The Missing Response to Selection in the Wild

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The Missing Response to Selection in the Wild

Benoît Pujol, Simon Blanchet, Anne Charmantier, Etienne Danchin, Benoit Facon, Pascal Marrot, Fabrice Roux, Ivan Scotti, Céline Teplitsky, Caroline

Thomson, et al.

To cite this version:

Benoît Pujol, Simon Blanchet, Anne Charmantier, Etienne Danchin, Benoit Facon, et al.. The Missing Response to Selection in the Wild. Trends in Ecology and Evolution, Elsevier, 2018, 33 (5), pp.337-346.

�10.1016/j.tree.2018.02.007�. �hal-02161757�

Opinion

The Missing Response to Selection in the Wild

Benoit Pujol,

*

Simon Blanchet,

Anne Charmantier,

Etienne Danchin,

Benoit Facon,

Pascal Marrot,

Fabrice Roux,

Ivan Scotti,

Céline Teplitsky,

Caroline E. Thomson,

and Isabel Winney

Although there are many examples of contemporary directional selection, evidenceforresponsestoselectionthatmatchpredictionsareoftenmissing inquantitativegeneticstudiesofwildpopulations.Thisisdespitethepresence ofgeneticvariationandselectionpressures–theoreticalprerequisitesforthe responsetoselection.Thisconundrumcanbeexplainedbystatisticalissues withaccurateparameterestimation,andbybiologicalmechanismsthatinter- ferewiththeresponsetoselection.Thesebiologicalmechanismscanacceler- ate or constrain this response. These mechanisms are generally studied independently but might act simultaneously. We therefore integrated these mechanismstoexplore theirpotentialcombinedeffect.Thishasimplications for explaining the apparent evolutionary stasis of wild populations and the conservationofwildlife.

OurAbilitytoPredicttheResponsetoSelectionintheWildIsLimited Evidenceforcontemporarymicroevolutionbynaturalselectionhasrepeatedlybeenfound in both plant and animal populations [1]. However,responses toselection often do not matchquantitativegeneticexpectationsinlong-termsurveysofwildpopulations(hereafter referredtoassurveyedpopulations)[2],evenwith10–70yearsofphenotypicandpedigree data[3].Alack ofobserved responsetoselection('evolutionarystasis')appearstobethe norm rather than the exception in these studies [4,5]. This is puzzling because the response to selection was often missing, even though there was evidence for genetic variation and selection pressures on a trait – theoretical prerequisites for evolution by naturalselection.These findings reveal aconundrum inwhich the general expectationof an absenceof response toselectionderived fromstudies ofthese surveyedpopulations conflictswiththeexpectationofthepresenceofaresponsebasedonevidencefromother types of studies.

Wefirstsummarizestatisticalexplanationsforthisconundrum,namelythatthemeasuresof selectionandquantitative geneticparametersareimprecise. Inour opinion, thestatistical issuesthatwehighlightbelowshouldbetakenintoaccountmoreofteninstudiesofsurveyed populations.Ourfocusisonissuesthatare mostrelevanttoa mixedmodelingapproach becausethisisthemostwidelyusedmethodforestimatingquantitativegeneticparameters [e.g., additive genetic(co)variance] in surveyed populations. We then briefly discuss the alternative, but not mutually exclusive, role of biological explanations in explaining this conundrum. Biological mechanisms have the potential to impede selection and thereby avoid the erosion of genetic variability by selection. We also introduce mechanisms that weargue needtobetakeninto accountinsurveyedpopulations.

Highlights

Recentdiscoveriesattheintersection ofquantitativegeneticsandevolution- aryecologyarechallengingourviews onthepotentialofwildpopulationsto respondtoselection.

Multiple biological mechanisms can disconnectgeneticvariationfromthe responsetoselectioninthewild.We highlightareasforfutureresearch.

Weprovideanintegrativeframework thatcanbeusedtoqualitativelyassess the combined influence of these mechanisms on the response to selection.

