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Review

Evaluating

Plasticity-First

Evolution

in

Nature:

Key

Criteria

and

Empirical

Approaches

Nicholas

A.

Levis

1,

*

and

David

W.

Pfennig

1

Many biologists are asking whether environmentally initiated phenotypic

change(i.e.,‘phenotypicplasticity’)precedes,andevenfacilitates,evolutionary

adaptation. However, this ‘plasticity-rst’ hypothesis remains controversial,

primarilybecausecomprehensivetestsfromnaturalpopulationsaregenerally

lacking.We brieydescribe theplasticity-rsthypothesis andpresent

much-neededkeycriteriatoallowtestsindiverse,naturalsystems.Furthermore,we

offeraframeworkforhowthesecriteriacanbeevaluatedanddiscussexamples

wheretheplasticity-firsthypothesis has been investigated in natural

popula-tions.Ourgoalistoprovideameansbywhichtheroleofplasticityinadaptive

evolutioncanbe assessed.

NeedforaPredictiveFramework

Amongtheenduringproblemsofevolutionarybiologyisexplaininghowcomplex,adaptivetraits originate[1,2].Althoughitiswidelyassumedthatnewtraitsarisesolelyfromgeneticfactors[3], manyresearchersareaskingwhetherenvironmentallyinitiatedphenotypicchange–inother wordsphenotypicplasticity(seeGlossary)–precedesandfacilitatesadaptation[4–12].

Thisalternativeroute,dubbedtheplasticity-firsthypothesis[4,13],restsontheobservation

thatphenotypicplasticityoftenproducesdevelopmentalvariantsthatcanenhancefitnessunder

stressfulconditions[4,5,14].Ifunderlyinggeneticvariationexistsinthetendencyormannerin whichindividualsproducesuchvariants(asisoftenthecase[15]),thenselectioncanrefinethe

traitfromaninitial,potentiallysuboptimalversionthroughquantitativegeneticchangesovertime; inotherwordsgeneticaccommodationoccurs[4].Furthermore,dependingonwhetheror notplasticityisfavored[16],thisselectioncanrespectivelypromoteeitherincreased environ-mental sensitivity –which maintains the trait as a polyphenism(sensu [17]) ordecreased environmentalsensitivity–whichcanresultintheconstitutiveexpressionofthetrait;inother wordsgeneticassimilation(sensu[18]).By‘jump-starting’phenotypicchangeinanadaptive direction[19],environmentallyinducedphenotypicchangeprecedes,andpromotes,the evo-lutionaryoriginsofacomplex,adaptivetrait(Figure1;Box1).

Wheninitiatedbyplasticity,refinementofadevelopmentalvariantintoanadaptivetrait(whether

novelornot)doesnotrequirenewgenes.Instead,environmentallyinducedphenotypicchange setsinmotionanevolutionarysequenceinwhichselectionpromotesadaptationbyactingon existinggeneticvariation(e.g.,[15,20–22]).Inessence,suchselectionrefinesatraitthrough

evolutionaryadjustmentsinboththeformandregulationoftraitexpression.Theoutcomeofthis processisanadaptivephenotypethat,relativetoitsinitialstate,hasbeenmodifiedbothinits

Trends

Phenotypic plasticity has long been

proposed to precede and possibly

facilitateadaptiveevolution.

This‘plasticity-firsthypothesis’ is

con-troversialbecauseskepticsarguethat

itlackscompellingevidencefrom

nat-uralpopulations.

A chief difficulty with demonstrating

plasticity-firstevolutioninnatural

popu-lationsisthat,onceatraithasevolved,

itsevolutioncannotbestudiedinsitu.

Togetaroundthisdifficulty,

research-erscanstudyextantlineagesthatact

asancestral-proxiestothelineage

pos-sessingthefocaltrait.

Usingsuchanapproach,keycriteriaof

the plasticity-first hypothesis can be

evaluated using a relatively simple

experimentaldesign.

Applyingthesecriteriatovarious

sys-tems,theplasticity-firsthypothesishas

some empirical support. However,

morestudiesareneededto

conclu-sivelydeterminethe roleof plasticity

inadaptiveevolution.

1DepartmentofBiology,CampusBox

3280,UniversityofNorthCarolina, ChapelHill,NC27599,USA

*Correspondence:

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morphologicalandphysiologicalattributesaswellasinitsenvironmentalsensitivity.Ofcourse, other evolutionary forces (e.g., genetic drift, mutation) could alter the degree of plasticity. However,theplasticity-firsthypothesisassumes thatanysuchchangeoccurredvia genetic

accommodation,which(bydefinition)isdrivenbyselection.

Althoughlabstudieshavedemonstratedthattheplasticity-firsthypothesiscanpromote

adap-tation(e.g.,[18,23–25]),andtherearesuggestivefieldstudies(e.g.,[26–30],reviewedin[31]), whetherplasticity,followedbygeneticaccommodation,hasactuallycontributedtotheevolution ofanycomplextraitinanynaturalpopulationiscontroversial[32–35].Partofthedifficultyisthat

thekeycriteriaoftheplasticity-firsthypothesishavenotbeenmadeclear.However,ifasstatedin

tworecentprominentreviews:‘whatremainstobedoneistogeneratecreativeapproachesto collectingempiricaldatafromnaturalpopulationstotestpredictions...’[11],andif‘thebestway toelevatetheprominenceofgenuinelyinterestingphenomenasuchasphenotypicplasticity...is tostrengthentheevidencefortheirimportance’[35],thenthesecriteriaandpredictionsmustbe madeclearandrigorouslytested.

