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Diversification of Neotropical Pitvipers

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Diversification of Neotropical Pitvipers DiversificationintheNeotropics:InsightsfromDemographicandPhylogeneticPatterns ofLanceheadPitvipers(Bothropsspp.) DISSERTATION PresentedinPartialFulfillmentoftheRequirementsfortheDegreeDoctorof PhilosophyintheGraduateSchoolofTheOhioStateUniversity By ChristianDavidSalazarValenzuela,B.S. GraduatePrograminEvolution,EcologyandOrganismalBiology TheOhioStateUniversity 2016 DissertationCommittee: Dr.H.LisleGibbs(Advisor) Dr.PaulA.Fuerst Dr.ThomasHetherington Dr.JohnFreudenstein 1 Copyrightby ChristianDavidSalazarValenzuela 2016 2 Abstract TheNeotropicsisthemostspeciesͲrichregionintheworld.Thecurrentdiversity anddistributionoflineagespresentinthisregionisinparttheresultofcomplex ecologicalandevolutionarytrendsdeterminedbyenvironmentalvariablesthathave operatedatdiversespatialandtemporalscales.Inaddition,demographicprocesses havealsoinfluencedthestructureofpresentͲdayphylogeographicpatterns.Several studieshaveusedNeotropicalpitvipersasmodelorganismstoexplorehistorical diversificationpatternsandecologicalprocessesthatproducediversityinthisregion. However,fewofthosestudieshaveexploredpatternsofdiversificationforgroupsof pitviperslikelyinfluencedbyoneofthemostsalientfeaturesoftheSouthAmerican continent:TheAndes.Here,Iuseacombinationofmolecular,morphological,and geographicaldatatoexplorediversificationpatternsandtheevolutionarymechanisms implicatedinthedivergenceoftwodistinctmembersofthegenusBothrops.First,I examinecrypticdiversitypresentinthewidespreadandmedicallyimportantsnakesof theB.asperspeciescomplex(Chapter2).Usingagenomicandmorphologicaldataset collectedacrossthedistributionofthegroup,Iidentifiedextensivephylogeographic ii structure,suggestingtheinfluenceofgeographicbarriersand/ordifferencesin ecologicalnichesintherecentdiversificationinthegroup.Adeepdivergencebetweena CentralandSouthAmericancladeisevident,butmorerecentlydivergedgroupsin SouthAmericashowcomplicatedpatternssuggestiveofrecentdivergenceand/orgene flowamonglineages.Next,IusethisinformationtoperformmodelͲbasedanalysesto investigatethedemographicprocessesinvolvedintherecentoriginoftwoEcuadorian montanelineagesofthesepitvipers(Chapter3).Thisapproachallowedmetoresolve someofthediscrepanciesofevolutionaryrelationshipsfoundinChapter2.Ifound evidencefortheisolationofoneofthemontanelineagesindryinterͲAndeanvalleys, whichseemtobeimportantdriversforthediversificationofthisgroupinSouth America.Finally,inChapter4Ideveloppredictivedistributionmapsforanendangered speciesofAndeanpitviper,B.lojanus,andbasedongeneticandmorphologicaldata identifytwodistinctgeneticgroupsinneedofconservationaction.Theevolutionary mechanismsandpatternsidentifiedinthesesnakesprovideinsightsintotheforces shapingtropicalbiodiversitywhilealsoofferingpracticalinformationforthe conservationandimprovedcoexistencewiththesefascinatingorganisms. iii Dedication ToPaola,Ruth,andMario iv Acknowledgments Thisefforthascometofruitionthankstoanumberofindividualsandinstitutions thathavecollaboratedwithme.Iamdeeplygratefulforhavingmetandworkedwith suchamazingindividualswhomadethisexperienceenrichingandlifechanging.First,I owemygratitudetomyresearchadvisor,H.LisleGibbs,foracceptingmeintohislab andgivingmeboththeindependencetodelineateandworkonmyresearchquestions, aswellassettinghighstandardsthatmotivatedandinspiredme.Hispatience,support andmotivationhavebeenkeytomefinishingthisdissertationfeelingthatI accomplishedwhatIsetouttodowhenIfirstarrivedatOSU.Iwouldalsoliketo expressmysincerethankstomycommitteemembers,JohnFreudenstein,Tom Hetherington,andPaulFuerstfortheiradviceandguidanceonhowtoimprovethis work.Myinteractionswiththemhavebeenthoughtprovokingandusefultoincrease myunderstandingofEvolutionaryBiology.Furthermore,Iwouldliketothankother EEOBfacultywhoseseminarshaveenhancedmyknowledge:BryanCarstens,Laura Kubatko,MegDaly,andAndreaWolfe. v Severalpeoplehelpeddevelopthisresearchthroughstimulatingdiscussions, professionalcollaboration,andlogisticsassistance.IwouldliketothankUlrichKuch, OmarTorresͲCarvajal,PabloAmaruLoaiza,EricSmith,WolfgangWüster,Mahmood Sasa,MónicaSaldarriaga,JimmyGuerrero,FelipeLiévano,SergioCubides,Jorge Valencia,SantiagoAyerbe,JoséMaríaGutierrez,BrunoLomonte,MarioGrijalva,Juan ManuelDaza,GustavoSilva,LuisColoma,ChristopherParkinson,andJonathan Campbell. Also,myearnestthankstocurrentandformermembersoftheGibbslab.Their friendship,insightfulobservations,andconstructivecriticismshavebeeninvaluable. ThankstoMikeSovic,TonyFries,JoséDiaz,MattHolding,RobDenton,JimmyChiucchi, SarahSmiley,OleksanderZinenko,andKatieGreenwald.SpecialthankstoJoséand Mikefortheirassistanceandinstructioninthelaboratory.Iwouldalsoliketothankmy fellowEEOBgraduateandpostͲdoctoralstudents:IsaacLigocki,EricMcCluskey,Erin