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Paleontological Society

Exaptation-A Missing Term in the Science of Form Author(s): Stephen Jay Gould and Elisabeth S. Vrba Reviewed work(s):

Source: Paleobiology, Vol. 8, No. 1 (Winter, 1982), pp. 4-15 Published by: Paleontological Society

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Paleobiology,8(1), 1982,pp. 4-15

Exaptation-a missing termin the science of form

StephenJayGould and ElisabethS. Vrba*

Abstract.-Adaptationhas been definedand recognizedby two differentcriteria:historicalgenesis(fea- turesbuiltby naturalselectionfortheirpresentrole)and currentutility(featuresnow enhancingfitness no matterhow theyarose). Biologistshave oftenfailedtorecognizethepotentialconfusionbetweenthese differentdefinitionsbecausewe have tendedtoview naturalselectionas so dominantamongevolutionary mechanismsthathistoricalprocessand currentproductbecomeone. Yet ifmanyfeaturesoforganisms are non-adapted,but available forusefulcooptationin descendants,thenan importantconcepthas no name in our lexicon(and unnamedideas generallyremainunconsidered):featuresthat now enhance fitnessbut were not builtby naturalselectionfortheircurrentrole. We proposethatsuch featuresbe called exaptationsand thatadaptationbe restricted,as Darwin suggested,to featuresbuiltby selection fortheircurrentrole. We presentseveralexamplesof exaptation,indicatingwherea failureto concep- tualizesuchan idea limitedtherangeofhypothesespreviouslyavailable. We exploreseveralconsequences ofexaptationand proposea terminologicalsolutionto theproblemofpreadaptation.

StephenJ. Gould.

02138

ElisabethS. Vrba.

Museum ofComparativeZoology,Harvard University,Cambridge,Massachusetts

TransvaalMuseum,Paul KrugerStreet,P.O. Box 413, Pretoria,SouthAfrica

Accepted: October15, 1981

I. Introduction

We wishto proposea termfora missingitem in the taxonomyof evolutionarymorphology. Termsin themselvesare trivial,buttaxonomies revisedfora differentorderingof thoughtare not withoutinterest.Taxonomiesare not neu- tralorarbitraryhat-racksfora setofunvarying concepts;theyreflect(or even create)different theoriesabout the structureof the world. As Michel Foucault has shown in several elegant books (1965 and 1970,forexample),whenyou knowwhypeopleclassifyin a certainway, you understandhow theythink. Successivetaxonomiesare thefossiltracesof substantialchanges in human culture.In the mid 17thcentury,madmenwereconfinedin in- stitutionsalong with the indigentand unem- ployed,thusendinga longtraditionofexile or tolerationfortheinsane. But what is the com- mongroundfora taxonomythatmixesthemad with the unemployed-an arrangementthat strikesus as absurd. The "key character"for the "highertaxon,"Foucault argues,was idle- ness, thecardinalsin and dangerin an age on the brinkof universalcommerceand industry

* An equal timeproduction;orderofauthorshipwas de- terminedbya transoceaniccoin flip.

(?) 1982The PaleontologicalSociety.All rightsreserved.

(Foucault's interpretationhas been challenged byBritishhistorianofscienceRoyPorter,MS). In othersystemsof thought,what seems pe- ripheralto us becomescentral,and distinctions essentialto us do not matter(whetheridleness is internallyinevitable,as in insanity,or exter- nallyimposed,as in unemployment).

II. Two MeaningsofAdaptation

In thevernacular,and in sciencesotherthan evolutionarybiology,the word adaptationhas several meaningsall consistentwith the ety- mologyofad + aptus,ortowardsa fit(fora par- ticularrole). When we adapt a tool fora new role,we changeitsdesignconsciouslyso thatit will workwellin itsappointedtask. Whencre- ationistsbeforeDarwin spoke of adaptation- for the term long precedes evolutionary thought-theyreferredto God's intelligentac- tion in designingorganismsfor definiteroles. When physiologistsclaim thatlargerlungs of Andean mountainpeoplesare adapted to local climates,theyspecifydirectedchangeforbetter function.In short,all thesemeaningsreferto historicalprocessesof change or creationfor definitefunctions.The "adaptation"is designed specificallyforthetask it performs. In evolutionarybiology, however, we en-

0094-83 73/82/0801-0002/$1.00

EXAPTATION

5

TABLE 1. A taxonomyoffitness.

Process

Natural selectionshapesthecharacter fora current use-adaptation

A character,previouslyshaped by naturalselection

fora

particularfunction(an adaptation),is coopted

fora

new use-cooptation

adaptation

exaptation

Character

aptation

Usage

function

effect

A characterwhoseorigincannotbe ascribedto thedirectaction ofnaturalselection(a nonaptation),is coopted fora currentuse-cooptation

countertwodifferentmeanings-and a possible conflationof concepts-forfeaturescalled ad- aptations.The firstis consistentwiththe ver- nacularusages citedabove: a featureis an ad- aptationonlyifitwas builtbynaturalselection forthe functionit now performs.The second definesadaptationin a static,orimmediateway as anyfeaturethatenhancescurrentfitness,re-

gardlessof its historicalorigin.(As a confusion,adaptationrefersboth to a

and a state of being. We are only discussing

stateofbeinghere-that is, featurescontribut- 1979, 1980). "An adaptationis, thus,a feature

ingtofitness.We includesomecommentsabout thisfurtherproblemin sectionVIE.) Williams,in his classic book on adaptation, recognizedthisdilemmaand restrictedtheterm to its first,or narrower,meaning.We should speak of adaptation,he argues,onlywhen we can "attributethe originand perfectionof this

design to a long period of selectionforeffec- examplefroma famoussource.In his chapter

devotedto"difficultieson theory,"Darwinwrote (1859, p. 197):