Wedescribeherekeycriteriafortestingtheplasticity-firsthypothesis.Wealsopresentageneral

frameworkinwhichthesecriteriacouldbeevaluatedinnaturalpopulations,andwediscusscase

Glossary

Crypticgeneticvariation:genetic

variationthatnormallyhaslittleorno

effectonphenotypicvariationexcept

underatypicalconditions.

Geneticaccommodation:a

mechanismofevolutionwhereina

phenotype,generatedbyeithera

mutationorenvironmentalchange,is

refinedintoanadaptivephenotype

throughselectiondrivingquantitative

geneticchanges.Accommodation

canalsopromoteeitherincreasedor

decreasedenvironmentalsensitivityof

thefocalphenotype;when

environmentallyinducedphenotypes

loseenvironmentalsensitivity,they

undergo‘geneticassimilation’.

Geneticassimilation:anextreme

formof‘geneticaccommodation’ that

occurswhenselectioncauses

environmentallyinduced(i.e.,plastic)

phenotypestolosetheir

environmentalsensitivityover

evolutionarytime.

Noveltrait:broadly,anymajor

developmentalinnovation;sometimes

definedasabodypartthatisneither

homologoustoanybodypartinthe

ancestrallineagenorserially

homologoustoanyotherbodypart

ofthesameorganism;adifficult

concepttodefine.

Phenotypicaccommodation:the

maintenanceofanovel,inducedtrait

orphenotypethatisanautomatic

consequenceofmultidimensional

adaptivephysiological,morphological,

and/orbehavioralplasticityintheface

ofadevelopmentalchange.

Phenotypicplasticity:theabilityof

anorganismtoalteritsbehavior,

morphology,and/orphysiologyin

responsetochangesin

environmentalconditions;sometimes

usedsynonymouslywith

developmentalplasticity.

Plasticity-firsthypothesis:a

mechanismofadaptiveevolutionin

whichenvironmentalperturbation

leads,viaphenotypicplasticity,to

developmentalreorganization(via,e.

g.,alteredgeneexpression)and

uncovers‘crypticgeneticvariation’

for,andultimatelyproductionof,a

noveldevelopmentalvariant(i.e.,trait)

thatimmediatelyundergoes

‘phenotypicaccommodation’andis

subsequentlyrefinedthrough‘genetic

accommodation’ somedefinitions

includecasesinwhichmutation

initiatestraitorigin(notdiscussed

here;seeBox1).

(A)

(B) (C)

(E) (D)

Figure1.AnIdealizedRepresentationofHowPlasticity-FirstEvolutionLeadstoaNovel,Adaptive,Complex Trait.(A)Ageneticallyvariablepopulation(here,different-coloredtadpolesrepresentdifferentgenotypes)(B)experiencesa

novelenvironment(shading),whichimmediatelyinducesnoveldevelopmentalvariants(dashedlines).However,different

genotypesvaryinthemannerinwhichtheyrespond(orindeed,iftheyrespondatall).(C)Selectionactsonthisformerly

crypticgeneticvariation(revealedbythechangeinenvironment)bydisfavoringthosegenotypesthatproducephenotypes

thatarepoorlyadaptedinthenewenvironment(here,theround-bodiedphenotypeisfavored,whereasallothersare

disfavored,asindicatedbythe‘X’).(D)Thisselectionalsoleadstotheadaptiverefinementofthefavoredphenotype

(depictedherebytheenlargementofthebluetadpole).Iftheancestralphenotype(i.e.,narrow-bodiedtadpole)isstill

maintainedintheancestralenvironment(seeA),thentheresultisanovelpolyphenism.(E)However,selectionmightinstead

favorthelossofplasticity(i.e.,geneticassimilation),resultinginanovelphenotypethatisnowproducedconstitutively,even

whenthepopulationexperiencestheancestralenvironment(indicatedherebythelossofshadinganddashedlines).Note

thatobservationsfromnaturalsystemslikelywillnotbeasclear-cutastheprocessdescribedhere.Furthermore,although

wehaveshownhowaplasticity-firstprocesspromotesnovelty,thisprocesscouldalsoexplaintheevolutionoftraitsthatare

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Polyphenism:environmentally

inducedalternativephenotypes.

Reactionnorm:agraphical

representationofthesetof

phenotypesthatasinglegenotype

producesinresponsetosome

specificenvironmentalvariable(s);

individualsshowplasticityiftheir

reactionnormisnon-horizontal.

studiesthathaveutilizedthisframeworktofindsupportforthesecriteria.Ourgoalistoprovidea

roadmapfor testingthe plasticity-first hypothesisandtherebyclarify the roleofplasticity in

adaptiveevolution.

KeyCriteriaforthePlasticity-FirstHypothesisof AdaptiveEvolution

Beforeoutliningcriteriafordemonstratingplasticity-firstevolutioninnaturalpopulations,wenote

thatthemostcompellingevidenceforthisprocesswouldbetoactuallyobserveittakingplace. Indeed,plasticity-firstevolutioncouldpotentiallybeobservedinreal-timein:(i)casesinwhich

naturallyoccurringpopulationsexperiencerapidenvironmentalchange(e.g.,climatechangeor introduced species[26]), or(ii) resurrectionstudies;for example,usingseeds from datable sedimentasancestralcontraststomodern,derivedindividualsfromthesamepopulation.In bothcontexts,theancestralconditionwouldbeknown,andenvironmentalchangecanoccur swiftlyenoughtoobservean evolutionaryresponse.Notethatathird context,studyingthe plasticity-firsthypothesisinlabpopulations of rapidlyevolving organisms [36,37],wouldbe

worthwhilebutwouldnotclarifywhetherplasticityhascontributedtoadaptationinanynatural population[32–35].

