehighestobservedviralrichnessn=18viruses,whileRousettusaegyptiacushadthegreatestnumberofvirusesconrmedviaPCRandviralisolationn=9.Observedviralrichnessperspeciesdidnotsignicantlydifferbetweencave-roostingbatsandnon-cave-roostingbatst=0.89,df=120.57,p=0.38,butthisdoesnotaccountforresearcheffortorotherexplanatoryvariablesseeGLMresultsbelow.

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Diversity 2017 , 9 ,35 7of16 Figure2.Hostphylogenyprunedfromthemammaliansupertreeofabatspeciesincludedinourdatabasen=205,andinsetsshownforthegenera:bMyotis,cRhinolophus,anddPteropus.Facultativecave-roostingbatspeciesinlightgreen,obligatecave-roostingspeciesindarkgreen,andnon-cave-roostingspeciesingrey.Apiechartshowcasingtheproportionofvirusesdetectedineachspeciesviaserologywhiteornucleicacidblueisnexttoeachspecies.

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Diversity 2017 , 9 ,35 8of16Nineteenviralfamilieshavebeendetectedinbats,withtheaviviruses,rhabdoviruses,andcoronavirusesexhibitingthegreatestviralrichness,with26,19,and13viralspeciesrespectively.Onaverage,eachvirushas5.22hostsand2.42stringenthosts.Outofthe82stringentlydetectedviruses,39havebeendetectedviaPCRinonlyasinglehostspecies.Halfofthebat-borneviruses%,59of114virusesarezoonotic,detectedinhumanseitherserologicallyorthroughnucleicaciddetection.Certainviruseshavebeenexclusivelydetectedviaserologicornucleicacidmethodsincave-roostingbats,notablyEuropeanbatlyssavirus1n=14hosts,Issyk-Kulvirusn=13,andSARScoronavirusn=8.Otherwell-knownpathogens,however,havebeendetectedinbothcave-andnon-cave-roostingspecies:rabiesvirusnon-cave-and59cave-roostingspecies,yellowfevervirusnon-cave-and10cave-roostingspecies,andWestNilevirusnon-caveand9cave-roostingspeciesFigure3.Zoonoticviruseshaveagreaternumberofbathostsmean=7.85speciesthannon-zoonoticvirusesmean=2.4species;t= )]TJ/F161 9.9626 Tf 8.194 0 Td [(3.46,df=63.92, p <0.001. Figure3.Bipartitenetworkofbathostssquares,n=153speciesandPCR-detectedvirusescircles,n =82species.Connectedby277associations.Cave-roostingbatsareshowningreenfacultative,n=102andblueobligate,n=10,whilenon-cave-roostingspeciesareshowninyellow.ViralabbreviationsarelistedwithICTVspeciesnameinSupplementaryTableS1. 3.2.ViralRichnessAnalysisTheGLMforviralrichnessperbatspeciesthatbesttourmainandstringentdatabasesincludedper-speciesmeasuresofresearcheffort,phylogenetically-correctedmass,countofsympatricspecies,androostingbehaviorSupplementaryTablesS2andS4.Inbothsetsofmodels,theresearchefforthadtheonlysignicantlypositiveeffect,whileanon-frugivorousdietwastheonlyvariablewithasignicantlynegativeeffectonviralrichness.Phylogenetically-correctedmass,spatialvariablesrangesizeandcountofsympatricviralhostspecies,androostingbehaviordidnothavesignicanteffectsonthemodel.Threatstatuswasnotincludedinouranalysesasonlysevenspeciesincludedinourdatabase%werelistedasvulnerableorendangered. 3.3.ViralSharingAnalysisEverybatspeciesinourdatabasesharesatleastoneviruswithanotherspecies.Onaverage,eachbatspeciessharesatleastoneviruswith31.38otherspeciesinourmaindatabaseor22.16