Lindstedt,JordanSatler,PaulBlischak,MichaelBroe,JasonMacrander,Orlando Combita,JuanCarlosPenagos,SuiPhang,andBenTitusfortheirsupport,friendship, andconstantencouragement. Iwouldequallyliketoacknowledgethecollaborationgivenbymycolleaguesand friendsattheMuseumofZoology,PontificalCatholicUniversityofEcuador:Santiago Ron,AndreaRodríguez,FernandoAyala,andDiegoPaucar.Thankstoallthepeoplethat havecomewithmetoremotelocationsinthemiddleofthenighttolookforsnakes: DarwinNuñez,WilliamandPaolaSantacruz,RuthValenzuelaandespeciallyPablo vi AmaruLoaiza.TothefacultyandstudentsoftheMaster’sPrograminConservation Biology,PontificalCatholicUniversityofEcuadorfortheirsupportandsolidarity.Also,I wanttorecognizethefinancialandlogisticalsupportfromtheinstitutionsthathave grantedresearchfundstopursuethisworkandextendmygratitudetotheCommission FulbrightEcuadorandtheFulbrightͲSenescytcooperationforprovidingmewitha scholarshiptostartmygraduatestudies. Finally,Iwouldliketoextendmydeepestgratitudetomyfamilyforsupporting methroughthisprocess,inspiringmetoworkhard,andkeepingmesane.Mymother’s strengthofcharacter,myfather’sdedication,andtheircommitmenttomedicine startedmeonthispath.Tomysiblingsandtheirfamiliesfortheirloveandsupport.I wouldespeciallyliketothankmywife,Paola,forthesacrificesshehasmadetobeable tosupportandencourageme.Abigpartofthisaccomplishmentbelongstoyou! Finally,thisworkwouldnothavebeenpossiblewithoutthepeopleoftheruralareasof Ecuadorwhoduringmyfieldtripswerealwayscooperative,curiousaboutmywork,and wagertosharetheiranecdotesandexperiences.Ihavegreatappreciationfortheirhard workandtheirconstantwillingnesstosharetheirknowledgeaboutnature. vii Vita 2007...............................................................B.S.Biology,PontificiaUniversidadCatólica delEcuador,Quito,Ecuador. 2009Ͳ2011.....................................................FulbrightScholar,DepartmentofEvolution, EcologyandOrganismalBiology,TheOhio StateUniversity 2011topresent.............................................GraduateTeachingandResearchAssociate, DepartmentofEvolution,Ecologyand OrganismalBiology,TheOhioState University Publications SalazarͲValenzuela,D.,A.Martins,L.AmadorͲOyola,andO.TorresͲCarvajal.2015.Anew speciesandcountryrecordofthreadsnakes(Serpentes:Leptotyphlopidae)from northernEcuador.Amphibian&ReptileConservation8:107–120. SalazarͲValenzuela,D.,D.MoraͲObando,M.L.Fernández,A.LoaizaͲLange,H.L.Gibbs, andB.Lomonte.2014.Proteomicandtoxicologicalprofilingofthevenomof Bothrocophiascampbelli,apitviperspeciesfromEcuadorandColombia.Toxicon 90:15–25. viii SalazarͲValenzuela,D.,O.TorresͲCarvajal,andP.Passos.2014.Anewspeciesof Atractus(Serpentes:Dipsadidae)fromtheAndesofEcuador.Herpetologica70: 350–363. SalazarͲValenzuela,D.,E.O.Carrillo,andS.Aldás.2010.Tricheilostomaanthracinum: geographicdistribution.HerpetologicalReview41:111–112. Bravo,F.andD.SalazarͲValenzuela.2009.AnewspeciesofSycoraxCurtis(Diptera, Psychodidae)collectedonharlequinfrogs(Anura:Bufonidae,Atelopus)inthe EcuadorianAndes.Zootaxa2093:37–42. Passos,P.,D.F.CisnerosͲHeredia,andD.SalazarͲValenzuela.2007.Rediscoveryand redescriptionoftherareAndeansnakeAtractusmodestus.Herpetological Journal17:1–6. ProañoͲBolaños,C.,A.MerinoͲViteri,P.PeñaͲLoyola,andD.SalazarͲValenzuela.2007.A midaltitudereportofBatrachochytriumdendrobatidisinEcuador.Froglog82:3– 4. Boada,C.,D.SalazarͲValenzuela,A.FreireLascano,andU.Kuch.2005.Thedietof Bothropsasper(Garman,1884)inthePacificlowlandsofEcuador.Herpetozoa 18:77–79. FieldsofStudy MajorField:Evolution,EcologyandOrganismalBiology ix TableofContents Abstract................................................................................................................................ii Dedication...........................................................................................................................iv Acknowledgments................................................................................................................v Vita....................................................................................................................................viii TableofContents.................................................................................................................x ListofTables.....................................................................................................................xvi ListofFigures..................................................................................................................xviii Chapter1:Introduction......................................................................................................1 References.......................................................................................................................5 Chapter2:AnalysisofgenomicͲlevelvariationprovidesinsightintotherecent
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