Formostsystems,however,itislikelythatonlythefinalproductsofanyputativeplasticity-first

processwillbepresentinmodern-daypopulations.Insuchsituationsthechiefdifficultywith

demonstratingplasticity-firstevolutionisthat,onceatraithasevolved,itsevolutioncannotbe

studiedinsitu.Togetaroundthisdifficultyonecouldeitherstudylineages(i.e.,speciesand/or

populations)thatareancestral-proxiestothelineagepossessingthefocaltrait[5]or, alterna-tively,evaluatewhetherenvironmentallyinduceddifferenceswithintaxareflectadaptive(fixed)

differencesamongthesesame(orrelated)taxa[31].Oftheseapproaches,ancestral-derived comparisonsproducestrongerevidenceofgeneticaccommodation[31].Althoughsuch com-parisonsareonlyfeasibleinsystemswithwell-understoodnaturalhistoriesandreadily acces-sibleancestral-proxyandderivedlineages(Box2),wefocusonthisapproachinsuggestingfour keycriteriaoftheplasticity-firsthypothesis.

Importantly,validationofanyonecriterion,byitself,isinsufficienttoestablishthatplasticity-first

evolutionhasoccurred.Forinstance,manysystemsappeartosatisfycriterion1below–thata trait is present in ancestral-proxy lineages as an environmentally induced variant [13,31]. However, themere existenceof suchancestralplasticity isinsufficient to demonstrate that

thetraitevolvedviaaplasticity-firstprocess.Asnotedabove,severalevolutionarymechanisms Box 1. Evolutionary Potential of Environmentally Initiated Versus Mutationally Initiated Phenotypic Change

Stresses– suchasmutationorenvironmentalchange– cangeneratenoveldevelopmentalvariants[4,5].The

sub-sequentgeneticaccommodationofsuchvariantscanoccurwhethertheyareinducedbymutationorachangeinthe

environment[4],andthesetwomodesofinductionareofteninterchangeable[4,12,13].However,environmentally

triggerednoveltieslikelyhavefargreaterevolutionarypotentialthanmutationallyinducedones,foratleastthreereasons

[4].First,changesintheenvironmentoftenaffectmanyindividualssimultaneously,incontrasttoageneticmutation,

whichinitiallyaffectsonlyoneindividualanditsimmediatedescendants(also,thevastmajorityof mutationsare

deleterious[58,59]).Thiswidespreadimpactofenvironmentalchangeenablesanewlyinducedtraittobetestedamong

diversegenotypes, thereby providingfertilegroundforselectiontoactandincreasingthechances thatgenetic

accommodationwilloccur[4].Second,althoughthechancethataparticularmutationwilloccurisnotinfluenced

bywhetherornottheorganismisinanenvironmentinwhichthatmutationwillbeadvantageous–inotherwords,

adaptivelydirectedmutationdoesnotoccur[60]– thesituationisdifferentforenvironmentallytriggeredtraits.Suchtraits

arealwaysassociatedwithaparticularenvironment– theonethattriggeredit.Therefore,environmentallyinducedtraits

aremorelikelythanmutationallyinducednoveltiestoexperienceconsistentselectionanddirectionalmodification[4].This

allowsnewenvironmentstoimmediatelyproduceandselectamongnewphenotypesandrapidlyrefinetheirexpression

[5].Third,plasticitypromotesthestorageandreleaseofcrypticgeneticvariation–inotherwordsvariationthatis

expressedonlyunderatypicalconditions(e.g.,[41,45,46]).Thereleaseofsuchvariationultimatelymakesgenetic

accommodationpossible[9,44].Forthesereasons,environmentalinitiationmighthavegreaterevolutionarypotential

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canleadtothesubsequentchangeinthedegreeofplasticity,buttheplasticity-firsthypothesis

requiresthatselectionfavoredanysuchchanges.Thus,confirmationofseveral(ideally,allfour)

criteriaincreasessupportforthismodeofevolution.

Criteria1and2focusondetectingpre-existingplasticityanddevelopmentalreorganization (i.e., phenotypic accommodation), whereas criteria 3 and 4 focus on the subsequent refinement ofexpression and formof the focal phenotype (i.e., genetic accommodation).

Notethatwehaveomittedcriteriaspecificallydealingwithhowdevelopmentalreorganization

canproduceanovelphenotypeinancestral-proxylineagesbecausesuchreorganizationhas extensivesupport(reviewedin[4])andiswidelyaccepted.However,weexpectanychanges inthemeasuredtraitbetweenancestral-proxyandderivedlineagestobeaccompaniedby concurrentmechanisticchanges(e.g.,hormones,alternativesplicing,transcription factors, cis-regulatory elements, etc.) [4,9,38–40] underlying production and/or regulation of that trait.

Belowwelisteachcriterionfollowedbytherationalebehindit.Althougheachofthesecriteriahas beendiscussedpreviously(e.g.,[4,5,9,22,29]),theyhavenotbeencollectivelyassembled,and clearmethodsfortestingthemhavenotbeenprovidedbeforenow.

