Gould &Amp; Vrba 1982_Paleobiology_exaptation

8/3/2019 Gould &Amp; Vrba 1982_Paleobiology_exaptation

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Paleontological Society

Exaptation-A Missing Term in the Science of FormAuthor(s): Stephen Jay Gould and Elisabeth S. VrbaReviewed work(s):Source: Paleobiology, Vol. 8, No. 1 (Winter, 1982), pp. 4-15Published by: Paleontological SocietyStable URL: http://www.jstor.org/stable/2400563 .

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

Exaptation-a missing term n the science of formStephenJayGould and Elisabeth S. Vrba*

Abstract.-Adaptationhas beendefined nd recognized y two differentriteria: istorical enesis fea-turesbuiltbynatural election or heir resent ole)and current tilityfeatures owenhancing itnessno matter ow they rose).Biologists aveoften ailed orecognize hepotential onfusion etween hesedifferentefinitionsecause we havetended o viewnatural election s so dominantmong volutionarymechanismshathistorical rocess nd current roductbecome one. Yet ifmanyfeatures forganismsare non-adapted, ut available foruseful ooptationn descendants,hen n importantoncepthas noname in our lexicon and unnamed deas generally emainunconsidered): eatures hatnow enhancefitness utwere not builtbynatural election or heir urrent ole. We propose that suchfeatures ecalled exaptations nd thatadaptationbe restricted,s Darwin suggested, ofeatures uiltbyselectionfor heir urrent ole.We present everalexamplesofexaptation, ndicatingwhere failure o concep-tualize uch n idea limited herange fhypothesesreviouslyvailable.We explore everal onsequencesofexaptationnd propose terminologicalolution o theproblem fpreadaptation.StephenJ. Gould. Museumof Comparative oology,Harvard University, ambridge,Massachusetts02138ElisabethS. Vrba. TransvaalMuseum,Paul Kruger treet, .O. Box 413, Pretoria, outhAfricaAccepted: October15, 1981

I. IntroductionWe wish topropose term or missingtemin the taxonomy f evolutionarymorphology.

Terms nthemselves retrivial, uttaxonomiesrevisedfora differentrdering fthought renotwithoutnterest. axonomiesare not neu-tralorarbitrary at-racks or setof unvaryingconcepts; heyreflector even create)differenttheories bout the structure f the world. AsMichel Foucault has shownin severalelegantbooks 1965 and 1970, for xample),whenyouknow whypeople classifyna certainway, youunderstand owthey hink.Successive axonomies re thefossil racesofsubstantial hanges in human culture. n themid 17th entury,madmenwereconfinednin-stitutions long with the indigent nd unem-ployed, hus ending long tradition fexile ortoleration or he nsane.But what is thecom-mon ground or taxonomy hatmixes hemadwith the unemployed-an arrangement hatstrikesus as absurd. The "keycharacter"forthe "higher axon,"Foucaultargues, was idle-ness, the cardinalsin and danger n an age on

thebrinkofuniversalcommerce nd industry* Anequal timeproduction; rder fauthorshipwas de-termined ya transoceanic oin flip.

(?) 1982 The Paleontological ociety.All rights eserved.

(Foucault's interpretationas been challengedbyBritishhistorian fscienceRoyPorter,MS).In othersystems f thought,what seems pe-ripheral o us becomescentral, nd distinctionsessential o us do notmatterwhetherdlenessis internallynevitable, s ininsanity, r exter-nally mposed, s in unemployment).II. Two Meanings ofAdaptation

In thevernacular, nd insciences ther hanevolutionary iology, hewordadaptationhasseveralmeanings all consistentwith the ety-mology fad + aptus,ortowards fit for par-ticularrole). When we adapt a tool for a newrole, we change tsdesign onsciously o that twill workwell n itsappointed ask. Whencre-ationists eforeDarwin spokeof adaptation-for the term long precedes evolutionarythought-they eferredo God's intelligentc-tion in designing rganisms or definite oles.When physiologistslaim that arger ungs ofAndeanmountain eoples are adapted to localclimates, hey pecify irectedhangeforbetterfunction.n short, ll thesemeaningsrefer ohistoricalprocessesof change or creationfordefiniteunctions. he "adaptation" sdesignedspecificallyor hetask tperforms.In evolutionarybiology,however, we en-

0094-83 73/82/0801-0002/$100


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EXAPTATION 5TABLE 1. A taxonomy f fitness.

Process Character UsageNatural selection hapes the character adaptation functionfor current se-adaptationA character, reviously haped by natural electionfor particular unctionan adaptation), s coopted aptationfor new use-cooptation exaptation effectA characterwhoseorigin annotbe ascribed o the direct ctionof natural election a nonaptation),s cooptedfor current se-cooptation

counter wo different eanings-and a possibleconflation f concepts-forfeatures alled ad-aptations.The firsts consistentwiththe ver-nacular usages cited above: a feature s an ad-aptation nly f twas builtby natural electionforthe function t now performs. he seconddefines daptationna static, r mmediatewayas anyfeature hatenhances urrentitness, e-gardless of its historical rigin. As a furtherconfusion, daptationrefers othto a processand a state of being. We are onlydiscussingstateofbeinghere-that is, features ontribut-ingto fitness.We include omecommentsboutthisfurther roblemn sectionVIE.)Williams, n his classicbook on adaptation,recognized hisdilemma nd restrictedhe termto its first, r narrower,meaning.We shouldspeak ofadaptation,he argues, onlywhenwecan "attribute heorigin nd perfectionf thisdesignto a long periodof selectionfor effec-tivenessn this particular ole" 1966, p. 6). Inhis terminology,function" efers nlyto theoperation f adaptations.Williamsfurther r-guesthatwe mustdistinguish daptations ndtheir unctions rom ortuitousffects. e uses"effect" n its vernacular sense-somethingcaused or produced,a resultor consequence.Williams' oncept f"effect"maybe appliedtoa character, rtoitsusage,or toa potentialorprocess), arising s a consequenceof true ad-aptation. Fortuitous ffect lways connotes aconsequencefollowing accidentally," nd notarising irectlyrom onstructionynatural e-lection.Othershave adopted various spects ofthis terminologyor "effects" ensu Williams(Paterson 1981; Vrba 1980; Lambert, MS).However, Williams and othersusually nvokethetermeffect' o designate heoperation f a