The suturesin theskullsofyoungmammals have beenadvancedas a beautifuladaptation foraidingparturition,and no doubttheyfa- cilitate,or maybe indispensableforthisact; but as suturesoccur in the skulls of young birdsand reptiles,whichhave onlyto escape froma brokenegg, we may inferthat this structurehas arisenfromthelaws ofgrowth, and has been takenadvantageofin thepar- turitionofthehigheranimals.

arisingdirectlyfromconstructionbynaturalse-

lection.Othershave adoptedvariousaspectsof this terminologyfor "effects"sensu Williams (Paterson 1981; Vrba 1980; Lambert, MS). However, Williamsand othersusuallyinvoke

theterm'effect'to designatetheoperationofa

The dilemmaof subsumingdifferentcriteria ofhistoricalgenesisand currentutilityundera singletermmaybe illustratedwitha neglected

usefulcharacternot built by selectionfor its currentrole-and we shall followthis restric- tion here (Table 1). Williams also recognizes thatmuchhagglingabout adaptationhas been "encouragedby imperfectionsof terminology" (1966,p. 8), a situationthatwe hopetoalleviate slightly. Bock, on theotherhand,championsthesec-

further ond, or broader, meaningin the other most

process

widely-citedanalysis of adaptation fromthe 1960's(Bock and von Wahlert1965;Bock 1967,

of the organism,whichinteractsoperationally withsomefactorofitsenvironmentso thatthe individualsurvivesand reproduces"(1979, p.

39).

tivenessin thisparticularrole"(1966, p. 6). In his terminology,"function"refersonly to the

operationof adaptations.Williamsfurtherar- gues thatwe mustdistinguishadaptationsand theirfunctionsfromfortuitouseffects.He uses "effect"in its vernacular sense-something caused or produced,a resultor consequence. Williams'conceptof"effect"maybe applied to a character,or to itsusage, or to a potential(or process),arisingas a consequenceof true ad- aptation. Fortuitouseffectalways connotesa consequencefollowing"accidentally,"and not

Darwin assertstheutility,indeedthenecessity, of unfusedsuturesbut explicitlydeclinesto la- bel theman adaptationbecause theywere not builtby selectionto functionas theynow do in mammals.WilliamsfollowsDarwin and would

6

STEPHEN JAY GOULD & ELISABETH S. VRBA

decline to call this featurean adaptation; he would designateits role in aidingthe survival of mammalsas a fortuitouseffect.But Bock would call the suturesand the timingof their fusionan adaptation,and a vitalone at that.

towardsfitness.They owe theirfitnessto fea- turespresentforotherreasons,and are there- forefit(aptus) byreason of (ex) theirform,or ex aptus.Mammaliansuturesare an exaptation forparturition.Adaptationshave functions;ex-

As an example of unrecognizedconfusion, aptationshave effects.The general,staticphe-

nomenonofbeingfitshouldbe called aptation, notadaptation.(The setofaptationsexistingat

10): "Any characteristicof living organisms any one timeconsistsof two partiallyoverlap-

considerthisdefinitionofadaptationfroma bi- ologicaldictionary(Abercrombieet al. 1951,p.

the

provestheirchancesofsurvivaland ultimately subsetof exaptations.This also applies to the

leaving descendants,in comparisonwith the chancesofsimilarorganismswithoutthe char- acteristic;natural selectionthereforetends to establishadaptationsina population." This def- initionconflatescurrentutilitywith historical genesis.What is to be done withusefulstruc-

turesnotbuiltbynaturalselectionfortheircur-

rentrole?

III.

which, in the environmenttheyinhabit,im-

pingsubsets:thesubsetof adaptationsand

moreinclusivesetofaptationsexistingthrough time;see Table 1.)

IV. The CurrentNeed fora ConceptofExaptation

Why has thisconflationof historicalgenesis withcurrentutilityattractedso littleattention heretofore?Every biologistsurelyrecognizes thatsomeusefulcharactersdid notariseby se-

lectionfortheircurrentroles;whyhave we not We have identifiedconfusionsurrounding honoredthatknowledgewitha name?Does our

A Definitionof Exaptation

one ofthecentralconceptsin evolutionarythe- ory.This confusionarises,in part,because the taxonomyof formin relationto fitnesslacks a term.FollowingWilliams(seeTable 1),we may designateas an adaptationanyfeaturethatpro- motesfitnessand was builtby selectionforits currentrole(criterionofhistoricalgenesis).The operationofan adaptationis itsfunction.(Bock

uses the termfunctionsomewhatdifferently, he clearlyrecognizedtheproblemand did sep-

but we believewe are followingthe biological vernacularhere.)We mayalso followWilliams

in labellingtheoperationof a usefulcharacter unnamed featuresthat we call exaptations)?

not builtby selectionforits currentrole as an effect.(We designateas an effectonlytheusage ofsucha character,notthecharacteritself,see

p. 5.) But what is the unselected,but useful

characteritselfto be called? Indeed it has no recognizedname(unlesswe acceptBock's broad definitionof adaptation-the criterionof cur- rentutilityalone and rejectbothDarwin and Williams).Its space on thelogicalchartis cur- rentlyblank. We suggestthatsuch characters,evolvedfor otherusages(orforno functionat all), and later

"coopted"fortheircurrentrole, be called ex- aptations. (See VIA on the relatedconceptof

"preadaptation.")They are fitfortheircurrent some importance(in assessingthecapacitiesof

role, henceaptus, but theywere not designed forit,and are thereforenotad aptus,or pushed

thehumanmind,forexample),buthe retained a preeminentroleforadaptationand oftendes-

failureto do so simplyunderscorethe unim- portanceof the subject? Or mightthis absent term,in Foucault's sense, reflecta conceptual structurethatexcludedit?And,finally,does the potentialneed forsuch a termat thistimein- dicate thatthe conceptualstructureitselfmay be altering? Whydid Williamsnot suggesta term,since

arate usages into functionsand effects(corre- spondingrespectivelyto adaptationsand to the