Criterion1.TheFocalTraitWillBeEnvironmentallyInducedinAncestral-ProxyLineages

Themostfundamentalcriterionoftheplasticity-firsthypothesisisthatthetraitofinterestshould

exhibitancestralplasticity.By‘ancestralplasticity’wemeanthatadevelopmentalvariant(or character state), similar to the derived (possibly fixed) trait, should be expressed among

individualsfromancestral-proxylineageswhentheseindividualsexperiencethederived envi-ronment; in other words the environmental conditions in which the focal trait is normally expressedinderivedlineages[4].Inaddition,ifthereisphylogeneticsupportthatataxonwith aninducibletraitresemblestheancestralcondition,and/orifthedevelopmentalmechanismsfor producingthetraitareconservedinrelatedspecieswherethetraitdoesnotregularlyoccur,then thiswouldsuggestthatthetraitstartedoutasanenvironmentallyinduceddevelopmentalvariant

[4].Itisimportanttonotethatthedevelopmentalvariantneednotbeexpressedtothesame degreeasisseeninderivedlineages.

Box2.ConsiderationsWhenChoosingaStudySystem

Asnoted,onlythefinalproductsofplasticity-firstevolutionmightstillexistformostsystems,makinginsituinvestigation

difficult.Onewaytocircumventthisdifficultyistouseotherlineages(i.e.,speciesorpopulations)asproxiesforthe

ancestralconditionandcomparethemtoderivedlineagesthatpossessthefocaltrait.Todoso,onemustknowthe

phylogeneticrelationshipsbetweenlineagesthatdifferintheformof,orpropensitytoproduce,aninducedphenotype.

Thisisimportantbecauseitisessentialtoknowwhichlineagescanrepresenttheancestralandderivedstates.However,

thismeansthatsomesystemsthatlackphylogeneticinformationmightnotbesuitableforevaluatingtheplasticity-first

hypothesisusingtheapproacheswehaveoutlinedhere.

Inaddition,ourcriteriadependonknowingtheenvironmentalstimulusthatmighthaveinitiallyledtoproductionofthetrait

aswellastheselectivepressuresleadingtoitsrefinementorchangeinfrequencyofexpressioninderivedlineages.

Withoutthisinformation,evaluatingtheplasticity-firsthypothesisisnotpossible.

Whileknowledgeofthephylogeneticrelationshipsandrelevantenvironmentalfactorsisrequired,othernon-essential

characteristicscouldimprovetheutilityofasysteminstudyingtheplasticity-firsthypothesis[61],including:

(i) Multiple,parallelderivedlineageswithvaryingdivergencetimesfromtheancestral-proxylineage.

(ii) Knowledgeoftheecologicalcircumstancesexperiencedby,andtheselectiveagentsimpingingon,both

ancestral-proxyandderivedlineages.

(iii) Aquantifiabletraitthatisreadilyinducedunderlaboratoryconditions.

(iv) Adequategenomicresourcesforinvestigationofmolecularunderpinnings.

(v) Otherfeaturesof‘typical’ modelorganisms(e.g.,fastgenerationtime,easytorearinlargenumbersinthelab,

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Criterion2.CrypticGeneticVariationWillBeUncoveredWhenAncestral-ProxyLineages

ExperiencetheDerivedEnvironment

Ifatraitonlyexistsasanenvironmentallyinducedvariant,andthereforeisinfrequently(ornever) exposedtoselection,thengeneticvariationshouldaccumulateintheresponseofthetraittoa novel environment (or in components that make up the trait) that can be revealed when environmentalconditionschange (Figure 1C).In a novelenvironment, thiscrypticgenetic variationwouldbeuncovered–manifestasanincreaseinheritabilityorgreaterphenotypic variation resultingfromperturbation of anevolutionary capacitor[30,41–43]–and actas a selectable substrate (Figure 1D) [4,9,44–46]. Subsequently, however, lineages inthe novel (derived)environmentshouldexperienceaselectivesweepandlosethisvariationasthetrait undergoes genetic accommodation [4,9,47]. Thus, once derived lineages have undergone genetic accommodation, theyshould exhibitreduced heritability and/orgenetic variation in thetraitofinterest.

Criterion3,TheFocalTraitWillExhibitEvidenceofHavingUndergoneanEvolutionary

ChangeinitsRegulation,Form,orBothinDerivedLineages

Thiscriterioncanbemanifestasachangeintheslopeorelevation(orboth)ofthereaction norm inderivedversus ancestral-proxy lineages. Because achange in sloperepresents a changeintheregulationofatraitandachangeinelevationindicatesachangeinitsform[30,48],

finding either in derived lineages would suggest genetic accommodation [4]. Furthermore, findingthatreactionnormsarefixedacrossdifferentenvironmentswouldsuggestthatthetrait

has beengenetically assimilated.Finally, changesin reactionnorms should bemirrored by changesinthemechanismsunderlyingthetrait(e.g.,hormones,alternativesplicing, transcrip-tionfactors,cis-regulatoryelements,etc.)[4,9,38–40].