usefulcharacternot built by selectionfor tscurrent ole-and we shall followthisrestric-tion here (Table 1). Williams also recognizesthatmuchhaggling bout adaptationhas been"encouragedby imperfectionsf terminology"(1966, p. 8), a situation hatwehope toalleviateslightly.Bock, on theotherhand,champions he sec-ond, or broader,meaning n the othermostwidely-citednalysis of adaptation fromthe1960's Bockand vonWahlert 965;Bock 1967,1979, 1980). "An adaptation s, thus, a featureof theorganism,which nteracts perationallywith omefactor f tsenvironmento thattheindividualsurvivesand reproduces"1979, p.39).The dilemmaofsubsuming ifferentriteriaof historical enesis nd current tility nderasingle ermmaybe illustrated ith neglectedexamplefrom famous ource. n his chapterdevoted o"difficultiesntheory," arwinwrote(1859,p. 197):

The suturesn theskullsofyoungmammalshavebeen advanced as a beautifuldaptationfor idingparturition,nd no doubttheyfa-cilitate, rmaybe indispensable or hisact;but as suturesoccur in the skullsof youngbirds nd reptiles,whichhaveonly oescapefrom brokenegg, we may infer hat thisstructure as arisenfrom he aws ofgrowth,and has beentakenadvantageof n thepar-turition fthe higher nimals.

Darwin asserts heutility,ndeedthenecessity,ofunfused uturesbutexplicitlyeclinesto la-bel them n adaptationbecause theywerenotbuiltbyselection ofunction s theynow do inmammals.WilliamsfollowsDarwin and would


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6 STEPHEN JAY GOULD & ELISABETH S. VRBA

decline to call this feature n adaptation; hewould designate ts rolein aidingthe survivalof mammals as a fortuitous ffect.But Bockwould call the sutures nd the timing f theirfusion n adaptation, nd a vital one at that.As an example of unrecognized onfusion,consider hisdefinitionf adaptation rom bi-ologicaldictionaryAbercrombiet al. 1951, p.10): "Any characteristic f living organismswhich, in the environmenthey nhabit, m-provestheir hances of survival nd ultimatelyleaving descendants, n comparisonwith thechances of similar rganismswithout he char-acteristic;natural selectionthereforeends toestablish daptationsna population. Thisdef-inition onflates urrent tilitywith historicalgenesis.What is to be done with useful truc-turesnotbuiltby natural election or heir ur-rentrole?

III. A Definition f ExaptationWe have identified onfusion urroundingone of thecentral onceptsnevolutionaryhe-ory.This confusionrises, n part,becausethetaxonomy f formn relation o fitnessacks aterm. ollowingWilliams see Table 1), we may

designate s an adaptation nyfeaturehatpro-motesfitness nd was builtby selection or tscurrentole criterionfhistorical enesis).Theoperation f n adaptation s its unction. Bockuses the termfunction omewhat differently,butwe believewe are following he biologicalvernacularhere.) We may also followWilliamsin labelling he operation f a useful haracternotbuiltby selection or tscurrent ole as aneffect.We designate s an effectnly heusageofsuch a character, otthecharactertself, eep. 5.) But what is the unselected, ut usefulcharacter tself o be called? Indeed it has norecognized ame unlesswe acceptBock's broaddefinitionf adaptation-the criterion f cur-rentutility lone and rejectbothDarwin andWilliams). ts space on the ogicalchart s cur-rently lank.We suggest hat uchcharacters,volved forother sages orfornofunctiontall), and later"coopted"fortheircurrent ole,be called ex-aptations. See VIA on therelated concept of"preadaptation.") hey are fit or heir urrentrole,henceaptus,but theywere not designedfor t,and arethereforeot d aptus,orpushed

towardsfitness. hey owe their itness o fea-tures present orotherreasons, nd are there-fore it aptus) byreasonof ex) their orm, rexaptus. Mammalian utures re anexaptationforparturition.daptations ave functions; x-aptationshave effects. he general, taticphe-nomenon fbeingfit houldbe called aptation,notadaptation. The set of aptations xisting tany one timeconsists f two partially verlap-ping subsets: he subsetofadaptations nd thesubset ofexaptations.This also applies to themore nclusive etofaptations xisting hroughtime; ee Table 1.)IV. The CurrentNeed forConceptofExaptation

Whyhas thisconflationfhistorical enesiswithcurrent tilityttractedo little ttentionheretofore? very biologistsurely recognizesthat ome useful haracters id not arisebyse-lection or heir urrent oles;whyhave we nothonored hatknowledgewith name?Does ourfailureto do so simplyunderscore he unim-portanceof the subject?Or might hisabsentterm, n Foucault'ssense,reflect conceptualstructurehat xcluded t?And,finally,oesthepotentialneedfor ucha term t this time n-dicate thattheconceptual tructuretselfmaybe altering?Whydid Williamsnotsuggest term, incehe clearly ecognized heproblem nd did sep-arate usages intofunctions nd effectscorre-sponding espectivelyoadaptations nd to theunnamed featuresthat we call exaptations)?WhydidBockfailtospecifyheproblem t all?We suspectthat the conceptualframework fmodern evolutionary hought,by continuallyemphasizinghesupreme mportancend con-tinuityfadaptation ndnatural election t alllevels, subtly elegated he issue of exaptationto a periphery f unimportance.How couldnonadaptive spectsofform aina properhear-ingunder Bock's definition1967, p. 63): "Ontheoretical rounds, ll existing eatures fan-imals are adaptive. If theywerenotadaptive,then heywould be eliminated yselection ndwoulddisappear."Williams ecognizedhephe-nomenonof exaptationand even granted tsomeimportancein assessing hecapacitiesofthehumanmind,for xample),but he retaineda preeminentolefor daptation nd often es-