Whydid Bock failto specifytheproblemat all? We suspectthatthe conceptualframeworkof modernevolutionarythought,by continually emphasizingthe supremeimportanceand con- tinuityofadaptationand naturalselectionat all levels, subtlyrelegatedthe issue of exaptation to a peripheryof unimportance.How could nonadaptiveaspectsofformgaina properhear- ing underBock's definition(1967, p. 63): "On theoreticalgrounds,all existingfeaturesof an- imals are adaptive. If theywere not adaptive, thentheywould be eliminatedbyselectionand

woulddisappear."Williamsrecognizedthephe-

nomenon of exaptation and even granted it

EXAPTATION

7

ignated effectsas fortuitousor peripheral- "merelyan incidentalconsequence"he statesin one passage (p. 8). We believethattheadaptationistprogramof modernevolutionarythought(Gould and Le-

wontin1979)has been weakeningas a

resultof

challengesfromall levels,moleculesto macro- evolution.At the biochemicallevel, we have theoriesofneutralismand suggestionsthatsub- stantialamountsof DNA may be nonadaptive at thelevel of the phenotype(Orgeland Crick 1980;Doolittleand Sapienza 1980).Studentsof macroevolutionhave arguedthatadaptationsin populationstranslateas effectsto yieldthepat- ternsof differentialspeciesdiversificationthat mayresultin evolutionarytrends(Vrba's effect hypothesis,1980). If nonadaptation(or what shouldbe callednonaptation)is abouttoassume an importantrolein a revisedevolutionarythe- ory,thenour terminologyofformmustrecog- nize its cardinal evolutionarysignificance- cooptabilityforfitness(see Seilacher1972, on importanteffectsof a nonaptivepatternin the structureand colorationofmolluscs). Some colleagues have said that theyprefer Bock's broaddefinitionbecauseitis moreeasily

operational.We can observeand experimentto determinewhat good a featuredoes foran or- ganismnow. To reconstructthehistoricalpath- way of its originis always moredifficultand often(whencrucialevidenceis missing)intract- able. To this we replythat we are not tryingto dismantleBock'sconcept.We merelyarguethat it should be called aptation(with adaptation and exaptationas its modes). As aptation,it retainsall the favorablepropertiesfortesting enumeratedabove. Historical genesis is, undoubtedly,a. more difficultproblembutwe cannotthereforeignore it. As evolutionists,we are charged,almostby definition,to regardhistoricalpathwaysas the essenceofoursubject.We cannotbe indifferent to thefactthatsimilarresultscan ariseby dif- ferenthistoricalroutes.Moreover,the distinc- tionbetweenad- and exaptation,howeverdif- ficult,is not unresolvable.If we ever finda small runningdinosaur,ancestralto birdsand clothedwithfeathers,we will knowthatearly featherswereexaptations,notadaptations,for flight.

V. ExamplesofExaptation

A) Feathersand flight-sequentialexaptation

in theevolutionofbirds.-Consider a common scenariofromtheevolutionofbirds.(We do not assertitscorrectness,but onlywishto examine appropriateterminologyfora commonset of hypotheses.)Skeletal features,including the sternum,rib basketand shoulderjoint, in late Jurassicfossilsof Archaeopteryxindicatethat thisearliestknownbirdwas probablycapable

of onlythe simplestfeatsof flight.Yet it was quite thoroughlyfeathered.This has suggested to many authorsthat selectionforthe initial developmentoffeathersin an ancestorwas for the functionof insulationand not for flight (Ostrom1974, 1979;Bakker 1975). Such a fun- damental innovationwould, of course, have manysmall as well as far-reaching,incidental consequences.For example,along no descen- dant lineage of thisfirstfeatheredspecies did (so faras we know)a furrycoveringofthebody evolve. The fixationearlyin thelifeoftheem- bryo,of cellularchangesthatlead on the one hand to hair,and on theotherto feathers,con- strainedthe subsequentcourseof evolutionin bodycovering(Oster 1980). Archaeopteryxalreadyhad largecontour-type feathers,arrangedalong its arms in a pattern verymuch as in the wings of modernbirds. Ostrom(1979, p. 55) asks: "Is it possiblethat the initial(pre-Archaeopteryx)enlargementof featherson those narrow hands mighthave been to increasethehand surfacearea, thereby makingit moreeffectivein catchinginsects?" He concludes(1979, p. 56): "I do believe that the predatorydesign of the wing skeletonin Archaeopteryxis strongevidence of a prior predatoryfunctionof the proto-wingin a cur- "

sorialproto-Archaeopteryx. Later selectionfor

changesin skeletalfeaturesand feathers,and forspecificneuromotorpatterns,resultedin the evolutionofflight. The Black Heron (or Black Egret,Egretta ardesiaca) of Africa,like most modernbirds, uses itswingsin flight.But italso uses themin

an interestingway to preyon small fish:"Its fishingis performedstandingin shallow water withwingsstretchedout and forward,forming an umbrella-likecanopywhichcasts a shadow on thewater.In thisway itsfoodcan be seen"

8

STEPHEN JAY GOULD & ELISABETH S. VRBA

(McLachlan and Liversidge1978, p. 39, Plate 6). This "mantling"ofthewingsappears to be a characteristicbehaviorpattern,witha genetic basis. The wing and featherstructuresthem- selvesdo notseemtobe modifiedincomparison withthoseof closelyrelatedspecies,the indi- vidualsofwhichdo nothuntin thisway (A. C. Kemp, pers.comm.). We see, in thisscenario,a sequentialset of adaptations,each convertedto an exaptationof

adaptation for storingphosphatesneeded for metabolicactivity.Only considerablylater in evolutiondid bone replacethecartilaginousen- doskeletonand adopt the functionof support forwhichit is now mostnoted. Thus, bonehas twomajorusesin extantver- tebrates:support/protectionand storage/homeo- stasis(as a storehouseforcertainmineralions, includingphosphateions). The ions in verte- bratebone are in equilibriumwiththosein tis-

differenteffectthatsets the basis fora

subse-

sue fluidsand blood, and functionin certain

quent adaptation. By this interplay,a

major

metabolicactivities(Scott and Symons 1977).