Criterion4.TheFocalTraitWillExhibitEvidenceofHavingUndergoneAdaptiveRefinement

inDerivedLineages

Undertheplasticity-firsthypothesis,thefrequencythatatraitisexpressedwilldeterminethe

degree to which it is refined by selection [4]. Therefore, compared with individuals from

ancestral-proxylineages,individualsfromderivedlineagesshouldproducesuperiorversions ofthe trait when bothtypes of lineages experience environmentsthat inducethe trait. For example,derivedindividualsshouldproduceaversionofthetraitwithimprovedfunctionality, fewer side effects, or a lower threshold for expression [4]. This criterion is based on two assumptions:(i)individualsinderivedlineagesshouldexpressthe traitmorefrequentlythan individualsinancestral-proxylineages(whichproducethetraitinfrequently),and(ii)atraitina populationinwhichitisexpressed(andexposedtoselection)morefrequentlyshouldevolve greaterandmorerapidrefinement[4].Asacorollary,thefitnessconsequencesofatrait–in otherwordsitscontributiontoindividualfitness–shouldbehigherinderivedlineagesthanin ancestral-proxylineageswhenbothareinthederivedenvironment[4,49].

EvaluatingthePlasticity-FirstHypothesisin Nature:General Framework

Ratherthandescribehoweachcriterioncouldbetestedindividually,wepresentaschemefor testingallcriteriasimultaneously(Figure2).Ourschemeconsistsoftwophases:(i)identification

ofancestral-proxyandderivedlineages,and(ii)common-gardenexperimentationinwhichboth typesoflineagesarerearedunderenvironmentalconditionssimilartothosethattheywould experienceinthewild.

Beforestarting,itisessentialthatbackgroundinformationaboutthestudysystemisknown (Box 2).Assuming this informationis available, the first phaserequires inferring ancestral

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becloselyrelatedtothederivedlineages,buttheyshouldnotpossessthederived(potentially

fixed)traitwhenintheirnatural(ancestral)environmentthatlackstheinducingstimulus.

In the second phase of testing the plasticity-firsthypothesis, all key criteriacan be tested

simultaneously.Thisrequiresrearingmultiplesibshipsfromancestral-proxyandderivedlineages (Figure2A)inconditionsrepresentingancestralandderivedenvironments(e.g.,withoutandwith theinducingstimulus,respectively).Thiscouldbedonewithacommon-gardenorreciprocal transplantdesign.Anadvantageofthisapproachisthatitallowsonetoestimatehowmuch evolutionarydistance(fromancestraltoderivedtrait) wascoveredwhenanancestrallineage experiencedanovelenvironment(indeed,suchenvironmentallyinducedvariantstypicallycover onlypartofthisevolutionarydistance;e.g.,[22,27,29,50]).Multiplesibshipsarenecessary,both becausetheexpressionofphenotypicplasticityoftenvariesamonggenotypes[15]andbecause criterion 2 specifically involves comparing genetic variability across ancestral and derived

environments.

Fromsuch an experiment, observations and measurementsthat could validate the criteria include:awidevarietyofphenotypesproducedbyancestral-proxysibshipsinderived environ-ments,someofwhicharealongthesameaxisofvariationasthefocalphenotypepossessedby derived individuals(criteria 1 and2; Figure 2B); an increase inheritability ofthe trait(s) (or componentsofthetrait)amongancestral-proxysibshipswhenrearedinderivedenvironments (A)

Lineage 1 Lineage 2 Lineage 3 Ancestral phenotype

Induced novel phenotype

Canalized novel phenotype

(C) Time 1 Time 2

Compare fitness of induced versus canalized novel phenotypes

(B)

Phenotype

Ancestral environment

Novel environment

Environment (A, ancestral; N, novel) N N

A A A N

Pre-exis!ng plas!city?

Compare reac!on norms and heritabili!es Lineage 1 Lineage 2 Lineage 3

Figure2.ApproachesforTestingtheKeyCriteriaofthePlasticity-FirstHypothesis.(A)Asaninitialstep,identify

lineagestoserveasancestral-proxiestothelineage(s)thatproduce(s)thefocaltrait.Inthisexample,lineage1doesnot

produceanoveltraitduringnormaldevelopment;lineage2producesthenoveltraitaspartofnormaldevelopment

dependingonenvironmentalconditions(i.e.,itexhibitsadaptiveplasticityintraitexpression);lineage3producesthenovel

traitregardlessofenvironmentalconditions(i.e.,itiscanalized,meaningthatitexhibitsnoplasticityinthetrait).(B)Next,use

acommon-gardenapproachtodetermineif:(i)ancestral-proxylineagesthatnormallylackthetraitofinterest(lineage1)

producedevelopmentalvariantsofthetraitthroughphenotypicplasticitywhenexperiencingthenovelenvironmental

stimulus(criterion1);(ii)thenovelenvironmentuncoverscrypticgeneticvariationintheseancestral-proxylineages(criterion

2);(iii)phenotypicvariationrevealedintheancestral-proxylineagesisgreaterthaninderivedlineages(andmightberandom

withrespecttoitsadaptivevalueinthenovelenvironment);and(iv)reactionnormshaveevolvedinamannersuggestingthat

selectionhasrefinedtraitexpressioninthenovelenvironment(indicatedbydirectionalreactionnormsinlineage2versusflat

reactionnormsinlineage3;criterion3).(C)Finally,useacommon-gardenapproachtodetermineifthetraithasindeed

undergoneadaptiverefinementbycomparingthefitnessofindividualsfromlineagesthatproducethenovelphenotype

facultativelyversusconstitutively(criterion4).Ifgeneticaccommodationhasoccurred,thelattershouldoutperformthe

formerinthenovelenvironment[indicatedbyincreasedgrowth(largersize)oftheblue(canalized)phenotypeattime2],but