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EXAPTATION 7ignated effects s fortuitous r peripheral-"merely n incidental onsequence"he states nonepassage (p. 8).We believethat headaptationistrogram fmodernevolutionaryhought Gould and Le-wontin1979)has beenweakening s a result fchallenges rom ll levels, molecules o macro-evolution.At the biochemical evel, we havetheories fneutralism nd suggestionshat ub-stantial mountsofDNA may be nonadaptiveat the evel of thephenotypeOrgeland Crick1980;Doolittle nd Sapienza 1980).Students fmacroevolutionave argued hat daptations npopulations ranslates effectsoyield hepat-ternsof differentialpeciesdiversificationhatmayresultn evolutionary rendsVrba's effecthypothesis, 980). If nonadaptation or whatshouldbe callednonaptation)sabouttoassumean importantole na revised volutionaryhe-ory,then ourterminologyf formmustrecog-nize its cardinal evolutionary ignificance-cooptability or fitnesssee Seilacher 1972, onimportantffects f a nonaptive atternn thestructurend coloration fmolluscs).Some colleagueshave said thatthey preferBock'sbroad definitionecause t s more asilyoperational.We can observe nd experimentodeterminewhatgood a feature oes for n or-ganismnow.To reconstructhehistorical ath-way of its origin s always more difficultndoftenwhencrucial vidence smissing)ntract-able.To thiswe replythat we are not trying odismantle ock'sconcept.Wemerely rguethatit should be called aptation withadaptationand exaptation s its modes). As aptation, tretains ll the favorableproperties or testingenumerated bove.Historical genesis is, undoubtedly, . moredifficultroblem utwe cannot hereforegnoreit. As evolutionists, e are charged, lmost bydefinition,o regardhistorical athways s theessenceof oursubject.We cannotbe indifferentto the factthat imilar esults an arisebydif-ferent istorical outes.Moreover, he distinc-tionbetween d- and exaptation, oweverdif-ficult, s not unresolvable. f we ever findasmallrunning inosaur, ncestral o birdsandclothedwithfeathers,we willknow thatearlyfeatherswereexaptations, otadaptations, orflight.

V. ExamplesofExaptationA) Feathersandflight-sequentialxaptationin theevolution fbirds.-Consider a commonscenario rom he volution fbirds. Wedonotassert tscorrectness, utonlywishto examineappropriate erminology ora commonset ofhypotheses.)Skeletal features, ncluding thesternum, ibbasket and shoulderoint, n lateJurassicfossilsofArchaeopteryxndicatethatthisearliestknownbirdwas probably apableofonlythesimplest eats offlight. et it wasquitethoroughlyeathered. his has suggestedto manyauthors that selectionforthe initialdevelopment ffeathersn an ancestorwas forthe function f insulationand not for flight

(Ostrom1974,1979;Bakker1975).Sucha fun-damental innovationwould, of course, havemanysmall as well as far-reaching,ncidentalconsequences.For example,along no descen-dant lineageof thisfirst eatheredpecies did(so far s we know) furryovering fthebodyevolve. The fixationarly nthe ifeofthe em-bryo,of cellularchanges that ead on theonehandto hair,and on theother ofeathers, on-strained hesubsequent ourseofevolution nbodycoveringOster1980).Archaeopteryxlreadyhad arge ontour-typefeathers,rranged long its arms in a patternverymuch as in the wings of modernbirds.Ostrom 1979, p. 55) asks: "Is it possible thatthe initial pre-Archaeopteryx)nlargement ffeatherson those narrow hands might havebeento increase hehandsurface rea, therebymaking t moreeffectiven catching nsects?"He concludes 1979, p. 56): "I do believethatthe predatory esignof the wing skeleton nArchaeopteryxs strongevidence of a priorpredatoryunction f theproto-wingn a cur-sorialproto-Archaeopteryx.Laterselection orchanges n skeletalfeatures nd feathers, ndfor pecific euromotoratterns,esultedntheevolution fflight.The Black Heron (or Black Egret,Egrettaardesiaca) of Africa, ike most modernbirds,uses itswings nflight. ut italso uses them nan interesting ay to preyon small fish: "Itsfishings performedtandingn shallow waterwithwings tretched ut and forward, ormingan umbrella-likeanopywhichcasts a shadowon the water. n thiswayitsfood can be seen"


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(McLachlan and Liversidge 1978, p. 39, Plate6). This "mantling" f the wings ppears to bea characteristicehaviorpattern,with geneticbasis. The wingand feather tructures hem-selvesdo not eemto be modifiedncomparisonwith those of closelyrelated pecies,the indi-viduals of whichdo not hunt nthisway A. C.Kemp, pers. comm.).We see, in thisscenario, sequential et ofadaptations, ach converted o an exaptation fdifferentffecthat sets the basis for a subse-quent adaptation.By this interplay, majorevolutionaryransformationccursthat proba-bly could not have arisen by purely ncreasingadaptation. Thus, the basic designof feathersis an adaptationfor hermoregulationnd, lat-er, an exaptation orcatchingnsects.The de-velopment f large contour eathers nd theirarrangementnthearm arise s adaptations orinsect catching and become exaptations forflight.Mantlingbehavioruses wings hataroseas an adaptationforflight.The neuromotormodificationsoverningmantling ehavior, ndthereforehemantling osture, re adaptationsforfishing. he wing perse is an exaptationnits current ffect fshading, ust as the featherscoveringtalso arose ndifferentdaptivecon-texts uthaveprovidedmuch volutionarylex-ibilityfor otheruses during the evolution ofbirds.B) Bone as storage nd support.-The devel-opment f bone was an eventofmajorsignifi-cance in the evolution fvertebrates.Withoutbone,vertebratesouldnothave later akenuplife on land. Halstead (1969) has investigatedthe question: grantingts subsequent mpor-tance as body support n the ater evolution fvertebrates,whydid bone evolve at such anearly tage nvertebrate istory?ome authorshave hypothesized hat bone initially rose asan osmoregulatoryesponse o life n freshwa-ter.Others, ikeRomer 1963), postulate nitialadaptation of bony "armor" for a protectivefunction. autard 1961, 1962) pointed ut thatanyorganism ithmuchmuscularctivity eedsa convenientlyccessible storeof phosphate.Following Pautard, and notingthe seasonalcycleofphosphate vailabilityn thesea, Hal-stead (1969) suggested he following cenario:Calciumphosphates,aid down in the skinoftheearliestvertebrates,volved nitially s an