evolutionarytransformationoccursthatproba-

For instance,in humans, 90% of body phos-

bly could not have arisenby purelyincreasing adaptation.Thus, the basic designof feathers

phorusis presentin theinorganicphase ofbone (Duthieand Ferguson1973).

is

an adaptationforthermoregulationand, lat-

FollowingHalstead's analysis,thedeposition

er, an exaptationforcatchinginsects.The de- velopmentof large contourfeathersand their arrangementon thearmariseas adaptationsfor insect catching and become exaptations for flight.Mantlingbehavioruses wingsthatarose

of phosphatein bodytissuesoriginallyevolved as an adaptationfora storage/metabolicfunc- tion. The metabolicmechanismforproducing bone per se can thus be interpretedas an ex- aptation for support. The metabolic mecha-

as an adaptation for flight.The neuromotor nismsfordepositingan increasedquantityof

phosphatesand formineralization,as well as thearrangementofbonyelementsin an internal skeleton,are thenadaptationsforsupport. C) The evolutionofmammalianlactation.- Dickersonand Geis (1969) recounthow Alex- anderFleming,in 1922,discoveredtheenzyme lysozyme.He had a coldand,forinterest'ssake, added a fewdropsofnasal mucusto a bacterial culture.To his surprisehe found,aftera few

opmentof bone was an eventof major signifi- days, thatsomethingin themucuswas killing

thebacteria:theenzymelysozyme,sincefound in mostbodilysecretionsand inlargequantities

life on land. Halstead (1969) has investigated in thewhitesofeggs. Lysozymedestroysmany

cance in the evolutionof vertebrates.Without bone,vertebratescould nothave latertakenup

modificationsgoverningmantlingbehavior,and thereforethemantlingposture,are adaptations forfishing.The wingper se is an exaptationin itscurrenteffectofshading,just as thefeathers coveringit also arosein differentadaptivecon- textsbuthave providedmuchevolutionaryflex- ibilityfor otheruses duringthe evolutionof birds.

B) Bone as storageand support.-The devel-

the question: grantingits subsequent impor- tance as bodysupportin thelaterevolutionof vertebrates,why did bone evolve at such an earlystagein vertebratehistory?Some authors have hypothesizedthat bone initiallyarose as an osmoregulatoryresponseto lifein freshwa- ter.Others,like Romer(1963),postulateinitial

adaptation of bony "armor"for a protective write:

function.Pautard(1961, 1962)pointedout that anyorganismwithmuchmuscularactivityneeds

a convenientlyaccessible store of phosphate. Following Pautard, and notingthe seasonal cycleof phosphateavailabilityin thesea, Hal- stead (1969) suggestedthe followingscenario:

Calcium phosphates,laid down in the skin of the earliestvertebrates,evolvedinitiallyas an

bacteriabylysing,or dissolving,themucopoly- saccharidestructureofthecellwall. The amino acid sequenceof a-lactalbumin,a milkprotein ofpreviouslyunknownfunction,was thenfound to be so close to that of lysozyme,that some relationshipof close homologymust be in- volved. Dickersonand Geis (1969, pp. 77-78)

a-Lactalbuminby itselfis notan enzymebut was foundto be one componentofa two-pro- tein lactose synthetasesystem,presentonly in mammaryglands duringlactation The othercomponent(the "A" protein)had beendiscoveredin theliverand otherorgans as an enzymeforthesynthesisofN-acetyllac-

EXAPTATION

9

tosaminefromgalactoseand NAG. But the combinationof the A proteinand a-lactal- buminsynthesizesthemilksugarlactosefrom galactoseand glucoseinstead.The non-cat-

alytica-lactalbuminevidentlyacts as a con- troldeviceto switchitspartnerfromone po-

tentialsynthesisto another

thatwhena milk-producing-systemwas being

developedduringtheevolutionofmammals,

and when a need fora polysaccharide-syn- engagein communalhunting.A mechanismfor

thesizingenzymearose, a suitableone was

reintegratingsolitarywanderersintotheirprop-

found in part by modifyinga pre-existing er clan mustbe developed.In themeetingcer-

polysaccaride-cuttingenzyme.

unconsciouslyforcedpreviousauthorsintothis erroneousconceptualbind. Kruuk(1972), theleadingstudentof spotted hyenas,for example, notes that the enlarged sexual organsoffemalesare used in an impor- tantbehaviorknow as themeetingceremony. Hyenas spendlong periodsas solitarywander- ers searchingforcarrion,but theyalso live in well integratedclans thatdefendterritoryand

It appears

emony,twohyenasstandsideto side,facingin oppositedirections.Each liftsthe inside hind leg,exposingan erectpenisorclitoristoitspart- ner'steeth.Theysniffand lickeach other'sgen- italsfor10 to 15 seconds,largelyat thebase of thepenisor clitorisand in frontofthescrotum or falsescrotum. Having discovereda currentutilityfor the prominentexternalgenitaliaoffemales,Kruuk (1972, pp. 229-230) infersthattheymusthave evolvedforthispurpose:

It is impossibleto thinkofanyotherpurpose forthisspecialfemalefeaturethanforuse in

the

It may also be,

then,thatan individualwitha familiarbut relativelycomplexand conspicuousstructure sniffedat duringthe meetinghas an advan- tage over others;the structurewould often facilitatethisreestablishmentofsocial bonds by keepingpartnerstogetherover a longer meetingperiod. This could be the selective advantage that has caused the evolutionof

thefemales'and cubs' genitalstructure.

