Adaptive speciation theory.docx
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Adaptivespeciationtheory
Adaptivespeciationtheory:
aconceptualreview
Abstract:
Speciation—theoriginofnewspecies—isthesourceofthediversityoflife.Atheoryofspeciationisessentialtolinkpoorlyunderstoodmacro-evolutionaryprocesses,suchastheoriginofbiodiversityandadaptiveradiation,towellunderstoodmicro-evolutionaryprocesses,suchasallelefrequencychangeduetonaturalorsexualselection.Animportantquestioniswhether,andtowhatextent,theprocessofspeciationis‘adaptive’,i.e.,drivenbynaturaland/orsexualselection.Here,wediscusstwomainmodellingapproachesinadaptivespeciationtheory.Ecologicalmodelsofspeciationfocusontheevolutionofecologicaldifferentiationthroughdivergentnaturalselection.Thesemodelscanexplainthestablecoexistenceoftheresultingdaughterspeciesinthefaceofinterspecificcompetition,buttheyareoftenvagueabouttheevolutionofreproductiveisolation.Mostsexualselectionmodelsofspeciationfocusonthediversificationofmatingstrategiesthroughdivergentsexualselection.Thesemodelscanexplaintheevolutionofprezygoticreproductiveisolation,buttheyaretypicallyvagueonquestionslikeecologicalcoexistence.Bymeansofanintegratedmodel,incorporatingbothecologicalinteractionsandsexualselection,wedemonstratethatdisruptiveselectiononbothecologicalandmatingstrategiesisnecessary,butnotsufficient,forspeciationtooccur.Toachievespeciation,matingmustatleastpartlyreflectecologicalcharacteristics.Theinteractionofnaturalandsexualselectionisalsopivotalinamodelwheresexualselectionfacilitatesecologicalspeciationevenintheabsenceofdivergingfemalepreferences.Inviewoftheseresults,itiscounterproductivetoconsiderecologicalandsexualselectionmodelsascontrastingandincompatibleviewsonspeciation,onebeingdominantovertheother.Instead,anintegrativeperspectiveisneededtoachieveathoroughandcoherentunderstandingofadaptivespeciation.
Keywords:
Speciationmodels.Prezygoticisolation.Postzygoticisolation.Reinforcement.Disruptiveselection.Evolutionarybranching.Competitivespeciation.Sexualselection.Fisherianrunawayprocess.Good-genesmodels.Condition-dependentornament
Introduction:
Recently,thescientificworldcelebratedthe150thanniversaryofthereleaseofCharlesDarwin'sseminalbookOntheOriginofSpeciesbyNaturalSelection.Darwin'sideas(Darwin1859;Darwin1871)onnaturalandsexualselectionhaveinspiredgenerationsofbiologists,andwehavenowafairlygoodcomprehensionofhowselectionactswithinpopulationsandhowpopulationsaretransformedundertheinfluenceofselectionpressures.Itisimportanttorealise,however,thatmuchofourunderstandingofselection-inducedchangesrelatestotheprocessofanagenesis,thegradualevolutionofwholepopulations.Asimilarunderstandingoftheroleofselectionincladogenesis,thesplittingofspeciesintoreproductivelyisolatedunits,islargelylacking.Despiteofitstitle,theOrigindidactuallynotcontributemuchtoresolvingthequestionwhetherand
howspeciationisdrivenbynaturalselection.Asoundunderstandingofspeciationisofkeyimportanceforevolutionarytheory,sincethebirthofnewspeciesisthecruciallinkbetweenmicro-evolution(thatmainlyoccursatorbelowthespecieslevel)andmacro-evolutionaryprocesseslikeadaptiveradiationsthatlargelyoccurabovethespecieslevel.Ifspeciationtendstobeadaptive,thatis,drivenbydirectionalforceslikenaturalorsexualselection,thenone
couldhopeforachievinganoverarchingadaptivetheoryincludingbothmicro-andmacro-evolution.
Darwin(Origin,chapter4)envisagedspeciationastheresultoftwoprocesses:
selectionfordiversificationallowingtheexploitationofpreviouslyunusedopportunities,andtheextinctionofintermediateformsasaconsequenceofseverecompetitionamongtheseforms.Hence,accordingtoDarwin,selectionplaysamajorroleinthespeciationprocess.Infact,hisviewcomesclosetomodernideasoncompetitivespeciationtobediscussedbelow.However,Darwin'sverbalargumentsareoftenvagueandnotalwaysconvincing,partlybecauseofhispre-Mendelianideasoninheritance.Itispartlyforthisreasonthatthefoundingfathersofthe‘ModernSynthesis’largelydiscardedDarwin'sviewonspeciation(MayrandProvine1998),givingnonselectivefactorslikegeographicisolationamuchmoreprominentrolethanselection.