adaptationforstoringphosphatesneeded formetabolic activity.Only considerablyater inevolution idbone replace he cartilaginous n-doskeleton nd adopt the function f supportforwhich tis nowmostnoted.Thus, bone has two major uses nextant er-tebrates: upport/protectionndstorage/homeo-stasis as a storehouse or ertainmineral ons,includingphosphate ons). The ions in verte-bratebone are in equilibriumwith hose n tis-sue fluids nd blood, and function n certainmetabolic activities Scott and Symons 1977).For instance, n humans, 90% of body phos-phorus s present n the norganic hase of bone(Duthie and Ferguson1973).FollowingHalstead's analysis, hedepositionofphosphate n bodytissues riginallyvolvedas an adaptationfora storage/metabolicunc-tion.The metabolicmechanism orproducingbone per se can thusbe interpreteds an ex-aptationfor support.The metabolic mecha-nismsfordepositing n increasedquantityofphosphates nd for mineralization, s well asthearrangementfbony lementsnan internalskeleton, re then daptations or upport.C) The evolution f mammalianactation.-

Dickerson and Geis (1969) recounthow Alex-anderFleming,n 1922,discovered heenzymelysozyme. e had a cold and, for nterest'sake,added a fewdropsofnasalmucus o a bacterialculture.To his surprisehe found, fter fewdays, thatsomethingn the mucus was killingthebacteria: heenzyme ysozyme,incefoundinmostbodily ecretionsnd in argequantitiesin the whites f eggs. Lysozyme estroysmanybacteriaby ysing, rdissolving,hemucopoly-saccharide tructurefthecellwall. The aminoacid sequenceofa-lactalbumin, milkproteinofpreviouslynknown unction, as then oundto be so close to that of lysozyme, hatsomerelationshipof close homologymust be in-volved. Dickersonand Geis (1969, pp. 77-78)write:a-Lactalbuminby tself s not an enzyme utwas found obe onecomponentfa two-pro-tein actose synthetase ystem, resent nlyin mammaryglands during actation . ..The other omponent the"A" protein)hadbeen discoverednthe iver nd other rgansas an enzyme or he ynthesisfN-acetyllac-


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EXAPTATION 9

tosamine romgalactoseand NAG. But thecombination f theA protein nd a-lactal-bumin ynthesizeshemilk ugar actosefromgalactoseand glucose nstead.The non-cat-alytic -lactalbumin videntlycts as a con-troldevicetoswitch tspartner rom nepo-tential ynthesiso another ... It appearsthatwhen milk-producing-systemas beingdevelopedduring he evolution fmammals,and when a need fora polysaccharide-syn-thesizing nzymearose, a suitableone wasfoundin part by modifying pre-existingpolysaccaride-cuttingnzyme.Thus, lysozyme,n all vertebratesn which

it occurs, s probablyn adaptation or hefunc-tion of killingbacteria. Further volution nmammals alteration f a duplicatedgene ac-cording o Dickersonand Geis, 1969) resultedin a-lactalbumin,n adaptation togetherwiththeA protein) orthe function flactose syn-thesisand lactation.Human lysozyme,n thisscenario,is an adaptationfor ysingthe cellwalls of bacteria,and an exaptationwithre-specttothe actosesynthetaseystem.D) Sexual "mimicry"n hyenas.-Females ofthespottedhyena,Crocutacrocuta,are largerthanmalesanddominant verthem.Pliny, ndother ncientwriters, ad alreadyrecognizedrelated nd unusualfeature ftheirbiology ncallingthem hermaphroditesfalsely, s Aris-totle howed).The external enitalia ffemalesare virtuallyndistinguishablerom he sexualorgans fmalesbysight.The clitoriss enlargedand extendedto forma cylindrical tructurewith narrow lit t itsdistal nd; t s nosmall-erthanthemale'spenis ndcanalso be erected.The labia majora are foldedover and fusedalong the midline to form false scrotalsac(thoughwithouttesticles f course),virtuallyidentical n form nd positionwiththe male'sscrotumHarrisonMatthews1939).The literaturenthis exual"mimicry"sfullof speculations bout adaptivemeaning.Mostofthesearguments ave conflatedurrent til-ityand historical enesis n assuming hat thedemonstrationf modernuse (Bockian adap-tation) pecifies hepath of origin adaptationas used byWilliamsand Darwin, and as ad-vocated n thispaper).We suggest hatthe ab-senceof n articulatedoncept f xaptation as

unconsciouslyorced revious uthors ntothiserroneous onceptualbind.Kruuk 1972), the eading student f spottedhyenas,for example, notes that the enlargedsexual organsof females re used in an impor-tant behaviorknowas the meeting eremony.Hyenas spend ongperiods s solitarywander-ers searching or carrion,butthey lso live inwell integratedlans that defend erritoryndengage ncommunalhunting. mechanism orreintegratingolitarywanderersnto heir rop-erclan mustbe developed. n themeeting er-emony, wo hyenas tandsideto side,facing noppositedirections. ach lifts he insidehindleg, exposingn erect enisor clitoriso tspart-ner's eeth.Theysniff nd lick each other's en-itals for10 to 15 seconds, argely t the base ofthe penisor clitoris nd infrontf the scrotumorfalse scrotum.Having discovered current tility ortheprominentxternal enitalia ffemales,Kruuk(1972, pp. 229-230) infers hattheymusthaveevolvedfor hispurpose:

It is impossible o think f any otherpurposefor his pecialfemalefeaturehanforuse inthe meeting eremony . . It mayalso be,then,that an individualwitha familiar utrelativelyomplex nd conspicuous tructuresniffed t during hemeeting as an advan-tage over others;the structurewould oftenfacilitatehis reestablishmentf social bondsby keeping partners ogether ver a longermeetingperiod.This could be the selectiveadvantage that has caused the evolutionofthefemales' nd cubs' genital tructure.Yet another hypothesis,based upon factsknown to everyBiology I student,virtuallycriesoutforrecognition.he penisand clitorisare homologous rgans, s are the scrotumndlabia majora. We knowthathigh evelsofan-drogen nduce the enlargementf the clitorisand thefoldingverand fusion fthe abia untilthey esemble enis ndscrotal ac respectively.(In fact, n an importantense,they re thenpenis and scrotalsac, giventhe homologies.)Human baby girlswithunusually nlarged d-

renals secretehigh evels of androgen, nd arebornwith peniformlitoris nd an empty cro-tal sac formed f the fused abia.Female hyenas are largerthan males and