1LaboratoireÉvolution&Diversité Biologique(EDBUMR5174), UniversitéFédéraledeToulouseMidi- Pyrénées,CNRS,IRD,UPS,31062 Toulouse,France

2Stationd’EcologieThéorique Expérimentale(SETE),CNRSUMR 5321,UniversitéPaulSabatier,09200 Moulis,France

3Centred’EcologieFonctionnelleet Evolutive(CEFE),CNRSUMR5175, 34293Montpellier,France

4DépartementdesSciences Biologiques,UniversitéduQuébecà Montréal,CP888SuccursaleCentre- Ville,H3P3P8QC,Canada

5UMRPeuplementsVégétauxet BioagresseursenMilieuTropical (PVBMT),InstitutNationaldela RechercheAgronomique(INRA),Saint Pierre,Réunion,France

6LaboratoiredesInteractionsPlantes–

Microorganismes(LIPM),INRA, CNRS,UniversitédeToulouse,31326 Castanet-Tolosan,France

7INRAUnitédeRecherche0629 EcologiedesForêts

Méditerranéennes,84914Avignon,

TrendsinEcology&Evolution,May2018,Vol.33,No.5 https://doi.org/10.1016/j.tree.2018.02.007 337

©2018TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Althoughsomemechanismslimittheamountofheritablevariationthatselectioncanactupon overshorttime-scales,othermechanismspromotetheresponsetoselection[6].Anissuewith thebiologicalexplanationsisthatthesemechanismshavegenerallybeenstudiedseparately.

Asaresult,theircumulativeandinteractiveeffectsremainunexplored.Wequalitativelycom- binedtheeffectsofseveralmechanismsinanimaginarypopulationofinterestcharacterizedby three‘known'mechanismstoillustratehowtopredictacorrectedbaselineexpectationforthe responsetoselection.Wealsodiscussthat,tosomeextent,thesumofthequalitativeeffectsof allthemechanismsthatwereportbelowcorroboratesanexpectationofevolutionarystasisin surveyedpopulations.Weconcludethat,althoughitdoesnotmakethestatisticalexplanation lessplausible,thebiologicalexplanationforevolutionarystasisissupportedbyourintegrative approach.Theseexplanationsandtheintegrativeframeworkthatwepresentherecanimprove predictive scenarios of adaptive evolution in the wild [7], with implications for biological conservation,climatechangemitigation,andthemanagementofgeneticresourcesinagron- omy(Box1).

TheStatisticalExplanations

PredictingtheResponsetoSelection,inTheory

Theadditivegeneticvariance(V_A)oftraitsiscentraltoquantitativegeneticstudiesofsurveyed populationsbecauseV_Aisusedas apredictoroftheevolutionarypotentialfortraitchange under directional selection. From V_A, we derive other parameters for comparing genetic variabilities [8]. Evolvability, for example, can be estimated by the coefficient of variation

(CV_A¼ ffiffiffiffiffiffi

V_A

p =z)toevaluatethemagnitudeoftheexpecteddirectionalresponsetoselection.

Narrow-senseheritability(h²=VA/VP,whereVPisthephenotypicvariance)isalsofrequently used, and evaluates the potential of a population to respond to selection. In theory, the univariateandmultivariatebreederequationspredicttheexpectedchangeinmeantraitvalue (s) as a result of selection (Dz). In the univariate case, this change is proportionalto trait

France

8MuséumNationald’Histoire Naturelle,CNRSUMR7204Centre d’ÉcologieetdesSciencesdela Conservation(CESCO),75005Paris, France

9GroupementdeRecherchede l’InstitutEcologieetEnvironnement 6448,GénétiqueQuantitativedansles PopulationsNaturelles(GQPN),c/o EDB,31062Toulouse,France

@Twitter:@BenoitPujol

*Correspondence:

[email protected](B.Pujol).

Box1.ApplicationsofMeasuringGeneticVariationinTraits MitigatingtheImpactofClimateChange

Climatechange can increaseecophysiologicaldemands on organisms.Rising mean temperatures,seasonality changes,anddroughteventsleavemanyorganismswithfewoptions:migrate,adapt,ordie.Theabilityofnatural populationstorespondtoselectionoftendependsonthosegeneticvariantsthatcancopewiththechanges[45],which givesthepotentialforrescueinparticularspecies.However,whenaresponsetoclimatechangeisobserved,this responsecanalsobeadaptiveplasticity[46].Uncoveringwhichmechanismscontributetoadaptivechanges[35]can informpoliciesthataimtomitigatethenegativeimpactsofclimatechange[47].