Yet another hypothesis,based upon facts known to every Biology I student,virtually criesout forrecognition.The penisand clitoris

labia majora. We knowthathighlevels of an- drogeninduce the enlargementof the clitoris and thefoldingoverand fusionofthelabia until theyresemblepenisand scrotalsac respectively. (In fact,in an importantsense,theyare thena penis and scrotalsac, given the homologies.) Human baby girlswithunusuallyenlargedad- renalssecretehighlevels of androgen,and are bornwitha peniformclitorisand an emptyscro- tal sac formedofthefusedlabia. Female hyenas are larger than males and

Thus, lysozyme,in all vertebratesin which itoccurs,is probablyan adaptationforthefunc- tion of killingbacteria. Furtherevolutionin mammals(alterationof a duplicatedgene ac- cordingto Dickersonand Geis, 1969) resulted in a-lactalbumin,an adaptation(togetherwith

the A protein)forthe functionof lactose syn- thesisand lactation.Human lysozyme,in this scenario, is an adaptation forlysingthe cell walls of bacteria,and an exaptationwith re- spectto thelactosesynthetasesystem.

D) Sexual "mimicry"in hyenas.-Females of

the spottedhyena,Crocutacrocuta,are larger thanmalesand dominantoverthem.Pliny,and otherancientwriters,had alreadyrecognizeda relatedand unusual featureof theirbiologyin calling themhermaphrodites(falsely,as Aris- totleshowed).The externalgenitaliaoffemales are virtuallyindistinguishablefromthe sexual organsofmalesbysight.The clitorisis enlarged and extendedto forma cylindricalstructure witha narrowslitat itsdistalend;itis no small-

erthanthemale'spenisand can also be erected. The labia majora are folded over and fused along the midlineto forma false scrotal sac

(thoughwithouttesticlesof course), virtually are homologousorgans,as are thescrotumand

identicalin formand positionwiththe male's

scrotum(HarrisonMatthews1939).

The literatureon thissexual"mimicry"is full of speculationsabout adaptive meaning.Most of theseargumentshave conflatedcurrentutil- ityand historicalgenesisin assumingthatthe demonstrationof modernuse (Bockian adap- tation)specifiesthe path of origin(adaptation as used by Williamsand Darwin, and as ad- vocatedin thispaper). We suggestthattheab- senceofan articulatedconceptofexaptationhas

10

STEPHEN JAY GOULD & ELISABETH S. VRBA

dominantover them. Since thesefeaturesare oftenhormonallymediatedinmammals,should we notconjecturethatfemalesattaintheirsta- tus by secretingandrogensand that the peni- formclitorisand falsescrotalsac are automatic, secondaryby-products.Since theyare formed anyway,a laterand secondaryutilitymighten- sue; theymay be cooptedto enhancefitnessin the meetingceremonyand then secondarily modifiedforthisnew role.We suggestthatthe peniformclitorisand falsescrotalsac arose as nonaptiveconsequencesofhighandrogenlevels

(a primaryadaptation relatedto the unusual

thatthe architectureof geneticmaterialmight fitall theirpresuppositionsabout evolutionary processes.The linearorderofnucleotidesmight be the beads on a stringof classical genetics:

one gene,one enzyme;one nucleotidesubstitu- tion,one minutealterationfornaturalselection to scrutinize.We are now, not even 20 years later,facedwithgenesin pieces,complexhier- archies of regulation and, above all, vast amountsof repetitiveDNA. Highlyrepetitive, orsatellite,DNA can existin millionsofcopies; middle-repetitiveDNA, withitstenstohundreds of copies, formsabout one quarterof the ge-

behavioralroleoffemales).Theyare,therefore, nome in bothDrosophila and Homo. What is

exaptationsforthemeetingceremony,and their effectin enhancingfitnessthroughthat cere- monydoes notspecifythehistoricalpathwayof theirorigin. Yet this obvious hypothesis,with its easily testablecardinalpremise,was notexplicitlyex- amined until 1979 after,literally,more than 2000 yearsofspeculationin theadaptivemode (both ancientauthorsand medievalbestiaries triedto inferGod's intentin creatingsuch an odd beast). Racey and Skinner(1979)foundno differencesin levels of androgenin blood plas- ma ofmale and femalespottedhyenas.Female fetusescontainedthe same highlevel of testos- teroneas adultfemales.In theothertwospecies of the familyHyaenidae, however,androgen levels in blood plasma are muchlower forfe- males thanformales. Females of thesespecies are notdominantovermalesand do notdevelop peniformclitorisesor falsescrotalsacs. We do notassertthatouralternativehypoth- esis of exaptationmustbe correct.One could runthescenarioin reverse(witha bitofforcing in our judgment):females"need" prominent genitaliaforthe meetingceremony;theybuild thembyselectionforhighandrogenlevels;large size and dominanceare a secondaryby-product

of the androgen.We raise, rathera different Lewin 1975; and Kleckner1977, all of whom

issue:whywas thisevidentalternativenotcon- sidered,especiallybyKruukin hisexcellentex- haustivebook on the species?We suggestthat

the absenceof an of exaptationhas

hypothesesin subtleand unexaminedways.