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(criterion2;Figure2B);achangefromreactionnormslackingconsistentdirectionalityamong ancestral-proxysibshipstohavingarelativelyconsistentslopeamongderivedsibships(criteria 2and3;Figure2B);achangeintheslopeorelevationofthereactionnorminderivedsibships relativetoancestral-proxysibships(criterion3;Figure2B);greatervarianceintraitvaluesfor ancestral-proxysibshipscomparedtoderivedsibshipswhenrearedinderivedenvironments (criteria2and3;Figure2B);greaterfitness(e.g.,survival,growth,size,development,fecundity,

etc.)ofderivedsibshipsthanancestral-proxysibshipswhenrearedinderivedenvironments (criterion4;Figure2C);andastrongercorrelationbetweenfitnessandtraitvalueinderived

sibshipsthanancestral-proxysibshipswhenrearedinderivedenvironments(criterion4;see

Box3forothersuggestionsfortestingcriterion4).

EvaluatingthePlasticity-FirstHypothesisin Nature:IllustrativeCaseStudies

Toillustratetheaboveframeworkfortestingthekeycriteriaoftheplasticity-firsthypothesis,we

describetwo casestudies.Althoughthesestudies arenot necessarilythe mostcompelling examplesofplasticity-firstevolution,theyillustratehowtotesttheplasticity-firsthypothesisina

naturalpopulation.

SpadefootToads

Speatadpoles exhibita novel polyphenismnot seenin otherspecies[22] consistingofan omnivore ecomorph, which eats detritus primarily, and a morphologically and behaviorally distinctivecarnivoreecomorph,whichspecializes onshrimpandwhichexpressesasuiteof unique,complextraits[51].Omnivoresarethedefaultmorph;carnivoresareinducedwhena young omnivoreeats shrimp orothertadpoles [28,52]. However, most populations harbor heritablevariationinthepropensitytoproducecarnivores[51].Carnivoresarisedevelopmentally fromanomnivore-likeformviaacceleratedgrowthoffeatures[53],andfrequency-dependent, disruptiveselection–stemmingfromresourcecompetition–maintainsbothecomorphswithin most populations [54]. Several studies, taken together, suggest that this novel carnivore ecomorpharosethroughplasticity-firstevolution[22,41,55].

Onestudyfoundsupportforcriteria1,3,and4 [22].Using ancestralcharacterstate recon-struction, Scaphiopus couchii was chosen as a proxy for non-plastic Spea ancestors

Box3.AlternativeMethodsforEvaluatingCriterion4ofthePlasticity-FirstHypothesis

Ourcriteriamightbevalidatedusingmethodsotherthanthosepresentedabove.Thisisespeciallylikelytobetruefor

criterion4becausewhatconstitutesasuperiortraitissystem-specific.Wehighlightheresomealternativeapproachesfor

testingcriterion4.

(i) Compareindifferentlineagestheamountofstimulusrequiredtoinducethefocaltrait(e.g.,[62]).Forexample,inthe

caseoflight-inducedresponseinplants,onecouldmeasuretheamountoflightneededtoinducethetraitand,inthe

caseofpredator-induced responsesineitherplantsoranimals,onecouldmeasuretheintensityofpredationor

abundanceofpredatorsneededtoinducethetrait.Moreover,iftheunderlyingendocrinesignalsareknown,onecould

manipulateconcentrationsofhormonestodeterminetheamountneededtoinducethetrait.Generally,theamountof

stimulusrequiredtoelicitinductionofatraitshouldbeinverselyproportionaltotheamountofevolutionarytimea

populationhasbeenexposedtothatstimulus.Thus,thethresholdofinductionshouldbelower(orzero)inderived

sibshipsthaninancestral-proxyones.

(ii) Performexperimentsinwhichindividualsfromancestral-proxyandderivedlineagesaredirectlysetagainstone

another(Figure2C)[28].Forexample,ifderivedindividualshaveanovelresource-acquisitiontrait,thentheycouldbe

directlycompetedwithancestral-proxyindividualsinobtainingthatresource.Onecouldthendetermineif(aspredicted)

derivedindividualsobtainmoreresourceandexhibitimprovedsurvivalorgrowththanancestral-proxyindividuals.

(iii) Measureselectiononthetraitinancestral-proxy,derivedpolyphenic,andderivedconstitutiveexpressionlineagesin

thewild[54].Ideally,onewouldidentifyindividualswithdifferenttraitvaluesandmeasuretheirfitness.Theexpectationis

thatderivedlineageswithconstitutiveexpressionshouldexhibitthestrongestselectionfavoringthetrait.Inpractice,

however,itmightonlybepossibletomeasureacomponentoffitness,suchassurvival,matingsuccess,orfecundity,or

(evenlessdirectly)atraitthatcorrelateswiththesefitnesscomponents,suchasbodysize.Regardless,fromtheslope

andshapeoftheregressionlinerelatingphenotypetofitness(orsomeproxyoffitness),onecoulddeterminethe

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(Sc.couchiiproduceonlyomnivores).Gutlength(carnivoresproduceshortergutsthan omni-vores)andgutcellproliferation(ameasureofgutperformance)werecomparedinSc.couchii, Speamultiplicata,andSp.bombifrons.Sc.couchiiproducedawiderrangeofgutlengthswhen fedshrimp[anoveldietforthisspecies,butrepresentingthederiveddiet(environment)forSpea] thanwhenfeddetritus,andthevariationwasnotdirectional:bothshorterandlongergutlengths wereproducedonshrimp.Bycontrast,bothSpeaspeciesconsistentlyproducedshorterguts whenfedshrimpthanwhenfeddetritus.Furthermore,whereasSc.couchiitadpolesdidnot exhibitincreasedgutcellproliferationwhenfedshrimp,bothSpeaspeciesdid,suggestingthat shrimpdigestionhasundergonegeneticaccommodationinSpea.