IntraspecificBiodiversityConservation

Biodiversityisdecliningbecauseofanthropicenvironmentalimpactsthatthreatentheexistenceofspeciesandthe ecosystemservicestheyprovide.Thereisdebateoverthecriteriafordeterminingwhichpopulationsorspecieswill benefitfromprotection[48]. Conservationagencies have establishedprioritieson the basis oftaxonomicand intraspecificgeneticdiversity[49].However,wearemissingthecompletelinkbetweenintraspecificgeneticdiversity andthelong-termabilityofnaturalpopulationstopersist[50].Thebiologicalmechanismsdiscussedinthisrevieware likelytoaffectintraspecificbiodiversityandtheevolutionaryresponsetoselectionofthreatenedwildpopulations.

ManagingGeneticResourcesinAgronomy

Inparallelwiththethreatsposedtoglobalfoodsecuritybyclimatechange[51],thereisaneedforincreasedagronomic yieldasaresultofhumanpopulationgrowthandchangesinsocietalpractices[52].Thecurrentratesofgenetic improvementinyielddonotmeetdemands[53].Thebiologicalmechanismssynthesizedinthisreviewcancontributeto thisissue,butmightalsobeusedtoalleviateitinthefuture.Globalfoodsecuritycanbeimprovedbyintegratingthese mechanismstomonitorandimprovecropyield.

338

heritability (h²)and the strengthof selection(or selection differential,S),i.e., Dz¼h²S [9].

Theseapproacheshavebeen successfullyapplied inplant andanimal breeding.However, preciselymeasuringV_Aanditsderivedstatistics,andmeasuringselection,ischallenging,as detailedbelow.

OversimplifyingGeneticandEnvironmentalEffectsMightBiasPredictions

Quantitativegeneticstudiesinsurveyedpopulationsoftenassumeanoversimplifiedviewofthe geneticbasisoftraits[10].Non-additivesourcesofgeneticvariation(e.g.,epistasis[11]and dominance[12])arerarelyaccountedfor,andcan beconfoundedwithVA,whichleadsto inflatedestimates.Environmentalcausesofphenotypicsimilaritybetweenrelatedindividuals have similareffects, butthey are morefrequentlyapproximated.This isgenerally doneby includingenvironmentalfactors[13]orindirectgeneticeffects(e.g.,maternaleffects[14])inthe mixedmodel.FailingtoaccountfortheseeffectscanbiasestimatesofVAandthereforethe predictionoftheresponsetoselection[15].

OwingtoPrecisionIssueswithStatisticalEstimates,QualitativePredictionsMightBeMore Realistic

Theprecision ofquantitativegeneticandselectionestimatesarereducedbylowstatistical power.Forexample,V_A estimatesoftenhave largeconfidenceintervals[7].Consequently, theseapproachesprovideanapproximatemagnitudeforthegeneticbasisoftraits(e.g.,small, medium,andlargeh²),andcautionmustthereforebetakenwithquantitativepredictionsor comparisons.Thesamecautionmustbetakenwhenmeasuringselection.Inaddition,skewed phenotypicdistributionscangeneratefalseestimatesofdirectionalselection[16]becausethe estimationofselectiongradientsassumesnormality.Nevertheless,ouropinionisthatdiscrim- inatingbetweenevolutionaryscenariosonthebasisofqualitativedifferencesremainspossible (e.g.,lowvshighh²)providedthatconfidenceintervalsarediscussedandpoweranalysesare conducted.

ExtrapolatingPredictionsCanBeMisleadingasaResultofCovaryingFactors

ExtrapolatingfindingsbasedonV_Aandselectiontodifferentcontexts(e.g.,multiplepopula- tions,years,similarenvironments)isunreliable[7].Thisisbecausetheseparametersarenot independentfromcovaryingfactorssuchasenvironmentalconditionsandtraitmeans[8].They alsovarywiththemethodbeingused(e.g.,sibshipsimilarityvsanimalmodelsforV_A).Estimates arethereforeassociatedwithauniquesetofconditionsandcannotbegeneralizedtoother populations. Comparisons between multiple populations can still be achievedbut require pedigreeconnectionsto quantify theeffectofsharedgenes indifferentenvironments[17], orcontrolledconditionstohomogenizeenvironmentaleffects[18].