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Diversity 2017 , 9 ,35 9of16otherspecieswhenlimitingtothestringentlydetectedvirusesFigure3.Whenweexcluderabiesvirus,viralsharingdecreasestoeachbatspeciessharingatleastoneviruswith16.10otherspeciesinourmaindatabaseor7.92otherspecieswhenlimitingtothestringentdatabase.Thisisexhibitedbytheconnectivityofbatspeciesinourforcedunipartitenetwork,ashostsarehighlyconnectedthroughvirusesQ=0.27andevenmoresoforstringentlydetectedvirusesQ=0.21,andrabiesasthemostcentralmeasuredbyeigenvectorcentralityvirusconnectedtothegreatestnumberofhostsn=61;Figure3.Outofthe19,900species-pairswithspatialoverlapinformation,4563%species-pairexhibitspatialoverlap.Onaverage,eachspecieshasanoverlappinggeographicrangewith4623otherbatspecieswithknownviralassociations.Fifty-twopercentofspeciessharetheirdietaryniche,7%arebothfrugivoresand43%arebothinsectivores.Sharedroostingbehaviorwasexhibitedby59%ofspecies-pairs,specically50%ofspecies-pairsbothroostincaves,while9%arebothnon-cave-roostingspecies.Sixty-twopercentofspecies-pairsarephylogeneticallydivergent,withbranchdistances100fromthemammaliansupertree.Roostingbehaviorwasnotasignicantvariableinthebest-tGLMforviralsharingamongspeciesinthemaindatabase.Ourbest-tGLMforviralsharingamongbatspeciesinourstringentdatabaseincludedper-pairmeasuresofresearcheffort,phylogeneticdistance,spatialoverlap,shareddiet,androostingbehaviorFigure4a,SupplementaryTableS5.Forstringentbatspecies-pairs,eachvariablehadasignicantlypositiveeffectexceptshareddiet,whichwasnotsignicant. Figure4.CoefcientplotforthebestviralsharinggeneralizedlinearmodelsforsharedstringentvirusesY/Nbetweenaallbatspecies-pairsn=7864andbco-roostingbatspecies-pairsn =1378.Eachmodelincludespublicationcount,phylogeneticdistance,sharedroostingbehavior,andshareddietaryniche.Spatialoverlapisthebestpredictorforallspecies,whilenumberofsympatricviralhostsperformedbetterintheco-roostingspeciessubset.Allvariablesaresignicant.Seventy-fourbatspeciesinourdatabasehaveliterature-documentedco-roostingbehaviorwithotherviralhostsintheliterature,with181documentedco-roostingpairs%ofthespecies-pairswithco-roostinginformation.Basedonourextensiveliteraturereview,onaverage,eachspecies

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Diversity 2017 , 9 ,35 10of16co-roostswith4.89otherbatspecies,witharangeofonetofteenspecies.Natalusstramineusexhibitedthegreatestco-roostingbehavior,withdocumentedroostsharingincaveswithfteenotherspecies.Ourbest-tmodelforboththemainandstringentdatabasesforthesubsetofco-roostingspeciesincludedreportingeffortalongwithlife-historyandgeographictraits.Thebestpredictorforstringentviralsharingbetweentwoco-roostingspeciesisnumberofbatspecieswithanoverlappingrange,followedbydocumentedco-roostingbehavior,phylogeneticdistance,publicationcount,andshareddietSupplementaryTableS5. 4.Discussion 4.1.CurrentStateofKnowledgeandDataGapsWecompiledacomprehensivelistofvirusesthathavebeendetectedinbatsglobally,andusedthesedatatospecicallytesttherolethatroostingbehaviormayplayasadeterminantofviralrichnessandviralsharinginbats.Wefoundthatmostspeciesinourdatabasearecave-roosting,includingobligateandfacultativecave-roostingbatspecies.Thispartiallyreectsthatmanybatspeciesexhibitapropensitytoroostincaves,butalsodemonstratesimportantbiasesinourknowledgeofroostingbehaviortodate.Manyspeciesthatarefoliage-andtree-roostingareverydifculttocaptureandobservee.g.,highlymigratoryhoarybatsinNorthAmerica[54].Oftenspecialtrappingmethodse.g.,canopynetsusedintall,verticalforestcommunitiesareneededtoadequatelysamplethefulldiversityofbatsinacommunity[55].Ourdatabasesuggestsastrongbiasinviralsamplingofbatsatcaves,wheretheyareeasiertocaptureandcanbereliablylocatedandsampled.Moreover,weonlyhavedocumentedviralassociationsi.e.,ICTV-namedvirusesfor205speciesglobally,representingroughly16%ofthedocumented1300speciesintheorderChiroptera[56].Additionaldatafrombatspeciessampledacrossmorediverseroosttypesmayleadtoadifferentpictureontheroleofroostingbehaviorandroostingsubstrateonviralrichnessandsharing. 