EversinceDarwin,theoreticalargumentshaveplayedanimportantroleindebatesonthecausesofspeciation.Inthesecondhalfofthe20thcentury,morethan100mathematicalmodelshavebeendevelopedtostudytheroleofselectioninspeciationwithgeneflow(reviewedinKirkpatrickandRavigné2002).Althoughmanyofthesemodelsdemonstratethatselection-drivenspeciationispossibleinprinciple,theytypicallyleadtotheconclusionthatselection-drivenspeciationwillonlyoccurunderhighlyspecificconditionsorforratherextremeparametercombinations(Felsenstein1981).Accordingly,speciationmodelsseemedtosuggestthatadaptivespeciationisarareandunlikelyphenomenon.Thisconclusionischallengedbytworecentdevelopmentsinspeciationtheory,whichseemtosuggestthatnaturalandsexualselectioncanbemorepowerfulinthecreationofnewspeciesthanthetraditionalmodelsseemtosuggest.First,avarietyofecologicalspeciationmodelshasbeendeveloped(Dieckmannetal.2004)thatshowthatDarwin'sintuitivenotionofcompetitivespeciationcanbegivenatheoreticalunderpinning.Thesemodelsarebasedonadynamicviewofnaturalselection,allowingselectiontoswitchfromstabilisingtodisruptiveinthesamecoherentframework.TherealisationthatDarwinianfitnessishighlycontextdependentanddynamic,andthatinadiversityofsettings,naturalselectioncandriveapopulationtowardaregimeofongoingdisruptiveselection,makesselection-drivenspeciationmoreplausiblethanintraditionalmodels.Second,varioussexualselectionmodelsofspeciation(Ritchie2007)givedisruptivesexualselectionaprominentplaceinthespeciationprocess.Severalstudies(e.g.,TurnerandBurrows1995;Higashietal.1999)demonstratethat,underspecificcircumstances,sexualselectionmayleadtothedivergenceoffemalepreferenceswithinasinglepopulation,eventuallyleadingtoreproductiveisolation.
Bothdevelopmentshaveinitiatedafiercedebateinthescientificliterature.Modelsofspeciationdrivenbydisruptiveselectionareinherentlycomplexandthereforehavetomakemanysimplifyingassumptions.Thequestionthereforeariseswhethertheresultsofthesemodelsaregeneralandrepresentativeforreal-worldsystems,orwhetherinstead,theymainlyreflectmodellingdetailsorthechoiceofparametersandinitialconditions.Incaseofecologicalspeciationmodels,theanalysisisoftenbasedonconceptsofadaptivedynamicstheory,whichhavebeenheavilycriticised(e.g.,WaxmanandGavrilets2005)anddefended(e.g.,DoebeliandDieckmann2005).Therepresentativenessofsimulationmodelsofecologicalspeciationhavebeenquestioned(e.g.,Gavrilets2004;butseeDoebeliandDieckmann2005)becauseoftheirassumptionsonthegeneticarchitectureoftraits,theirchoiceofparameterslikemutationrateorpopulationsize,andtheirassumptionsunderlyingtheevolutionofassortativemating(Matessietal.2001).Likewise,modelsofspeciationthroughdisruptivesexualselectionhavebeencriticised(e.g.,VanDoornandWeissing2001;ArnegardandKondrashov2004;VanDoornetal.2004)becauseoftheirhighlyspecialinitialconditionsandthelackofstabilityoftheincipientspeciesinthefaceofecologicalcompetition.Fornon-specialists(andnotonlyforthem!
),itisincreasinglydifficulttojudgethescopeandvalidityoftheargumentsandcounterargumentsinthisdebate.Thisispartlyaconsequenceofthehighdegreeoftechnicalsophisticationrequiredforsettingupandanalysingadaptivespeciationmodels.Moreover,proponentsandopponentstendtobasetheirviewsonmodelvariantsthatdiffertosuchanextentintheirassumptionsthatthemodeloutcomesarenotdirectlycomparable.
Insituationslikethese,itisoftenimpossibletosaythatonemodelvariantis“inherently”betterthananalternativeone.Selection-drivenspeciationresultsfromtheintricateinterplayofprocessesatthephenotypiclevel(wherenaturalandsexualselectionareoperating)andatthegeneticlevel(where,forexample,linkagedisequilibriahavetoevolvebetweenecologicalandmatingcharacters),andmodelsfocusingsimultaneouslyonbothlevelstendtobeintractable.Themoretraditionalspeciationmodelstendtohavetheirfocusongeneticprocessesandareoftenquitesophisticatedinthisrespect.Onthedownside,theyoftenmakesimplisticassumptionsonselectionandmating,whichcannoteasilybegivenamechanisticinterpretationandwhichtypicallylackapopulationdynamicalunderpinning.Incontrast,theadaptivedynamicsschooltendstoderivefitnessfromfirstprinciples;fitness“emerges”frommechanisticandpopulationdynamicalconsiderations(Metz2008).Onthedownside,theassumptionsontheunderlyinggeneticsareoftensimplisticandunrealistic.Itisimportanttorealisethatbothapproacheshavetheirvirtuesandtheirshortcomings;andthateachapproachshedslightondifferentaspectsoftheprocessofspeciation.Althoughthediversityofmodelsandmodeloutcomesmaylookconfusing,apluralisticapproachmayactuallybethebestresearchstrategyforachievingrobustinsights.Speciationtheoryistheprototypeexampleofaresearchfieldwherescientifictruthcanonlybeapproachedt