TheProblemofAssigningCausalityBetweenSelectionandGeneticChange

Anotherlimittoevaluatingtheexpectedresponsetoselectionbyusingh²istherarelyverified assumption that selection acts on the underlying genetic variation of traits [19,20]. Any environmentalsource ofcovariancebetweentraitandfitnessviolates thisassumption[20], causing biased predictions [19]. An alternative method which relaxes the assumption of causationistheRobertson–Priceequation,alsoknownasthesecondarytheoremofnatural selection (STS[19]), Dz¼sAðw;zÞ, where phenotypic change Dz is equal to the additive geneticcovariancebetweenthetrait(z)andrelativefitness(w).Althoughtheoreticallycorrect, itsapplicationisneverthelesssubjecttotwolimitations.First,examplesofgeneticvariancefor fitnessarerare(butsee[21]).Second,theSTSmightnotalwaysquantifyachangecausedby selection[19].UsingtheSTStoestimatephenotypicchangecausedbyselectionismisleading becausethechangeinatraitofinterestthatisnotunderselectioncanbedrivenbyitsgenetic

TrendsinEcology&Evolution,May2018,Vol.33,No.5 339

correlationwith any unmeasured traitunder selection. This will causegenetic covariance between measured traits and fitness [19]. A possible solution is to adopt a multivariate approachto selection (genotypicselectiongradient[21]).Such anapproach mightlead to amoreaccurateprediction ofevolutionarychangebyselectiononphenotypictraits.

Ourinterpretationofevolutionaryprocessesandbiologicalmechanismsisbasedonstatistical measures(e.g.,VA).Thelimitationsofthesemeasuresimplythatitmightbestatisticalfailures, ratherthanbiologicalmechanisms,thatcauseadiscrepancybetweenpredictionsandobser- vationsofmicroevolutionarychange.However,qualitativepredictionsforevolutionaryscenar- ios are still possible. The conclusion that there is a missing response to selection might thereforebemisleadingiftheexpectedresponsetoselectionismisestimated.

TheBiologicalExplanations

TheMechanismsWeKnow,andtheMechanismsWeDoNotKnow

Thehypothesisthatbiologicalmechanismsmightberesponsibleforthemissingresponseto selectioninsurveyedpopulationsiswidelyacknowledged[2].Manybiologicalmechanisms, suchasphenotypicplasticity,geneticcorrelations,indirectgeneticeffects,andage-specific responses,arewellknowntointerferewiththeconnectionbetweengeneticvariationandthe response to selection, but are not always accounted for (Box 2). In addition, fluctuating selectionaffectsthespatialandtemporalscaleatwhichwedetectselection(Box2).Figure1 graphicallydepictstheimpactofeachofthesemechanismsontheresponsetoselectionthat waspredictedfromthebreeder’sequation(R,representedonthehorizontalaxis).Thevertical axis depicts the departure from the baseline expectation that VA will decrease following selection. For example, inthe case of negative genetic correlations between traits under positive selection, the response to selection is expected to be constrained, and genetic variationmaintained (Figure1Bii).We presentbelowothermechanismsto incorporateinto thelistofbiologicalexplanations.

DemographyandConnectivityShapethePotentialofPopulationstoRespondtoSelection PopulationdemographycanaffectV_Aandselection,butthisisneglectedinmostquantitative geneticstudiesofsurveyedpopulations.Forinstance,asharpdecreaseinpopulationsize(e.g., populationfoundingeventorcollapse)reducesgeneticdiversity(geneticbottleneck[22]),V_A, andtheresponsetoselection(Figure2A)[23,24].Conversely,geneticconnectivitybetween populationswithdifferentadaptiveoptimacanlimitlocaladaptationbutincreaseorrestore geneticvariabilityandadaptivepotential[25,26].Inaddition,anegativecorrelationisexpected betweenthepopulationgrowthrate andthevariationinrelative fitness(theopportunityfor selection) [27]. Thus, declining populations are expected to have a higheropportunity for selection,andmightthereforeexperiencestrongerselection[28].Althoughtherehavebeen someempiricalstudies ontheeffects ofdemography andconnectivity,theseeffects have mostlybeenexploredthroughtheoreticalwork.Theirapplicabilityandprevalenceinthewild remaintobeaddressed.