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dominant ver them. Since thesefeatures reoften ormonally ediatednmammals, houldwe notconjecture hatfemales ttaintheir ta-tus by secretingndrogens nd that the peni-form litoris ndfalse crotal ac areautomatic,secondaryby-products. ince they re formedanyway, later nd secondary tilitymight n-sue; theymay be coopted to enhancefitnessnthe meeting ceremony nd then secondarilymodified or hisnewrole. We suggest hat thepeniformlitoris nd falsescrotal ac arose asnonaptive onsequences f high ndrogenevels(a primary daptationrelatedto the unusualbehavioral oleoffemales). heyare, therefore,exaptations or hemeetingeremony,nd theireffectn enhancingfitness hrough hat cere-monydoesnot specify hehistorical athway ftheir rigin.Yet thisobvioushypothesis,with ts easilytestable ardinalpremise,was notexplicitlyx-amined until 1979 after, iterally,more than2000 yearsofspeculationnthe adaptive mode(both ancient authors and medieval bestiariestriedto inferGod's intentn creating uch anodd beast).Raceyand Skinner1979)foundnodifferencesn levelsofandrogenn bloodplas-ma of male and female pottedhyenas.Femalefetuses ontained he samehigh evelof testos-terone s adultfemales.n theother wospeciesof the familyHyaenidae, however, androgenlevels in blood plasma are much owerfor fe-males than formales. Females of thesespeciesare notdominant vermales and do notdeveloppeniformlitorises r false scrotal acs.We do not assert hatour alternative ypoth-esis of exaptationmust be correct.One couldrunthe cenarionreverse with bitofforcingin our judgment):females "need" prominentgenitaliaforthemeeting eremony; heybuildthemby election orhigh ndrogenevels; argesize and dominance re a secondary y-productof the androgen.We raise, rather differentissue: whywas this vident lternative ot con-sidered, specially yKruuk nhisexcellentx-haustivebook on thespecies?We suggest hatthe absenceof an explicitlyrticulatedonceptofexaptationhas constrainedherangeof ourhypothesesn subtle nd unexaminedways.E) The uses of repetitive NA.-For a fewyears afterWatson and Crick elucidated thestructure f DNA, many evolutionists oped

thatthearchitecture fgeneticmaterialmightfit ll theirpresuppositionsbout evolutionaryprocesses.The linear rder fnucleotidesmightbe the beads on a string f classical genetics:one gene, one enzyme; nenucleotideubstitu-tion,oneminute lteration ornatural electionto scrutinize.We are now, not even 20 yearslater,facedwithgenes npieces,complexhier-archies of regulation and, above all, vastamountsofrepetitive NA. Highlyrepetitive,orsatellite, NA can exist nmillions fcopies;middle-repetitiveNA, with ts ens ohundredsof copies,forms bout one quarterof the ge-nome in bothDrosophila and Homo. What isall therepetitive NA for ifanything)? owdid itgetthere?A survey fprevious iteratureDoolittle ndSapienza 1980;Gould 1981)reveals woemerg-ing traditions f argument, othbased on theselectionist ssumptionthat repetitiveDNAmustbe good forsomething f so much of itexists.One traditionsee BrittenndDavidson1971for ts ocusclassicus)holds thatrepeatedcopies are conventional daptations, selectedfor n immediate ole nregulationbybringingpreviouslysolatedparts fthegenomentonewandfavorable ombinations, or xample,whenrepeatedcopies disperseamongseveral chro-mosomes).We do not doubtthatconventionaladaptationexplains the preservation f muchrepeatedDNA in thismanner.But many molecular evolutionists nowstronglyuspectthatdirect daptation cannotexplain the existence of all repetitiveDNA:there s simply oo muchof t. The second tra-dition herefore oldsthatrepetitiveNA mustexistbecause evolutionneeds it so badlyforaflexible uture-as inthefavored rgumenthat"unemployed," edundant opiesare free o al-terbecause their ecessary roducts stillbeinggenerated ytheoriginal opy seeCohen 1976;Lewin 1975; and Kleckner1977, all ofwhomalso follow the first radition nd argue bothsides).Whilewe do not doubtthat uchfutureuses are vitally mportant onsequencesof re-peatedDNA, they imply annot be thecauseof tsexistence, nlesswe returnocertain heis-tic views that permitthe control of presenteventsbyfuture eeds.This secondtraditionxpresses correctn-tuitionn a patently onsensical in itsnonpe-


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EXAPTATION 11

jorativemeaning)manner.Themissing houghtthat supplies ense s a well articulatedonceptof exaptation. efenders f the econdtraditionunderstand ow mportant epetitiveNA is toevolution, ut onlyknow the conventionalan-guage ofadaptationfor xpressinghis convic-tion.But sinceutilitys a future onditionwhentheredundantopy ssumes differentunctionor undergoes econdary daptationfora newrole), an impasse in expressiondevelops. Tobreakthis mpasse,we might uggest hatre-peated copies are nonaptedfeatures, vailableforcooptationater,butnot serving nydirectfunction t the moment.When coopted, theywill be exaptationsn theirnew role withsec-ondary daptive modificationsfaltered).What then s thesourceofthese xaptations?According o the first radition, hey arise astrue daptations ndlater ssume heir ifferentfunction.The second tradition,we have ar-gued,must be abandoned. A thirdpossibilityhas recently een proposed or, rather,bettercodified fter revioushints): erhapsrepeatedcopiescan originate orno adaptivereasonthatconcerns hetraditional arwinian evelofphe-notypicdvantage OrgelandCrick 1980;Doo-little nd Sapienza 1980). SomeDNA elementsare transposable; f these can duplicate andmove,what s to stop heir ccumulations longas theyremain nvisibleto the phenotype ifthey ecome o numerous hat hey egin o ex-ert n energeticonstraintponthephenotype,thennatural electionwilleliminate hem)? uch"selfish NA" maybe playingts own Darwin-ian game at a genic evel, but it representstruenonaptationt the evel ofthephenotype.Thus, repeatedDNA may often rise as a non-aptation.Such a statementn no way arguesagainst ts vital mportance or volutionaryu-tures. When used to greatadvantage in thatfuture,heserepeated opiesareexaptations.VI. Significancef Exaptation