4.2.ViralRichnessWithinBatSpeciesWhenwecontrolforresearchbiasandotherspecies-specictraitsinourmultivariatemodel,wefoundthatroostingbehaviori.e.,whetherornotaspeciesroostsincaveswasnotasignicantpredictorofviralrichnessforthe205batspeciesincludedinouranalysis.Thisdisagreeswiththeoneotheranalysisofroostingbehaviorandviralrichness[14];however,thisstudywaslimitedto52batspecieswithroostingbehaviorinformation.Ourndingssupportpreviouslypublishedwork,indicatingthatdietwasanimportantlife-historytraitforviralrichness[18,57].Frugivorousbatshostmorevirusesthanotherdietaryguilds.Phylogenetically-correctedmassandspatialfactorssuchasgeographicrangesizeandnumberofsympatricbatspecies,weresurprisinglynotsignicantpredictorsofviralrichnessinourstudy,astheyhadbeenpreviouslyidentiedasanimportantvariableinotherspecies-levelanalysesofviralrichness[11,18,58].Dietarynicheandfeedingbehaviorsmaycontributetoabat'sexposuretoandspreadofviralpathogens.Frugivorousbatshavebeenknowntotransmithenipavirusesviatheirurine,feces,andsalivain“dripzones”aroundfruitingtrees[27].WhiletheseinfectedforagingareashavebeenimportantforNipahvirusspilloverintopigsandHendravirusspilloverintohorses,theroleofcontaminatedfoodinviraltransmissionamongbatsislessclear.Theenvironmentalandagriculturalbenetsoffrugivorousbats,conversely,arewelldocumented.Frugivorouscave-roostingbatsareinstrumentalintheformation,regeneration,andmaintenanceoftropicalforests,duetotheirseeddispersalcapabilities[59].Forinstance,lesserdawnbatsEonycterisspelaea,anobligatecave-roostingspecies,aretheprimarypollinatorsofdurianandpetai[60,61],whichgeneraterevenuesinsouthernThailandthatexceed$137millionannually[62].Thesepositiveecologicalandeconomicbenetsmustbeconsideredinanydiscussionregardingtheecosystemservicesi.e.,pollination,insectcontrolordisservicesi.e.,asdiseasereservoirsthatcave-roostingbatsprovide.

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Diversity 2017 , 9 ,35 11of16 4.3.ViralSharingAmongBatSpeciesViralsharingamongbatsiscommon:halfofthebat-associatedvirusesinourdatabase%haveinfectedmultiplebatspecies,demonstratingevidenceforviralhostshiftsamongspecies.Themostsharedvirusis,unsurprisingly,rabies—amammaliangeneralistvirushostedanddetectedin61ofthe205%batspeciesinourdatabase.Outofthe15virusesinourdatabasewiththegreatestnumberofbathostspecies,onlytwohavenotyetbeendetectedinhumanpopulations:Lagosbatvirusn=6batspeciesandMiniopterusbatcoronavirus1n=5batspecies.Formostknownhumanviruses,thereisaresearcheffortbiasthathasledtotheidenticationofabroaderrangeofhostspecies.Rabiesinparticularhasreceivedtargetedsurveillanceduetoitslonghistoryasasevere,andoftenfatal,viralinfectioninhumansanddogs.Additionally,severalofthevirusesthatwouldbecategorizedasspecialistvirusesinourdatabaseonlyviralnucleicaciddetectionfoundinonebatspeciesareactuallyhostedbyspeciesinothervertebratetaxa,includingAvesbirds;e.g.,WestNileandNewcastlediseasevirusesorPrimatese.g.,Bocavirus1and2.Theinter-orderhostrangeofthesevirusesmaybeakeyfactorintheirabilitytoinfect,andbepathogenic,inhumans,butfurtherresearchisneeded.Wefoundthatsharingofvirusesismorelikelybetweencave-roostingvs.non-caveroostingspecies,thoughthegreatestpredictorofviralsharingisdegreeofspatialoverlapbetweenaspecies-pair.Co-roosting,however,consistentlywasthegreatestpredictorofviralsharingforbothourmainandourstringentdatabases.Formodelsinwhichweincludedco-roostingbehavior,phylogeneticdistancebetweenbathostshadasignicantlypositiveeffectonlyforstringentviralsharing,andshareddietwassignicantlynegative.Thesendingsdifferfrompreviousstudiesinbats[28],andalsotrendsfoundmorebroadlyacrossmammals[11].Thismaybeduetoco-roostingbatspeciesoftenbeingfromdivergenttaxonomicgroupsordietaryniches.Thus,ecologicalopportunityanddirectcontact,ratherthansharedlife-historytraitslikedietandphylogeny,arekeytoviralsharingbetweenspecies.Thebarrierstoviralsharingamongspeciesarepoorlyunderstood.Whilesomeviruseshavebeendetectedinbatsofphylogeneticallydistinctclades[63],othersgroupsofvirusesarethoughttohavecloselyevolvedwithasinglespecies.Newevolutionaryanalysesofherpesviruses,however,haverecentlydemonstratedthatthesehistoriclineagesmaybecomprisedofmorefrequenthost-switchingeventsthanpreviouslythought[64].Also,whilesomevirusesarehostedbymultiplespecies,specicstrainsofaviralspeciesmaybeconstrainedtobatsofasinglespeciesorphylogeneticallyrelatedhosts[28].Viralsharingamongadiverserangeofhosttaxa,aswehaveidentiedhereamongdivergentcave-sharingbatspecies,isaknowndriverofzoonoticspillover[11,65],potentiallyduetoadaptiontomultiplehostcellreceptors[66]. 4.4.CaveatsandFutureDirectionsFurtherworktodetermineandunderstandtheviromeofbatsandexpandthelistofknownhost-virusassociationswillcontinuetoshedlightonthegeographic,functional,andtemporaldynamicsofviralinfectionacrossmultiplebatspecies[67],aswellasidentifyspatialgapsinviralsurveillance.Standardizedeldsurveillanceintargetedsitesarebeginningtollthesegaps[23].Ourcalculatedspatialvariablesrelyonanassumptionthatviraldistributionextendsacrossaspecies'entiregeographicrange[11,68],althoughpathogendistributionislikelymoreconstrainedtocertainbatpopulationsorhabitatfragments.Hosttraitsnotassessedinthisstudy,butmaycontributetoviralrichness,includelevelofmigration,gregariousness,andcavetype[14].Cavescanvarygreatlyinsizeandmicroclimaticproles,whichmayinuenceviralpersistenceandviralsharingamongbatspeciescommunitieswithincertaincaveenvironments.Forouranalyses,weusedacategoricalhosttraittodescriberoostingbehavior,eithercave-roostingobligateorfacultativeandnon-cave-roosting.Finerscalecriteriaofthepermanence,temperature,oraccessibilityofroostsitemaybeimportantforpathogenpersistenceintheenvironment[69].Exclusionoftheseadditionalfactorswaslargelyduetoincompleteandscatteredliteraturethatwouldhavegreatlyreducedthenumberofhostspecieswithcompletedata.Asvirusdiscoverybecomeslesstimeandcostintensive[70,71],thesehost-virus

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Diversity 2017 , 9 ,35 12of16associationsneedtobecontinuouslycompiledintointerpretabledatabaseinconjunctionwithadequatehostecologicalandlife-historytraits.Astheviralcommunitiesofcave-roostingbatshaveonlybeenpartiallycharacterized,muchremainsunknownabouttheriskofviralspilloverfromcaveecosystems.However,whatisknownisthattheriskofpathogenspillovertohumansfromanywildlifespeciesisdrivenbyanthropogenicdisturbanceandincreasedcontactrates,alongwithhost-specicfactorslikephylogeneticrelatednesstohumans[11,72].Tragically,cave-roostingbatsareunderpressurefromamultitudeofhumanthreatsatroostingsites,andthiscontactnotonlystressesthebats,butalsointroducesopportunityforzoonoticspillover.Whilerare,virusspilloverfromcave-roostingbatstohumansincaveshaveoccurred.Forexample,Marburgvirusfatallyspilledoverfromcave-roostingbatsintoworkersattheKitakaMineandtouristsatthePythonCaveinUganda[26,73].Ouranalysisshowsthatcave-roostingbehaviorisanimportantdriverofviralsharinginbats.Thisndingalonesuggeststhatmorein-depthandlongitudinalsurveillanceeffortsaimedatcave-roostingbatspecieswillbevaluabletobetterunderstandtheecologicalmechanismsthatpromoteviralsharing.Cavesareidealsitesforviralsurveillanceascomparedtoothereldsites,duetoconsistentbatpopulations,predictableexitingtimes,andamplebatguanofornon-invasivesampling.Asviralsurveillanceincave-roostingspeciesexpandsinthefuture,wemustbeconscioustoutilizednon-lethalsamplingmethodsandminimizehabitatdisturbancetothesevulnerableandecologicallyimportantspecies,whilesimultaneouslyndingwaystoassessandmitigatetheriskofzoonoticspillover. SupplementaryMaterials:Thefollowingareavailableonlineatwww.mdpi.com/1424-2818/9/3/35/s1,ItemS1:VirusReferences,ItemS2:RoostingBehaviorReferences,TableS1:Bat-VirusAssociations,TableS2:HostTraits,TableS3:Species-PairTraits,TableS4:ViralRichnessGLMsummaries,TableS5:ViralSharingGLMsummaries. Acknowledgments:ThisworkwasmadepossiblebythegeneroussupportoftheAmericanpeoplethroughtheUnitedStatesAgencyforInternationalDevelopmentUSAID.ThecontentsaretheresponsibilityofthePREDICTConsortiumanddonotnecessarilyreecttheviewsofUSAIDortheUnitedStatesGovernment.TheauthorsthankthePREDICTin-countryteamsandglobalteamfortheircontributionofbat-virusassociationstothisdatabase.TheauthorsthankC.N.BasarabaandB.Watsonforassistancewithspatialanalyses. AuthorContributions:AnnaR.Willoughby,KevinJ.OlivalandPREDICTConsortiumdesignedthestudyandstatisticalapproach.AnnaR.WilloughbyandKevinJ.Olivalwrotethecode.KendraL.Phelps,PREDICTConsortiumandAnnaR.Willoughbycollectedthedata.AnnaR.Willoughbygeneratedgures.AnnaR.Willoughby,KendraL.PhelpsandKevinJ.Olivalwrotethemanuscript.DetailinformationaboutPREDICTConsortiumcanbefoundbythewebsite:www.consortium.predict.global. ConictsofInterest:Theauthorsdeclarenoconictofinterest.Thefundingsponsorshadnoroleinthedesignofthestudy;inthecollection,analyses,orinterpretationofdata;inthewritingofthemanuscript,andinthedecisiontopublishtheresults. References 1.Culver,D.C.;Pipan,T.TheBiologyofCavesandOtherSubterraneanHabitats;OxfordUniversityPress:NewYork,NY,USA,2009;ISBN978-0-1992-1993-3. 2.Kunz,T.H.Roostingecologyofbats.InEcologyofBats;Kunz,T.H.,Ed.;PlenumPublishingCorporation:NewYork,NY,USA,1982;pp.1,ISBN978-1-4613-3423-1. 3.Arita,H.T.ConservationbiologyofthecavebatsofMexico. J.Mammal. 1993 , 74 ,693.[CrossRef] 4.Hutson,A.M.;Mickleburgh,S.P.MicrochiropteranBats:GlobalStatusSurveyandConservationActionPlan;IUCN:Gland,Switzerland,2001;Volume56,ISBN2-8317-0595-9. 5.Mickleburgh,S.P.;Hutson,A.M.;Racey,P.A.Areviewoftheglobalconservationstatusofbats.Oryx2002,36 ,18.[CrossRef] 6.Furey,N.M.;Racey,P.A.Conservationecologyofcavebats.InBatsintheAnthropocene:ConservationofBatsinaChangingWorld;Voigt,C.,Kingston,T.,Eds.;Springer:Cham,Switzerland,2016;pp.463,ISBN978-3-319-25220-9. 7.Brunet,A.K.;Medelln,R.A.Thespecies–arearelationshipinbatassemblagesoftropicalcaves.J.Mammal.2001 , 82 ,1114.[CrossRef]

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