TheUnknownImpactofCoevolutiononEvolutionaryPredictions

Interactingspecies that exert reciprocal selectivepressures upon one another are widely documented in host–pathogen, predator–prey, and mutualisticinteractions[29].However, coevolutionislargelyignoredinstudiesofsurveyedpopulations(butsee[30,31]).Wearguethat neglectingtheseaspectscanleadtothemisestimationofV_Aandtheresponsetoselection (Figure2B).Theclassicillustrationofthisisthepromotion ofgenetic variationinvertebrate majorhistocompatibilitygenesthroughcoevolutionwithpathogens[32].Inaddition,pathogens can maintaingenetic variation inother traits ofhost species [33]. However, thesestudies 340

generallyestimateparametersinonlyoneoftheinteractingspecies,whileafulldemonstration ofcoevolutionrequiresthattheseareshowninbothpartnerspecies[33].Suchsimultaneous estimatesremainvirtuallyabsent.Fillingthisgapshouldconfirmpredictionsthathost–patho- gencoevolutionpromotesV_A[34].Takingintoaccountcoevolutionwouldimprovethedetec- tionofselectionpressuresandresponsesthatotherwisewouldnothavebeendetected,or wouldhavebeenoverestimated.

ThePotentialSignificanceofNongeneticInheritance

Whereadaptivephenotypicchangesweredetectedinsurveyedpopulations,onlyonethirdof thesewereassociatedwithgeneticchangeinresponsetoselection[35].Thisraisesquestions aboutthemechanismsunderlyingtheresponsetoselection,inparticularwhetherthereisa contributionofnongeneticinheritance.Theorypredictsthatinheritednongeneticvariationcan respond to natural selection [36,37] (Figure 2C). Nongenetic inheritance might therefore accountforamissingfractionofthegeneticresponsetoselectioninthewild[39,40].Equally,

Box2.WidelyAcknowledgedBiologicalMechanisms PhenotypicPlasticity

Phenotypicchanges inwildpopulations oftenresultfromplasticityratherthanfrommicroevolution [5,46].This shortcuttingofselectioncanresultingeneticvariationbeingmaintained.Whenplasticityvariesamongthegenotypes (genotype-by-environmentinteractions)underselection[54],themagnitudeand/orthedirectionofselectioncanbe alteredandlesspredictable[55].Geneticassimilation,wherebyphenotypicplasticityislostandthetraitbecomes canalizedbygeneticvariation[56],isaparticularcaseofresponsetoselection[57],althoughitsprevalenceinwild populationsremainsunclear.

GeneticCorrelationsamongTraits

Traitsthataregeneticallycorrelateddonotevolveindependently[58,59].Whenthiscorrelationisantagonistictothe directionofselection,theresponsetoselectionisconstrained[60]becauseachangeinonetraitreducesfitnessthrough theeffectontheothertrait.Consequently,geneticvariationcanbemaintained.Conversely,whenselectionandgenetic correlationsarealigned,thisfavorstheresponsetoselection[6],anddepletesgeneticvariation,comparedtobaseline expectations.Globally,geneticcorrelationswerefoundtohavebotheffectsonselection[61].

IndirectGeneticEffects(IGEs)

IGEsarisewhenthephenotypeofagivenindividualisaffectedbythetransmissibletraitsofotherswithwhomitinteracts [62],whichcaninfluencetheresponsetoselection[63].Thisisclearlydemonstratedbyparentaleffects[64,65].

Furthermore,antagonisticselectionbetweenparentalandoffspringtraitscouldconstraintheresponsetoselection[66].

Manystudiesneglectparentaleffects,potentiallybiasingheritabilityestimatesandbaselineexpectations[67].

Age-SpecificResponses

Quantitativegeneticevidenceforsenescence,usuallydefinedasthedecreaseofsurvivalandreproductiveprospects withage,iscommoninwildanimalpopulations[68],butisfarfromubiquitousinplants[69].Thisage-specificdeclinein selectionoftenresultsinhigherheritablevariationinolderageclasses[70].Agestructuresofnaturalpopulationsare rarelyaccountedforinquantitativegeneticstudies[71],andthiscanmisleadinglyaffectthepredictorsofevolutionary potential.

FluctuatingSelection

Fluctuationsinselectionstrengthand/ordirectionexistovershortspatialandtimescales[72,73],buttheirevolutionary significanceremainsuncertaininnature[74].Strongfluctuationsoccurringfasterthantheproductionofvariationcan reducegeneticvariationmorethanexpected,althoughintermediateslowfluctuationsmaintainhighergeneticvariation.