A) A solution to theproblem f preadapta-tion. The concept fpreadaptation as alwaysbeen troubling o evolutionists.We acknowl-edge tsnecessitys theonlyDarwinian olutiontoMivart's 1871)oldtaunt hat incipienttagesof useful tructures" ould notfunction s theperfectedorms o (whrat ood s 5% of a wing).The incipient tages,we argue,musthave per-

formedna differentay thermoregulationorfeathers,for example). Yet we traditionallyapologizefor preadaptation"nourtextbooks,and laboriously oint uttostudents hatwe donotmeanto imply oreordination,nd that theword s somehowwrong though he concept ssecure). Frazzetta 1975, p. 212), forexample,writes: The association etween heword pre-adaptation' and dubiousteleologytill ingers,and I can oftenproduce a wave of nausea insome evolutionary iologistswhen I use theword unless am quick to saywhat meanbyit."Indeed,theword swrong nd our ongstand-ing intuitive iscomforts justified see Lam-bert,MS). For ifwe divide the classof featurescontributingo fitnessntoadaptations nd ex-aptations, nd ifadaptationswereconstructed(and exaptationsoopted)for heir urrent se,thenfeaturesworking n one way cannot bepreadaptations o a differentnd subsequentusage: the termmakesno sense at all.The recognitionf exaptation olves the di-lemmaneatly, orwhat we now ncorrectlyall"preadaptation" s merely category f exap-tationconsideredbeforethe fact. If feathersevolved for hermoregulation,heybecome ex-aptations or lightncebirds ake off. f,how-ever,with thehindsightfhistory,we chooseto look at featherswhile they till encase therunning, inosaurianancestors f birds,thenthey reonlypotential xaptations or light,rpreaptationsthat s, aptus-or fit-before heiractual cooptation).The term"preadaptation"should be droppedin favor of "preaptation."Preaptations re potential, ut unrealized, x-aptations; hey esolveMivart'smajor challengeto Darwin.B) Primaryexaptations nd secondaryad-aptations.-Feathers,in their asic design,areexaptations orflight, ut once thisnew effectwas added to thefunction fthermoregulationas an importantsource of fitness,feathersunderwent suite of secondaryadaptations(sometimesalled post-adaptations)o enhancetheirutilityn flight.The order and arrange-ment ftetrapodimbbones s an exaptation orwalkingon land; manymodificationsf shapeand musculature re secondarydaptations orterrestrialife.The evolutionaryistoryfanycomplexfea-


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12 STEPHEN JAY GOULD & ELISABETH S. VRBAturewill probably nclude sequentialmixtureof adaptations, primary xaptations nd sec-ondary daptations.Just s any feature s ple-siomorphic t one taxonomic evel and apo-morphic at another (torsion in the classGastropoda and in the phylumMollusca), weare not disturbed hat complexfeatures re amixture f exaptations nd adaptations. Anycoopted tructurean exaptation)will probablynot arise perfected or its new effect. t willthereforeevelop secondary daptations or henew role. The primary xaptations nd second-ary adaptations can, in principle,be distin-guished.C) The sources of exaptation.-Featurescoopted as exaptationshave two possible pre-vious statuses. hey mayhave been adaptationsforanotherfunction, r they may have beennon-aptive tructures. he first as long beenrecognized as important, he second under-played. Yet the enormous ool of nonaptationsmustbe the wellspring nd reservoir f mostevolutionary lexibility.We need to recognizethe centralrole of "cooptability orfitness" sthe primary volutionary ignificance f ubiq-uitous nonaptationn organisms.n thissense,and at its evel of thephenotype,hisnonaptivepool is an analogof mutation-a sourceofrawmaterial orfurtherelection.Both adaptations and nonaptations,whiletheymayhave non-random roximate auses,can be regarded s randomly roducedwithre-spectto any potential ooptation yfurther e-gimes of selection.Simplyput: all exaptationsoriginate andomlywithrespect o their ffects.Together, hese two classes of characters, d-aptationsand nonaptations, rovidean enor-mouspool ofvariability,t a levelhigher hanmutations,or ooptations exaptations. Lam-bert,MS, has discussed hiswith espect opre-adaptations only-preaptations n our termi-nology. He explored the evolutionaryimplications fthe notion hatfor ny function,resulting irectly romnatural election t anyone time, heremaybe multiple ffects.)If all exaptationsbegan as adaptationsforanotherfunctionn ancestors,we would nothave writtenhispaper. For the conceptwouldbe covered ytheprinciplef"preadaptation"-and we would only need to point out that"preaptation"wouldbe a better erm, nd that

etymologyequires differentame forpreap-tations fter hey re established.Exaptationsthat beganas nonaptations epresent hemiss-ing concept.Theyare notcoveredby theprin-ciple ofpreaptation, or heywere notadapta-tions n ancestors.They trulyhave no name,and conceptswithout amescannotbe properlyincorporatedn thought.The great confusionsofhistorical enesis ndcurrenttilityrimarilyinvolveusefulfeatures hat were not adapta-tions nancestors-as inourexamples fsexual"mimicry"n hyenas nd the uses ofmiddle-re-petitive NA.D) The ironyofour terminologyornonap-tation.-It seems odd to define n importantthing ywhat t s not.Students f arlygeologyarerightlyffended hatwe refero 5/6 ofearthhistory s Precambrian. eaturesnotnow con-tributing o fitness re usuallycallednonadap-tations. In our terminologyhey re nonapta-tions.)This curiousnegative efinitionan onlyrecord feelinghatthe subject s "lesser" hanthething t is not.We believethat thisfeelingis wrong, nd that thesize of the pool ofnon-aptationss a central henomenonnevolution.The term nonadaptive" s butanother ndica-tionofprevious-and in our view false-con-victionsabout the supremacyof adaptation.The burdenof nomenclature s alreadygreatenough n thispaper and we do notproposeanew termforfeatureswithout urrent itness.But we do wishto record he rony.E) Process and state-of-being.Evolutionarybiologistsuse the termadaptationto describeboth a current tate-of-beingas discussedinthispaper) and theprocess eadingto it. Thisduality resents oproblemncases oftrue d-aptation,wherea processof selectiondirectlyproducesthe stateof fitness. xaptations,onthe otherhand,are notfashioned or heir ur-rentrole and reflect o attendant rocess be-yondcooptationTable 1); theywere built inthepast either s nonaptiveby-productsr asadaptations ordifferentoles.Perhapswe shouldbeginouranalysis fpro-cesswith descriptivepproach nd simply o-cus uponthe set offeatureshat ncreasetheirrelativeor absolute abundance withinpopula-tions, peciesorclades bytheonlygeneralpro-cesses that can yield such "plurifaction," r"moremaking":differentialranching r per-