But many molecular evolutionists now stronglysuspectthat directadaptationcannot explain the existenceof all repetitiveDNA:

thereis simplytoo muchofit. The secondtra- ditionthereforeholdsthatrepetitiveDNA must existbecause evolutionneeds it so badly fora flexiblefuture-as in thefavoredargumentthat "unemployed,"redundantcopiesare freeto al- terbecausetheirnecessaryproductis stillbeing generatedbytheoriginalcopy(see Cohen 1976;

all the repetitiveDNA for(ifanything)?How did it getthere? A surveyofpreviousliterature(Doolittleand

Sapienza 1980;Gould 1981)revealstwoemerg- ing traditionsof argument,both based on the selectionistassumption that repetitiveDNA must be good for somethingif so much of it exists.One tradition(see Brittenand Davidson 1971foritslocus classicus)holdsthatrepeated copies are conventionaladaptations,selected foran immediaterolein regulation(bybringing previouslyisolatedpartsofthegenomeintonew and favorablecombinations,forexample,when repeatedcopies disperseamong several chro- mosomes).We do not doubtthatconventional adaptationexplains the preservationof much

repeatedDNA in thismanner.

also followthe firsttraditionand argue both sides). Whilewe do notdoubtthatsuch future uses are vitallyimportantconsequencesof re- peated DNA, theysimplycannotbe the cause ofitsexistence,unlesswe returntocertaintheis- tic views that permitthe controlof present eventsbyfutureneeds. This second traditionexpressesa correctin- tuitionin a patentlynonsensical(in its nonpe-

explicitlyarticulatedconcept constrainedthe rangeof our

a few

years afterWatson and Crick elucidated the

structureof DNA, many evolutionistshoped

E) The uses ofrepetitiveDNA.-For

EXAPTATION

11

jorativemeaning)manner.The missingthought thatsuppliessenseis a well articulatedconcept ofexaptation.Defendersofthesecondtradition understandhowimportantrepetitiveDNA is to

formedin a differentway (thermoregulationfor feathers,for example). Yet we traditionally apologizefor"preadaptation"in ourtextbooks, and laboriouslypointouttostudentsthatwe do notmean to implyforeordination,and thatthe wordis somehowwrong(thoughtheconceptis secure).Frazzetta(1975, p. 212), forexample,

adaptation'and dubious teleologystilllingers, and I can oftenproducea wave of nausea in some evolutionarybiologistswhen I use the wordunlessI am quick to say whatI mean by it." Indeed,thewordis wrongand ourlongstand- ing intuitivediscomfortis justified(see Lam- bert,MS). For ifwe dividetheclass offeatures contributingto fitnessintoadaptationsand ex- aptations,and ifadaptationswere constructed

then featuresworkingin one way cannot be

usage: thetermmakesno senseat all. The recognitionof exaptationsolves the di- lemmaneatly,forwhatwe now incorrectlycall "preadaptation"is merelya categoryof exap- tation consideredbeforethe fact. If feathers

evolvedforthermoregulation,theybecomeex-

aptationsforflightoncebirdstakeoff.If, how- ever, withthe hindsightof history,we choose to look at featherswhile theystillencase the running,dinosaurianancestorsof birds, then theyare onlypotentialexaptationsforflight,or preaptations(thatis, aptus-or fit-beforetheir actual cooptation).The term"preadaptation" should be dropped in favorof "preaptation." Preaptationsare potential,but unrealized,ex- aptations;theyresolveMivart'smajorchallenge to Darwin. B) Primaryexaptationsand secondaryad- aptations.-Feathers, in theirbasic design,are exaptationsforflight,but once thisnew effect was added to thefunctionof thermoregulation

as an importantsource of fitness,feathers underwenta suite of secondaryadaptations (sometimescalled post-adaptations)to enhance theirutilityin flight.The orderand arrange- mentoftetrapodlimbbonesis an exaptationfor walkingon land; manymodificationsof shape and musculatureare secondaryadaptationsfor terrestriallife. The evolutionaryhistoryofanycomplexfea-

evolution,butonlyknowtheconventionallan-

guage of adaptationforexpressingthisconvic- tion.But sinceutilityis a futurecondition(when

theredundantcopyassumesa differentfunction writes:"The associationbetweentheword'pre-

or undergoessecondaryadaptationfora new role), an impasse in expressiondevelops. To break thisimpasse,we mightsuggestthat re- peated copies are nonaptedfeatures,available forcooptationlater,but notservingany direct functionat the moment.When coopted, they will be exaptationsin theirnew role(withsec- ondaryadaptivemodificationsifaltered). Whatthenis thesourceoftheseexaptations? Accordingto the firsttradition,theyarise as

trueadaptationsand laterassumetheirdifferent (and exaptationscoopted)fortheircurrentuse,

function.The second tradition,we have ar-

gued, must be abandoned. A thirdpossibility preadaptationsto a differentand subsequent

has recentlybeen proposed(or, rather,better

codifiedafterprevioushints):perhapsrepeated copiescan originateforno adaptivereasonthat

concernsthetraditionalDarwinianlevelofphe-

notypicadvantage(Orgeland Crick1980;Doo- littleand Sapienza 1980). Some DNA elements are transposable;if these can duplicate and move,whatis tostoptheiraccumulationas long as theyremaininvisibleto the phenotype(if theybecomeso numerousthattheybeginto ex- ertan energeticconstraintuponthephenotype, thennaturalselectionwilleliminatethem)?Such "selfishDNA" maybe playingitsown Darwin- ian game at a geniclevel, but it representsa truenonaptationat thelevel ofthephenotype. Thus, repeatedDNA mayoftenariseas a non- aptation. Such a statementin no way argues

againstitsvitalimportanceforevolutionaryfu-

tures. When used to greatadvantage in that future,theserepeatedcopiesare exaptations.