Twosubsequentstudiesfurthersupportcriteria2,3,and4[41,55].Crypticgeneticvariationin Sc.couchii was detectedwhenfed differentdiets andexposed to corticosterone(a stress hormone). These Sc. couchii tadpoles developed and grew more slowly, had increased corticosteronelevels, andexhibited greater heritability insize, development,andgut length whenfedshrimpthanwhenfeddetritus.Inaddition,Sc.couchiitadpolesexposedto cortico-steronehadgreaterheritabilityindevelopmentandgutlength.Therefore,thesestudies dem-onstratedareleaseofcrypticgeneticvariationintheancestralconditionwhentadpoleswere exposedtothederivedstimulus,andtheyalsoidentifiedapossiblehormonalmediatorofthe

carnivoreecomorph.

Moreover, this novelecomorph appearsto have undergone genetic assimilation insome derivedpopulationsofSpea.Inancestralpopulationscontainingonlyasinglespecies,both Sp.multiplicataandSp.bombifronsproducesimilar,intermediatefrequenciesofboth eco-morphs.Bycontrast,inderivedpopulationswherethesespeciesco-occur,eachbecomes nearlymonomorphic,withSp.multiplicataproducingmostlyomnivores,andSp.bombifrons producingmostlycarnivores,regardlessofresourceavailability[28].Thisnearfixationofone

ecomorphisadaptivebecauseitminimizescompetitionbetweenthetwospecies[28].More generally, this selection-driven shift from plastic to fixed ecomorph production supports

criterion3.

Note,however,thatSc.couchiimightnotrepresenttheancestralcondition(theymighthave evolvedtheomnivorefeedingstrategysecondarilyasanadaptiveresponsetocompetitionwith, orpredation by, sympatricSpea tadpoles),and supportfor criteria1–3 could therefore be questioned.Inaddition,supportforcriterion4islimited.Nevertheless,thissystemillustrateshow plasticitymight have contributedto the evolution ofa novel,complexphenotype innatural populations.

Cavefish

Eyelossincave-dwellingpopulationsofMexicantetra(Astyanaxmexicanus)alsoprovidesan excellentsettingfortestingtheplasticity-firsthypothesis.Thecaveenvironmentisan

evolution-arily novel environment, and it is known that cave populations are derived from surface populations[56].

The greatest abiotic difference between surface and cave environments (other than light availability)islowerconductivityofcavewater[43].WhensurfaceA.mexicanuswerereared underlowconductivity,theydisplayedgreatervariationineyeandorbitsize,andthey upregu-latedHSP90[43].Moreover,whenHSP90wasmanipulatedtomimicenvironmentalstress(i.e., itschaperoneabilitywasreduced),surfacefishdisplayedgreatervariationineyeandorbitsize

beyondtherangeobservedincontrols.CavefishdidnotincreasetraitvariationunderHSP90

manipulation.Inaddition,whenHSP90-manipulatedfishwiththesmallesteyeswerecrossed,

theiruntreatedF2progenyhadeyesandorbitsizesatthelowerendoftherangeinparentalfish,

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Table1.ExamplesofSpecies,Conditions,andTraitsforwhichTwoorMoreKeyCriteriaofthePlasticity-First HypothesisAreSupportedinNaturallyOccurringSystems

Species NovelCondition(s) Trait Criteria

Supported Refs

Plants

Arabidopsisthaliana Shade,HSP90inhibition Morphology;growth 1,2 [42,63]

Acaciaspp. Antguards Antmutualism 1,3,4 [64,65]

Nematodes

Rhabditinaspp. Alternativediets Mouthmorphology 1,3 [66]

Crustaceans

Daphniamelanica Fishpredators Melanization 1,3 [26]

Insects

Drosophilamojavensis Alternativehosts Hostpreference 1,3 [67–69]

Politessabuleti

(skipperbutterfly)

Lowtemperatures Wingpatterning;

coloration

1,3 [70]

Nymphalisantiopa(mourning

cloakbutterfly)

Lowtemperatures Wingpatterning;

coloration

1,3 [71]

Fishes

Fundulusspp.(killifish) Varioussalinities Salinitytolerance 1,3 [72–76]

Cyprinodondiabolis

(DevilsHolepupfish)

Hightemperatures;

reducedresources

Pelvicfinloss 1,3 [77,78]

Gasterosteusaculeatus

(threespinestickleback)

Reduced cannibalism

Antipredatorand

courtshipbehavior

1,3 [79,80]

Gasterosteusaculeatus

(threespinestickleback)

Alternative resources

Resourceuse

ecotypes

1,3 [29]

Gasterosteusaculeatus

(threespinestickleback)

Freshwater Growth(size);salinity

tolerance

1,2,3,4 [30,81–84]

Astyanaxmexicanus

(Mexicantetra)

Caves Eyeloss 1,2,3,4(?) [43,56]

Amphibians

Spadefoottoadspp. Ephemeralponds Developmenttime 1,3 [85]

Notophthalmusviridescens

(easternnewt)

Alteredpond

hydroperiod

Developmental strategy

1,3,4 [86–88]

Lithobatessylvaticus

(woodfrog)

Insecticide Insecticide

tolerance

1,3,4 [89]

Speaspp.