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EXAPTATION 13

sistence see Arnold- nd Fristrup,MS). Thisdescriptiverocess f plurifactionas two basiccauses. First, featuresmay increasetheirrep-resentationctivelyby contributingo branch-ing orpersistence ither s adaptations volvedby selectionfortheircurrent unction, r ex-aptations volvedby another oute nd cooptedfor heir seful ffect. econdly, nd particular-ly at thehigher evel of specieswithin lades,featuresmayincrease heir wn representationfor hostofnonaptive easons, ncluding ausalcorrelation ithfeatures ontributingo fitness,and fortuitousorrelation ound at such sur-prisinglyighfrequencyn random imulationsby Raup and Gould (1974). These nonaptivefeatures stablish n enormous-poolorpoten-tial exaptation.VII. Conclusion

The ultimate ecision boutwhether e havewritten trivial ssayon terminologyr madea potentiallynterestingtatementbout evo-lutionmust hinge upon theimportance f ex-aptation,both nfrequencynd inrole. We be-lieve thatthe failureof evolutionistso codifysucha conceptmustrecord n inarticulated e-lief n itsrelative nsignificance.We suspect,however,that the subjects ofnonaptationnd cooptabilityre ofparamountimportance n evolution. (When cooptabilityhas been recognized-in theprinciple f "pre-adaptation"-we have focussedupon shift nrolefor features reviouslydapted for some-thing lse, noton thepotential or xaptationnnonaptedstructures.) he flexibilityf evolu-tion ies in therangeof rawmaterial resentedto processes f selection.We all recognize hisindiscussingheconventionalources f geneticvariation-mutation, recombination, nd soforth-presentedo natural selection rom hegeneticevel below.Butwehave not dequatelyappreciated that featuresof the phenotypethemselves withtheirusually complexgeneticbases) can also act as variants o enhance andrestrict uture volutionary hange. Thus theimportant tatement f Fisher's fundamentaltheorem onsiders nly geneticvariance n re-lationtofitness:The rateof ncrease n fitnessofany organism t anytime s equal to itsge-neticvariance in fitness t that time" Fisher1958). n an analogous way,we might onsider

theflexibilityfphenotypicharacters s a pri-maryenhancer f or damper uponfuture vo-lutionary hange.Flexibilityies in the pool offeatures vailable forcooptationeither s ad-aptations o something lse that has ceased tobe importantn new selectiveregimes, s ad-aptationswhoseoriginal unctionontinues utwhichmaybe cooptedfor n additional ole,oras nonaptations lways potentiallyvailable).The paths of evolution-both the constraintsand theopportunities-must e largely et bythesize and nature fthispool ofpotential x-aptations.Exaptive possibilities efine he"in-ternal" contributionhat organismsmake totheir wnevolutionaryuture.A. R. Wallace, a strict daptationist fevertherewas one, nonetheless eniedthatnaturalselection ad builtthehumanbrain."Savages"(living primitives),he argued, have mentalequipment qual to ours,butmaintainonlyarude and primitiveulture-that s, they o notuse mostof theirmental apacities nd naturalselection anonlybuildformmediate se. Dar-win, who was not a strict daptationist,wasbothbemused nd angered.He recognized hehiddenfallacy n Wallace's argument: hatthebrain, hough ndoubtedlyuiltby selection orsomecomplex etoffunctions, an, as a resultof its intricatetructure, ork n an unlimitednumber f waysquiteunrelated otheselectivepressure hat onstructedt. Many of hesewaysmightbecome mportant,fnotindispensable,forfuture urvival n later social contextslikeafternoon ea for Wallace's contemporaries).But current tility arriesno automatic mpli-cation bout historical rigin.Most ofwhatthebrain now does to enhanceoursurvival ies inthe domainofexaptation-and does not allowus tomakehypothesesboutthe elective athsofhumanhistory. ow muchofthe evolution-ary literature n human behavior would col-lapse ifwe incorporated heprinciple f exap-tation nto hecoreofourevolutionaryhinking?This collapse would be constructiveecause itwouldvastlybroadenourrangeofhypotheses,and focus ttention n current unctionnd de-velopmentall testablepropositions)nsteadofleadingus to unprovable everies boutprimalfratricide n the African avanna or dispatch-ingmammoths t theedgeofgreat ce sheets-a validsubject,but onebetter reatednnovels