VI. Significanceof Exaptation

A) A solutionto the problemofpreadapta- tion.-The conceptofpreadaptationhas always been troublingto evolutionists.We acknowl- edgeitsnecessityas theonlyDarwiniansolution toMivart's(1871)old tauntthat"incipientstages of usefulstructures"could not functionas the perfectedformsdo (whratgoodis 5% ofa wing). The incipientstages,we argue,musthave per-

12

STEPHEN JAY GOULD & ELISABETH

S. VRBA

turewillprobablyincludea sequentialmixture etymologyrequiresa differentname forpreap-

of adaptations,primaryexaptationsand sec- ondaryadaptations.Justas any featureis ple- siomorphicat one taxonomiclevel and apo- morphic at another (torsion in the class Gastropodaand in the phylumMollusca), we are not disturbedthat complexfeaturesare a mixtureof exaptationsand adaptations. Any cooptedstructure(an exaptation)will probably not arise perfectedfor its new effect.It will thereforedevelopsecondaryadaptationsforthe new role.The primaryexaptationsand second- ary adaptations can, in principle,be distin- guished. C) The sources of exaptation.-Features cooptedas exaptationshave two possiblepre- viousstatuses.Theymayhavebeenadaptations for anotherfunction,or theymay have been non-aptivestructures.The firsthas long been recognized as important,the second under-

played.Yet theenormouspool ofnonaptations tions.)This curiousnegativedefinitioncan only

must be the wellspringand reservoirof most evolutionaryflexibility.We need to recognize the centralrole of "cooptabilityforfitness"as the primaryevolutionarysignificanceof ubiq- uitousnonaptationin organisms.In thissense, and at itslevelofthephenotype,thisnonaptive pool is an analog ofmutation-a sourceofraw materialforfurtherselection. Both adaptations and nonaptations,while theymay have non-randomproximatecauses, can be regardedas randomlyproducedwithre- spectto any potentialcooptationby furtherre- gimesof selection.Simplyput: all exaptations

D) The ironyof our terminologyfor nonap-

tationsaftertheyare established.Exaptations thatbegan as nonaptationsrepresentthe miss- ing concept.They are notcoveredby theprin-

ciple of preaptation,fortheywerenotadapta- tions in ancestors.They trulyhave no name, and conceptswithoutnamescannotbe properly incorporatedin thought.The greatconfusions ofhistoricalgenesisand currentutilityprimarily involve usefulfeaturesthat were not adapta- tionsin ancestors-as in ourexamplesofsexual "mimicry"in hyenasand theuses ofmiddle-re- petitiveDNA.

tation.-It seems odd to definean important thingbywhatitis not.Studentsofearlygeology are rightlyoffendedthatwe referto 5/6 ofearth historyas Precambrian.Featuresnotnow con- tributingto fitnessare usuallycalled nonadap- tations.(In our terminologytheyare nonapta-

recorda feelingthatthesubjectis "lesser"than the thingit is not. We believethatthisfeeling is wrong,and thatthe size ofthe pool of non- aptationsis a centralphenomenonin evolution. The term"nonadaptive"is but anotherindica- tion of previous-and in our view false-con- victionsabout the supremacyof adaptation. The burden of nomenclatureis already great enoughin thispaper and we do not proposea new termforfeatureswithoutcurrentfitness. But we do wishto recordtheirony.

E) Processand state-of-being.-Evolutionary

biologistsuse the termadaptationto describe

originaterandomlywithrespecttotheireffects. both a currentstate-of-being(as discussed in

Together,thesetwo classes of characters,ad- aptationsand nonaptations,providean enor- mous pool ofvariability,at a level higherthan mutations,forcooptationas exaptations.(Lam- bert,MS, has discussedthiswithrespecttopre- adaptations only-preaptationsin our termi- nology. He explored the evolutionary

implicationsofthenotionthatforanyfunction, the past eitheras nonaptiveby-productsor as

resultingdirectlyfromnaturalselectionat any one time,theremaybe multipleeffects.) If all exaptationsbegan as adaptationsfor anotherfunctionin ancestors,we would not have writtenthispaper. For theconceptwould be coveredbytheprincipleof"preadaptation"- and we would only need to point out that "preaptation"would be a betterterm,and that

thispaper) and the processleadingto it. This dualitypresentsno problemin cases oftruead- aptation,wherea processof selectiondirectly producesthe state of fitness.Exaptations,on theotherhand, are notfashionedfortheircur- rentrole and reflectno attendantprocessbe- yond cooptation(Table 1); theywere built in

adaptationsfordifferentroles. Perhapswe shouldbeginouranalysisofpro- cess witha descriptiveapproachand simplyfo- cus upon the set of featuresthatincreasetheir relativeor absoluteabundancewithinpopula- tions,speciesor clades by theonlygeneralpro- cesses that can yield such "plurifaction,"or "moremaking":differentialbranchingor per-

EXAPTATION

13

sistence(see Arnold-and Fristrup,MS). This descriptiveprocessofplurifactionhas twobasic causes. First,featuresmay increasetheirrep- resentationactivelyby contributingto branch- ingor persistenceeitheras adaptationsevolved by selectionfortheircurrentfunction,or ex- aptationsevolvedbyanotherrouteand coopted

fortheirusefuleffect.Secondly,and particular- whichmaybe cooptedforan additionalrole,or

ly at the higherlevel of specieswithinclades,

featuresmay increasetheirown representation The paths of evolution-both the constraints

fora hostofnonaptivereasons,includingcausal

correlationwithfeaturescontributingto fitness, thesize and natureofthispool ofpotentialex-

and fortuitouscorrelationfoundat such sur-

prisinglyhighfrequencyin randomsimulations ternal" contributionthat organismsmake to

by Raup and Gould (1974). These nonaptive featuresestablishan enormous-poolforpoten- tial exaptation.

therewas one, nonethelessdeniedthatnatural selectionhad builtthehumanbrain."Savages" (living primitives),he argued, have mental equipmentequal to ours, but maintainonlya rudeand primitiveculture-thatis, theydo not use mostoftheirmentalcapacitiesand natural selectioncan onlybuildforimmediateuse. Dar- win, who was not a strictadaptationist,was

lieve thatthe failureof evolutioniststo codify bothbemusedand angered.He recognizedthe

such a conceptmustrecordan inarticulatedbe- liefin itsrelativeinsignificance. We suspect,however, that the subjects of

nonaptationand cooptabilityare ofparamount of its intricatestructure,workin an unlimited

a potentiallyinterestingstatementabout evo- lutionmusthingeupon the importanceof ex- aptation,bothin frequencyand in role.We be-

The ultimatedecisionaboutwhetherwe have writtena trivialessay on terminologyor made

VII. Conclusion

theflexibilityofphenotypiccharactersas a pri- maryenhancerof or damperupon futureevo- lutionarychange. Flexibilitylies in the pool of featuresavailable forcooptation(eitheras ad- aptationsto somethingelse thathas ceased to be importantin new selectiveregimes,as ad- aptationswhoseoriginalfunctioncontinuesbut

as nonaptationsalways potentiallyavailable).

and the opportunities-mustbe largelyset by

aptations.Exaptive possibilitiesdefinethe "in-

theirown evolutionaryfuture.

