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

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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 Stable URL: http://www.jstor.org/stable/2400563 . Accessed: 27/08/2012 17:43

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http://www.jstor.org Paleobiology,8(1), 1982, pp. 4-15

Exaptation-a missing term in the science of form

StephenJay Gould and Elisabeth S. Vrba*

Abstract.-Adaptationhas been definedand recognizedby two differentcriteria: historical genesis (featuresbuilt by naturalselection for their present role) and currentutility (features now enhancingfitness no matterhow theyarose). Biologistshave oftenfailed to recognizethe potentialconfusion between these differentdefinitions because we have tendedto view naturalselection as so dominantamong evolutionary mechanismsthat historicalprocess and currentproduct become one. Yet if manyfeatures of organisms are non-adapted,but available foruseful cooptation in descendants,then an importantconcept has no name in our lexicon (and unnamed ideas generallyremain unconsidered):features that now enhance fitnessbut were not built by naturalselection for their current role. We propose that such featuresbe called exaptationsand that adaptationbe restricted,as Darwin suggested,to featuresbuilt by selection fortheir current role. We presentseveral examples of exaptation,indicating where a failureto concep- tualizesuch an idea limitedthe range of hypotheses previously available. We exploreseveral consequences of exaptationand proposea terminologicalsolution to the problemof preadaptation.

StephenJ. Gould. Museum of ComparativeZoology, Harvard University,Cambridge, Massachusetts 02138 Elisabeth S. Vrba. TransvaalMuseum, Paul KrugerStreet, P.O. Box 413, Pretoria,South Africa

Accepted: October 15, 1981

I. Introduction (Foucault's interpretationhas been challenged We wish to proposea termfor a missingitem by Britishhistorian of scienceRoy Porter,MS). in the taxonomyof evolutionarymorphology. In other systemsof thought,what seems pe- Termsin themselvesare trivial,but taxonomies ripheralto us becomescentral, and distinctions revisedfor a differentordering of thoughtare essentialto us do not matter(whether idleness not withoutinterest. Taxonomies are not neu- is internallyinevitable, as in insanity,or exter- tralor arbitraryhat-racks for a set of unvarying nally imposed,as in unemployment). concepts;they reflect (or even create) different II. Two Meanings of Adaptation theoriesabout the structureof the world. As Michel Foucault has shown in several elegant In the vernacular,and in sciencesother than books (1965 and 1970, forexample), when you evolutionarybiology, the word adaptation has know whypeople classifyin a certainway, you several meanings all consistentwith the ety- understandhow theythink. mologyof ad + aptus,or towardsa fit(for a par- Successivetaxonomies are the fossiltraces of ticularrole). When we adapt a tool for a new substantialchanges in human culture. In the role, we changeits designconsciously so thatit mid 17thcentury, madmen were confined in in- will workwell in its appointedtask. When cre- stitutionsalong with the indigentand unem- ationistsbefore Darwin spoke of adaptation- ployed,thus endinga long traditionof exile or for the term long precedes evolutionary tolerationfor the insane. But what is the com- thought-theyreferred to God's intelligentac- mon groundfor a taxonomythat mixes the mad tion in designingorganisms for definiteroles. with the unemployed-an arrangementthat When physiologistsclaim that larger lungs of strikesus as absurd. The "key character"for Andean mountainpeoples are adapted to local the "highertaxon," Foucault argues, was idle- climates,they specify directed change for better ness, the cardinal sin and danger in an age on function.In short,all these meaningsrefer to the brinkof universalcommerce and industry historicalprocesses of change or creation for definitefunctions. The "adaptation"is designed * An equal timeproduction; order of authorshipwas de- specificallyfor the task it performs. terminedby a transoceaniccoin flip. In evolutionarybiology, however, we en- (?) 1982 The PaleontologicalSociety. All rightsreserved. 0094-83 73/82/0801-0002/$1.00 EXAPTATION 5

TABLE 1. A taxonomyof fitness.

Process Character Usage Natural selectionshapes the character adaptation function fora currentuse-adaptation A character,previously shaped by naturalselection fora particularfunction (an adaptation),is coopted aptation fora new use-cooptation exaptation effect A characterwhose origincannot be ascribedto the directaction of naturalselection (a nonaptation),is coopted fora currentuse-cooptation