Neglectingfluctuationscanleadtoerroneousestimatesofthestrengthanddirectionofselection,particularlyifselection changessignatunmeasuredtimesand/orlocations.

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nongenetic inheritance can lead to inflated estimates of h²,contributing to the mismatch betweenthepredictedandobservedphenotypicresponsetoselection.Apartfromparental environmental effects, nongenetic components of heritability cannot yet be estimated in surveyedpopulations.Nevertheless,twostudiesdisentangledgeneticandnongeneticcom- ponentsofphenotypicsimilarity[41,42],whichisanimportantfirststep[43].Thereisaneedto (A) Phenotypic

plas city (B) Gene c

correla ons (C) Indirect

gene c effects (E) Fluctua ng selec on

(D) Age

(i) (i)

(i)

(ii)

(ii)

(iii)

(iv) (ii)

(iii) R

R R R R

R R

R R

R

R

V_A V_A

V_A

V_A

V_A

VA

VA

V_A V_A

V_A

VA

Figure1.DeparturefromBaselineEvolutionaryExpectations:WidelyAcknowledgedMechanisms.Quadrant plotsillustratetheeffectofwidelyacknowledgedmechanismsontheresponsetoselection(R)andthechangeinadditive geneticvariation(VA)relativetobaselinepredictions.Mechanismsincreasingtheresponsetoselectionlietotherightofthe yaxis,andthosedecreasingitlietotheleft.Mechanismscausingthemaintenanceofadditivegeneticvariationlieabove thexaxis,thoseerodingitliebelow.Whereexpectationsareclosetobaselinepredictions,theeffectremainscentered aroundtheaxis.Thesemechanismsare(A)phenotypicplasticity,(B)geneticcorrelations,(C)indirectgeneticeffects (maternalgeneticeffect),(D)ageeffects,whereoldageclassesareoftenassociatedwithincreasedadditivegenetic variation,and(E)fluctuatingselection.Phenotypicplasticity(A)wassplitinto(i)theeffectofplasticityitself,(ii)theeffectof thecanalizationofplastictraitvariationthatbecomesconstitutivelyexpressed,asinthecaseofgeneticassimilation,and (iii)genotype-by-environmentinteractions.Geneticcorrelations(B)weresplitinto(i)theeffectofgeneticcorrelations alignedwiththedirectionofselection,and(ii)theeffectofgeneticcorrelationsthatareantagonisticwiththedirectionof selection.Fluctuatingselection(E)wassplitinto(i)theeffectofalow-frequencyfluctuationwithsignchanges,(ii)effectof fastfrequencyfluctuationwithsignchanges,(iii)low-amplitudefluctuationwithsignchanges,and(iv)low-amplitude fluctuationwithconsistentsign.

Demography CoevoluƟon NongeneƟc inheritance

(B) (C) (A)

V_A V_A V_A

R R R

Figure2.DeparturefromBaselineEvolutionaryExpectations:NewMechanisms.Inthisfigurewepresentin quadrantplotstheeffectofmechanismsthatinouropinionshouldalsobeconsideredtoaffecttheresponsetoselection (R)andthechangeinadditivegeneticvariation(VA)relativetobaselinepredictions.Mechanismsincreasingtheresponseto selectionlietotherightoftheyaxis,andthosedecreasingitlietotheleft.Mechanismscausingthemaintenanceofadditive geneticvariationlieabovethexaxis,thoseerodingitliebelow.Whereexpectationsareclosetobaselinepredictions,the effectremainscenteredaroundtheaxis.Themechanismsoutlinedhereare(A)demography;weshowheretheeffectof foundingevents,orlong-termsmallpopulationsizeassociatedwithgeneticdrift,(B)coevolution,and(C)nongenetic inheritance.

342

improveboththeoreticalandempiricalunderstandingofnongeneticinheritance,particularlyto (i)assessthelong-termstabilityofnongeneticinheritancemechanisms,(ii)buildatheoretical frameworktakingintoaccounttheirkeyproperties,and(iii)testfortheirroleintheresponseto selection.