A. R. Wallace, a strictadaptationistif ever

hiddenfallacyin Wallace's argument:thatthe brain,thoughundoubtedlybuiltbyselectionfor some complexset of functions,can, as a result

importancein evolution. (When cooptability has been recognized-in the principleof "pre- adaptation"-we have focussedupon shiftin role forfeaturespreviouslyadapted forsome- thingelse,noton thepotentialforexaptationin nonaptedstructures.)The flexibilityof evolu-

tionlies in therangeofraw materialpresented cationabouthistoricalorigin.Most ofwhatthe

to processesof selection.We all recognizethis

in discussingtheconventionalsourcesofgenetic the domainof exaptation-and does not allow

variation-mutation, recombination,and so forth-presentedto naturalselectionfromthe geneticlevelbelow.But we havenotadequately appreciated that features of the phenotype

themselves(withtheirusuallycomplexgenetic tationintothecoreofourevolutionarythinking?

bases) can also act as variantsto enhanceand restrictfutureevolutionarychange. Thus the

importantstatementof Fisher's fundamental and focusattentionon currentfunctionand de-

theoremconsidersonlygeneticvariancein re-

lationto fitness:"The rateofincreasein fitness leadingus to unprovablereveriesabout primal

of any organismat any timeis equal to its ge- neticvariance in fitnessat that time" (Fisher

numberofwaysquiteunrelatedto theselective pressurethatconstructedit.Manyoftheseways mightbecomeimportant,ifnot indispensable, forfuturesurvivalin latersocial contexts(like afternoontea for Wallace's contemporaries). But currentutilitycarriesno automaticimpli-

brainnow does to enhanceour survivallies in

us to makehypothesesabouttheselectivepaths ofhumanhistory.How muchoftheevolution- ary literatureon human behaviorwould col- lapse ifwe incorporatedtheprincipleof exap-

This collapse would be constructivebecause it would vastlybroadenour rangeofhypotheses,

velopment(all testablepropositions)insteadof

fratricideon the Africansavanna or dispatch- ingmammothsat theedge ofgreatice sheets-

1958).In an analogousway,we mightconsider a valid subject,butone bettertreatedin novels

14

STEPHEN JAY GOULD & ELISABETH

S. VRBA

that can be quite enlighteningscientifically

(Kurten1980).

Consideralso theapparentlycrucialrolethat repeatedDNA has played in the evolutionof phenotypiccomplexityin organisms.If each genecodesforan indispensableenzyme(or per- formsanynecessaryfunction),asksOhno (1970) in his seminalbook, how does evolutiontran- scendmeretinkeringalongestablishedlinesand achievetheflexibilityto build new typesof or- ganization.Ohnoarguesthatthisflexibilitymust ariseas theincidentalresultofgeneduplication, withitsproductionof redundantgeneticmate-

rial: "Had evolutionbeen entirelydependent referringus to theexamplesofmantlingbehav-

upon naturalselection,froma bacteriumonly numerous forms of bacteria would have

emerged

redundantwas able toescapefromtherelentless discussedwithus theubiquitouspresence,and

pressureof naturalselection,and by escaping, it accumulatedformerlyforbiddenmutationsto

is not anti-selectionist,and we view thispaper as a contributionto Darwinism,not as a skir- mishin a nihilisticvendetta.The main theme is, afterall, cooptabilityforfitness.Exaptations are vitalcomponentsofanyorganism'ssuccess.

Acknowledgments

The followinghave commentedon themanu- script:C. K. Brain,C. A. Green,A. C. Kemp, H. E. H. Paterson.One of us (E.S.V.) owes a debttoHugh Patersonforan introduction,dur- ingextensivediscussions,to theterminologyof effects(sensuWilliams).We boththankhimfor

ior in the Black Heron and lysozyme/a-lactal- buminevolution.D. M. Lamberthas givenus access to an unpublishedmanuscript,and has

enormousimportance,in evolutionof what he and otherscall preadaptation.

Only the cistronwhich became

emergeas a new genelocus" (fromthepreface to Ohno 1970). We arguedin sectionVE thatmuch of this repetitiveDNA mayarisefornonaptivereasons at the level of the individualphenotype(as in the "selfishDNA" hypothesis).The repeated copies are thenexaptations,cooptedforfitness and secondarilyadapted for new roles. And theyare exaptationsin theinterestingcategory of structuresthatarose as nonaptations,when the"selfishDNA" hypothesisapplies. Thus, the two evolutionaryphenomenathat mayhave beenmostcrucialtothedevelopment ofcomplexitywithconsciousnesson our planet (if readerswill pardon some drippinganthro-

pocentrismforthemoment)-theprocessofcre-

atinggeneticredundancyin thefirstplace, and the myriadand inescapable consequences of buildingany computingdevice as complexas the humanbrain-may bothrepresentexapta- tions that began as nonaptations,the concept previouslymissingin our evolutionarytermi- nology.Withexamplessuch as these,the sub- ject cannotbe deemedunimportant! In short,the codificationof exaptationnot onlyidentifiesa commonflawin much evolu- tionaryreasoning-the inferenceof historical genesisfromcurrentutility.It also focussesat- tentionupon theneglectedbut paramountrole of nonaptivefeaturesin bothconstrainingand facilitatingthepathofevolution.The argument

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