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that can be quite enlighteningcientifically(Kurten 1980).Consider lso theapparentlyrucialrole thatrepeatedDNA has played in the evolutionofphenotypic omplexity n organisms. f eachgene codesfor n indispensablenzyme orper-formsny necessary unction),sksOhno 1970)in his seminalbook, how does evolution ran-scendmere inkeringlongestablishedinesandachievetheflexibilityobuildnewtypes f or-ganization. hnoargues hat his lexibility ustariseas the ncidental esult fgeneduplication,with tsproductionfredundant eneticmate-rial: "Had evolution been entirely ependentupon natural election, rom bacterium nlynumerous forms of bacteria would haveemerged. . . Only the cistronwhichbecameredundantwas able to escapefrom herelentlesspressure fnatural election, nd byescaping,itaccumulated ormerlyorbiddenmutationsoemerge s a newgene ocus" (from heprefacetoOhno 1970).We argued n sectionVE that much ofthisrepetitive NA may arisefornonaptive easonsat thelevel ofthe individualphenotypeas inthe "selfishDNA" hypothesis). he repeatedcopiesare thenexaptations, ooptedforfitnessand secondarily dapted for new roles. Andthey re exaptationsn the nterestingategoryofstructures hatarose as nonaptations,whenthe"selfish NA" hypothesispplies.Thus, the twoevolutionary henomena hatmayhave been most rucial o thedevelopmentofcomplexity ithconsciousnessn ourplanet(if readerswill pardonsomedripping nthro-pocentrismor hemoment)-theprocess fcre-ating genetic edundancynthe first lace, andthe myriadand inescapable consequencesofbuilding ny computing evice as complexasthe humanbrain-may bothrepresentxapta-tions thatbegan as nonaptations,he conceptpreviouslymissing n our evolutionary ermi-nology.Withexamples uch as these,thesub-ject cannotbe deemedunimportant!In short,the codification f exaptationnotonly dentifies commonflaw n much evolu-tionaryreasoning-the inference f historicalgenesisfrom urrent tility.t also focusses t-tention pontheneglected utparamount oleofnonaptive eaturesn bothconstrainingndfacilitatinghepathof evolution. he argument

is notanti-selectionist,nd we viewthispaperas a contributiono Darwinism,not as a skir-mish n a nihilistic endetta.The main themeis, after ll, cooptabilityorfitness.xaptationsare vitalcomponents fanyorganism'success.Acknowledgments

The following avecommented nthemanu-script:C. K. Brain, C. A. Green,A. C. Kemp,H. E. H. Paterson.One of us (E.S.V.) owes adebttoHughPaterson or n introduction,ur-ingextensive iscussions, o theterminologyfeffectssensuWilliams).We both hankhimforreferrings to theexamples fmantling ehav-ior in the Black Heron and lysozyme/a-lactal-buminevolution.D. M. Lamberthas givenusaccess to an unpublishedmanuscript,nd hasdiscussedwithus theubiquitouspresence, ndenormousmportance,n evolution fwhat heand others all preadaptation.Literature itedABERCROMBIE, M., C. H. HICKMAN, AND M. L. JOHNSON. 1951.A Dictionary of Biology. 5th edition, 1966. Hunt Bernard andCo. Ltd., Aylesbury, reat Britain.ARNOLD, A. J. AND K. FRISTRUP. 1982. The hierarchical basis for

a unified theoryof evolution. Paleobiology, in press.BAKKER, R. T. 1975. Dinosaur renaissance. Sci. Am. 232(4):58-78.BOCK, W. 1967. The use of adaptive characters in avian classifi-cation. Proc. XIV Int. Ornith.Cong., pp. 66-74.BOCK, W. 1979. A syntheticxplanationof macroevolutionarychange-a reductionisticpproach. Bull. CarnegieMus. Nat.Hist. No. 13:20-69.BOCK, W. J. 1980. The definitionnd recognitionfbiological d-aptation.Am. Zool. 20:217-227.BOCK. W. J. AND G. VON WAHLERT. 1965. Adaptation nd theform-functionomplex.Evolution.10:269-299.BRITTEN,R. J.AND E. H. DAVIDSON. 1971. Repetitive nd non-repetitive NA sequences and a speculation n the originsofevolutionary ovelty.Q. Rev. Biol. 46:111-131.COHEN, S. N. 1976. Transposable genetic lements nd plasmidevolution.Nature. 263:731-738.DARWIN, . 1859. On theOrigin f Species. J.Murray:London.DICKERSON,R. E. AND I. GEIS. 1969. The Structure nd ActionofProteins.Harperand Row; New York.DOOLITTLE,W. F. AND C. SAPIENZA. 1980. Selfish enes, he phe-notype aradigm, nd genome volution.Nature. 284:601-603.DUTHIE,R. B. AND A. B. FERGUSON. 1973. Mercer'sOrthopaedicSurgery. thedition.Edward Arnold;London.FISHER,R. A. 1958. GeneticalTheoryof NaturalSelection. 2ndrevised dition).Dover;New York.FOUCAULT,M. 1965. Madness and Civilization.Random House;New York.FOUCAULT,M. 1970. The OrderofThings. RandomHouse; New

York.FRAZZETTA,. H. 1975. Complex Adaptationsn Evolving Popu-lations. 267 pp. SinauerAssociates; underland,Massachusetts.GOULD,S. J. 1981. Whathappensto bodies fgenes ct for hem-selves? Nat. Hist. November.


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OSTROM, J. H. 1979. Bird flight: ow did it begin?Am. Sci.67:46-56.PATERSON, H. E. H. 1982. Species as a consequence of sex, inpress. Am. Sci.PAUTARD, F. G. E. 1961. Calcium,phosphorus, nd theorigin fbackbones.New Sci. 12: 364-366.PAUTARD, F. G. E. 1962. The molecular-biologicackground otheevolution fbone. Clin. Orthopaed. 4:230-244.PORTER, R. MS. Problems n thetreatmentf madness' n Englishscience,medicine nd literaturen theeighteenthentury.RACEY, P. A. AND J. C. SKINNER. 1979. Endocrine spectsof sex-ual mimicrynspottedhyenasCrocuta rocuta.J.Zool. London.187:315-326.RAuP,D. M. ANDS. J. GOULD. 1974. Stochastic imulation ndevolution of morphology-towards nomothetic aleontology.Syst.Zool. 23:305-322.ROMER, A. S. 1963.The ancienthistory' fbone.Ann.N.Y. Acad.Sci. 109:168-176.SCOTT, J.D. AND N. B. B. SYMONS. 1977. IntroductionoDentalAnatomy.Churchill ivingstone; ondon.SEILACHER, A. 1970. ArbeitskonzepturKonstruktionsmorpholo-gie. Lethaia.3:393-396.SEILACHER, A. 1972. Divariate patternsn pelecypod hells. Le-thaia. 5:325-343.VRBA, E. S. 1980. Evolution, species and fossils: how does lifeevolve? S. Afr.J. Sci. 76:61-84.WILLIAMS, G. C. 1966. Adaptation ndNatural Selection.Prince-tonUniversity ress;Princeton, ew Jersey.

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