TowardsanIntegrativeViewofBiologicalMechanisms

Biological mechanisms acting in isolation have been found to influence the response to selection in surveyed populations [2,44],but an integrative perspective of their combined actionislacking.Asaresult,twoimportantquestionsremainunanswered.First,canwerefine ourexpectationsoftheresponsetoselectionifweidentifythebiologicalmechanismsactingina wildpopulationofinterest?Second,domostmechanismsconstraintheresponsetoselection andmaintainVA?Ifthemajorityofbiologicalmechanismsconstraintheresponsetoselection, thiswouldsupportabiologicalexplanationforevolutionarystasis.Untilthesequestionsare addressed,thestandingevolutionarypotentialofwildpopulationscannotbeproperlyevalu- ated.Wecanimproveourpredictivecapabilitiesbyintegratingpredictionsfromwell-studied mechanisms,butthere iscurrentlynoframeworkforassessingtheircombinedimpact.We buildhereaqualitativeframeworkasafirstversionofanintegrativetheoryoftheirimpactonthe evolutionarypotentialofwildpopulationstorespondtodirectionalselection.

HowtoRefineOurBaselineExpectationoftheResponsetoSelection

Thebasisofthisapproachtakesthepredictedresponsetoselection(R)fromthebreeder’s equation,andtheconsequentreductioninVAasabaselineexpectation.Figures1,2illustrate thedeviationfromthesebaselineexpectationscausedbyindividualmechanisms(indicatedby theshadedregions).Assuminganequalweightingofthesemechanisms,wecanqualitatively combinetheeffectsofindividualmechanismsthemostlikelyevolutionaryscenarioinagiven population.Itisthenpossibletoadjustbaselineexpectationsforaparticularpopulation.

Implementing this graphical tool should be possible in any population, and give testable predictionstorefine ourexpectationsofevolutionarychange.Figure3Aillustrateshowthe impactofthreemechanismscanbequalitativelycombinedforanimaginarypopulation.Inour example,animaginarypopulationisintroducedtoanewhabitat,leadingtoafoundingevent thatincreasesthelossofV_Aanddeceleratestheresponsetoselection(Figure2A).Inthisnew environment,differentgenotypeshavedifferentlevelsofplasticity,whichdoesnotaffectthe baselinepredictionsforV_A butcanleadto amoreuncertainpredictionofR(genotype-by- environmentinteractions;Figure1Aiii).Furthermore,twotraitsunderpositiveselectioninthis populationhaveanegativegeneticcorrelationthatisnotalignedwiththedirectionofselection, therebyconstrainingtheresponsetoselectionandmaintainingVA(Figure1Bii).Thus,com- bining thesemechanisms gives us the most likely evolutionary scenario in this imaginary population(illustratedbythedarkestsectoronthecombinedgraphinFigure3A):areduced responseto selectioncomparedtobaseline prediction,andachangeinVA thatislikelyto conformwiththebaselineprediction.Anemergentpropertyofthisframeworkisthatitcan identifywhendisparatespeciesandpopulationsareexpectedtorespondsimilarlytoselection owingtoparallelsintheeffectsofbiologicalmechanisms.

TakingStepsTowardsaGlobalUnderstanding

Thisintegrativeapproachcouldultimatelybeappliedtomanymechanisms,populations,and speciestorefinethepredictionsoftheresponsetoselectionandchangesingeneticvariation.

Figure3Billustratestheresultofanintegrationofallthemechanismsoutlinedhere.Thedarkest sector in the combined plot indicates a reduced responseto selection compared to our baselineexpectation,andthemaintenanceofaslightlyhigherthanexpectedlevelofgenetic

TrendsinEcology&Evolution,May2018,Vol.33,No.5 343

variation.Thisintegrativeperspectivethereforeappearstomatchthegeneralobservationof evolutionarystasis, thereby corroboratingthe biological explanation forstasis. However,a rangeofscenarios otherthan evolutionarystasisremainspossible,indicatedbythebroad shadingacrossFigure3B,althoughempiricalevidenceforthesescenariosisscarce.

Itisimportanttonotethatthestatisticalexplanationsarenotrefutedbythisapproach,andthe imprecisionofquantitativegeneticestimates thereforestill needs tobetakenintoaccount.Thereis alsothecaveatthatourlistofmechanismsisnotexhaustive,butothermechanismsmightbeof interest, such as sexual selection and those that are yet to be documented, and can be incorporatedintothisframework.Thefrequencywithwhichdifferentmechanismsoccurinnatural populationsremainsunclearbecausethatreportedinpublishedstudiesmightbeanartefactof researchmotivatedtofindexplanationsforevolutionarystasis.Thiscouldbeclarifiedbybroad- eningtherangeofstudysystems.Futureworkcouldintegrateadditionalmechanismsandweight allmechanismsbytheirfrequencyofoccurrenceandtherelativestrengthoftheireffects.