(spadefoottoad)

Alternativediets;

competitors

Resourceuse

ecomorph

1,2,3,4 [22,28,41,55]

Reptiles

Anolisspp. Alternativeperch diameters

Hindlimblength 1,4 [27,50,90,91]

Notechisscutatus

(tigersnake)

Alternativediets Headsize 1,3,4 [20,92,93]

Birds

Agelaiusphoeniceus(red-wing

blackbird),Parusmajor

(greattit),andotherurban

birds

Urbanlandscapes Song 1,3 [94,95]

Carpodacusmexicanus

(housefinch)

Various Reproductiveattributes;

offspringmorphology

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suggest that: stressful conditions (i.e., low conductivity) induce similar changes in HSP90 functionasinlaboratorymanipulationofHSP90;bothstressfulconditionsandHSP90 manipu-lationresultinuncoveringofcrypticgeneticvariationforeyesize;andindividualsthatdevelop smalleyeswhenHSP90isinhibitedcontainallelesthatcontributetotheinheritanceofreduced eyes,evenintheabsenceoftreatment(i.e.,becomegeneticallyassimilated).

Subsequentrefinementofthisinducedeyelessphenotypeisassociatedwithimproved

func-tionality in cave conditions. When competed directly, cavefish forage better than

surface-dwellingfishinthedark[56].

Thus,the transitionfrom surfaceto cave likelyinvolved theproduction ofa range ofnovel phenotypes(satisfyingcriterion 1),whichwasfacilitatedbytheuncoveringofcrypticgenetic variation(satisfyingcriterion2).Thiswasfollowedbyselectionfavoringfixationoftheeyeless

phenotype(satisfyingcriterion3)andpossiblerefinementofthisphenotype,suchthatcavefish

outcompetesurfacefishforfoodinthedark(potentiallysatisfyingcriterion4).Note,however,

thatitisunclearifderived(cave-dwelling)populationsexhibitenhancedresourceacquisition becauseofrefinementofthefocaltraitperse(reducedeyesize;asrequiredbycriterion4)as

opposedtosomeotheraspectofthephenotype(e.g.,olfaction),whichcouldhavearisenvia newmutations.Thus,furtherstudieswillbenecessarytodetermineifcriterion4issatisfiedinthis

system.Nevertheless,thissystemagainillustrateshowplasticitymighthavecontributedtothe evolutionofacomplextrait.

EvaluatingthePlasticity-FirstHypothesisin Nature:General Assessmentof

theEvidence

Beyondthesecasestudies,researchershave(intentionallyornot)demonstratedportionsofthe plasticity-first hypothesis in numerous natural systems. Indeed, two recent reviews have

evaluatedtheempiricalsupportforplasticity-firstevolutionandfoundmanysystemsinwhich

an adaptive trait is present inancestral (orancestral-proxy) lineages as an environmentally inducedvariant[13,31],therebysatisfyingcriterion1above.However,asnotedpreviously,the mereexistenceofsuchancestralplasticityisnotsufficienttodemonstratethatatraitevolvedvia

aplasticity-firstprocess;demonstratingthat plasticity-firstevolution haslikely occurredalso

requiresevidence that any evolutionary changesin expressionof plasticity reflectselection

(criteria3and4).

InTable1 weprovide examplesofnaturallyoccurringsystemsinwhichourliteraturesurvey revealedthattwoormorecriteriawerevalidated.Ourgeneralassessmentisthatfewsystems havefulfilledallfourcriteria.Inparticular,althoughmanysystemshavesatisfiedcriteria1and3,

fewsatisfycriteria2(accumulationandrelease ofcrypticgenetic variationinancestral-proxy lineages)and4(increasedrefinementinderivedlineages).Whilecriterion2istheleastcrucialof

thefourcriteria(andamongthemostdifficult toevaluate),criterion4 isessentialtoruleout

alternativeevolutionaryexplanations(seeabove).

Wehastentoadd,however,thatalthoughfewsystemssupportallfourcriteria,takentogether thebodyofevidenceisreminiscentofDarwin'sapproachtosupporting evolutionbynatural selection[57]:multiple linesofpartial evidencepointtowardthesameprocess operatingin many,diversetaxa.

ConcludingRemarks

Wehavedescribedkeycriteriaforevaluatingtheplasticity-firsthypothesisinnaturalpopulations,

providedaroadmapfortestingthesecriteria(Figure2andBox3),andpresentedexamplesthat serveasaguidefortestingthecriteria(Table1).Moretestsareneededbeforetheplasticity-first

hypothesiscanberegardedasageneralexplanationforhowcomplex,adaptivetraitsoriginate.

OutstandingQuestions

Howpervasiveisplasticity-first

evolu-tioninnature?

Canweobserveplasticity-first

evolu-tioninreal-timeinnaturalpopulations?

Whatarethemolecularsignaturesof

theplasticity-firsthypothesis?

Areparticulartaxonomicgroups and

traitsmorelikelytoexperience

plastic-ity-firstevolutionthanothers,and,ifso,

why?

Whataretheselectiveandproximate

bases (e.g., molecular mechanisms)

of genetic accommodation and

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Acknowledgments

WethankK.Pfennig,C.Ledón-Rettig,C.Martin,P.Durst,andtwoanonymousreviewersforvaluablediscussionand

comments.

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