ConcludingRemarks

Thepast20yearsofquantitativegeneticstudiesinsurveyedpopulationshaveconfirmedthat geneticvariationfortraitsisnotalwayssynonymouswithevolutionarypotential,andthatthe expectedresponsetoselectionisoftenmissing.Althoughinitiallyparadoxical,multipleexplan- ationshavebeenfoundforthesefrequentcasesofstasis.Thewidelyacknowledgedstatistical explanationspointtotheimprecisionofempiricalmeasuresofquantitativegeneticvariationand selection as a likely explanation. However,biological mechanisms studied inisolation can causeamismatchbetweenthepredictedandobservedresponsetoselection.Theunified frameworkthatweproposeimpliesthatthecombinedactionofthesemechanismsislikelyto limittheresponsetoselectionofwildpopulations ingeneral.However,quantitativegenetic studies ofsurveyed populations are restrictedto a relatively smallnumberof cases.Their extensiontoothersystemsmightaddfurthermechanismstothisframeworkandcontributeto ourunderstandingofmicroevolution.

Combining mechanisms

in a given populaƟon Combining all mechanisms

(A) (B)

V _A V _A

R R

Figure3.AnIntegrativeFrameworkforPredictingMicroevolutionaryChange.Weshowherehowtointegrate multiplemechanismsintoourframework.Thequadrantplotsillustratetheeffectofmechanismsthataffecttheresponseto selection(R)andthechangeinadditivegeneticvariation(VA)relativetobaselinepredictions.Mechanismsincreasingthe responsetoselectionlietotherightoftheyaxis,andthosedecreasingitlietotheleft.Mechanismscausingthe maintenanceofadditivegeneticvariationlieabovethexaxis,thoseerodingitliebelow.Whereexpectationsarecloseto baselinepredictions,theeffectremainscenteredaroundtheaxis.Mechanismsarecombinedbysuperimposingthe quadrantplotsoftheireffects,whichrevealsadarkenedareathatcorrespondstothemostlikelypredictionsaboutthe responsetoselectionandchangesingeneticvariation,relativetobaselineexpectations.Plot(A)illustrateshowasampleof mechanismsknowntocharacterizeaparticularpopulationcanbeintegrated.Thisillustratespredictionsforanimaginary population,wherefoundingeffects,gene-by-environmentinteractions,andnegativegeneticcorrelationsbetweentraits underpositiveselectionarecombinedtogivepredictionsofreducedresponsetoselection,accompaniedbyrelatively negligiblechangesingeneticvariationcomparedtothebaselineexpectation.Plot(B)illustratesthecombinedeffectofall themechanismslistedinthemaintext.

OutstandingQuestions

Whatistherelativestrengthofimpact ofeachbiologicalmechanismaffecting theresponsetoselection?Weprovide aframeworkwhereequalweightingis given to each mechanism, but this mightnotalwaysbethecase.Inaddi- tion, these mechanismsmight have non-additiveinteractions.Comparing ourqualitativepredictionstowhatis observedwillinformusabouttherela- tiveweightingthequantitativeeffects ofthesemechanisms.

Whatisthebiologicalfoundationfor the observation that expected responsestoselectionaremissingin thewild?Thepredictionsfromisolated mechanismsaffectingtheresponseto selectioncoverarangeofevolutionary scenarios(responsetoselectionand changesingeneticvariation)thathave notbeenobservedinthewild.Whether thisisanartefactofcurrentresearchor reflectsbiologicalrealitywillbecome clearerwithanincreaseinthenumber of quantitative genetic studies in diversestudysystems.

Whymightsomespeciesorpopula- tions sharesimilar suitesofmecha- nisms?Essentially, are thereshared selectionsyndromesinthewild?Simi- larevolutionarychangescould bea resultofparallelsbetweenpopulations inthemechanismsinfluencinggenetic variationandtheresponsetoselec- tion.Usingtheintegrativeframework inmultiplepopulationswillrevealpat- terns across disparate species and populations.

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