countertwo differentmeanings-and a possible useful characternot built by selectionfor its conflationof concepts-for featurescalled ad- currentrole-and we shall followthis restric- aptations.The firstis consistentwith the ver- tion here (Table 1). Williams also recognizes nacular usages cited above: a featureis an ad- that much hagglingabout adaptationhas been aptationonly if it was builtby naturalselection "encouragedby imperfectionsof terminology" for the functionit now performs.The second (1966, p. 8), a situationthat we hope to alleviate definesadaptation in a static,or immediateway slightly. as any featurethat enhances current fitness, re- Bock, on the otherhand, championsthe sec- gardless of its historicalorigin. (As a further ond, or broader, meaning in the other most confusion,adaptation refersboth to a process widely-citedanalysis of adaptation from the and a state of being. We are only discussing 1960's(Bock and von Wahlert1965; Bock 1967, state of being here-that is, featurescontribut- 1979, 1980). "An adaptationis, thus, a feature ing to fitness.We includesome comments about of the organism,which interactsoperationally thisfurther problem in sectionVIE.) withsome factorof its environmentso that the Williams,in his classic book on adaptation, individual survives and reproduces"(1979, p. recognizedthis dilemma and restrictedthe term 39). to its first,or narrower,meaning. We should The dilemmaof subsumingdifferent criteria speak of adaptation,he argues, only when we of historicalgenesis and currentutility under a can "attributethe originand perfectionof this singleterm may be illustratedwith a neglected design to a long period of selectionfor effec- example froma famoussource. In his chapter tivenessin this particularrole" (1966, p. 6). In devotedto "difficultieson theory,"Darwin wrote his terminology,"function" refers only to the (1859, p. 197): operationof adaptations. Williams furtherar- The suturesin the skulls of youngmammals gues that we must distinguishadaptations and have been advanced as a beautifuladaptation theirfunctions from fortuitous effects. He uses foraiding parturition,and no doubt theyfa- "effect" in its vernacular sense-something cilitate,or may be indispensablefor this act; caused or produced, a resultor consequence. but as suturesoccur in the skulls of young Williams'concept of "effect"may be applied to birdsand reptiles,which have onlyto escape a character,or to its usage, or to a potential(or froma broken egg, we may inferthat this process), arisingas a consequenceof true ad- structurehas arisenfrom the laws of growth, aptation. Fortuitouseffect always connotes a and has been taken advantage of in the par- consequencefollowing "accidentally," and not turitionof the higheranimals. arisingdirectly from construction by naturalselection.Others have adopted variousaspects of Darwin assertsthe utility,indeed the necessity, this terminologyfor "effects"sensu Williams of unfusedsutures but explicitlydeclines to la- (Paterson 1981; Vrba 1980; Lambert, MS). bel theman adaptationbecause theywere not However, Williams and othersusually invoke builtby selectionto functionas theynow do in the term'effect' to designatethe operationof a mammals.Williams follows Darwin and would 6 STEPHEN JAY GOULD & ELISABETH S. VRBA decline to call this featurean adaptation; he towardsfitness. They owe theirfitness to fea- would designateits role in aiding the survival tures presentfor otherreasons, and are there- of mammals as a fortuitouseffect. But Bock forefit (aptus) by reason of (ex) theirform, or would call the suturesand the timingof their ex aptus. Mammaliansutures are an exaptation fusionan adaptation,and a vital one at that. forparturition. Adaptations have functions;ex- As an example of unrecognizedconfusion, aptationshave effects.The general,static phe- considerthis definition of adaptationfrom a bi- nomenonof beingfit should be called aptation, ologicaldictionary (Abercrombie et al. 1951, p. not adaptation.(The set of aptationsexisting at 10): "Any characteristicof living organisms any one time consistsof two partiallyoverlap- which, in the environmentthey inhabit, im- ping subsets:the subsetof adaptationsand the provestheir chances of survivaland ultimately subset of exaptations.This also applies to the leaving descendants,in comparisonwith the moreinclusive set of aptationsexisting through chances of similarorganisms without the char- time;see Table 1.) acteristic;natural selectiontherefore tends to establishadaptations in a population." This def- IV. The CurrentNeed fora initionconflates current utility with historical Conceptof Exaptation genesis. What is to be done with usefulstruc- Why has this conflationof historicalgenesis turesnot built by naturalselection for their cur- with currentutility attracted so littleattention rentrole? heretofore?Every biologist surely recognizes that some usefulcharacters did not arise by se- III. A Definitionof Exaptation lectionfor their current roles; why have we not We have identifiedconfusion surrounding honoredthat knowledge with a name?Does our one of the centralconcepts in evolutionarythe- failureto do so simplyunderscore the unim- ory. This confusionarises, in part,because the portanceof the subject? Or mightthis absent taxonomyof formin relationto fitnesslacks a term,in Foucault's sense, reflecta conceptual term.Following Williams (see Table 1), we may structurethat excluded it? And, finally,does the designateas an adaptationany feature that pro- potentialneed for such a termat this time in- motesfitness and was built by selectionfor its dicate that the conceptualstructure itself may currentrole (criterion of historicalgenesis). The be altering? operationof an adaptationis itsfunction. (Bock Why did Williams not suggesta term,since uses the term functionsomewhat differently,he clearlyrecognized the problemand did sep- but we believe we are followingthe biological arate usages into functionsand effects(corre- vernacularhere.) We may also followWilliams spondingrespectively to adaptationsand to the in labellingthe operationof a usefulcharacter unnamed featuresthat we call exaptations)? not built by selectionfor its currentrole as an Whydid Bock failto specifythe problem at all? effect.(We designateas an effectonly the usage We suspect that the conceptualframework of of such a character,not the characteritself, see modern evolutionarythought, by continually p. 5.) But what is the unselected,but useful emphasizingthe supremeimportance and con- characteritself to be called? Indeed it has no tinuityof adaptationand naturalselection at all recognizedname (unlesswe acceptBock's broad levels, subtlyrelegated the issue of exaptation definitionof adaptation-the criterionof cur- to a peripheryof unimportance.How could rentutility alone and rejectboth Darwin and nonadaptiveaspects of form gain a properhear- Williams).Its space on the logical chartis cur- ing under Bock's definition(1967, p. 63): "On rentlyblank. theoreticalgrounds, all existingfeatures of an- We suggestthat such characters,evolved for imals are adaptive. If theywere not adaptive, otherusages (or forno functionat all), and later thenthey would be eliminatedby selectionand "coopted" for theircurrent role, be called ex- would disappear."Williams recognized the phe- aptations. (See VIA on the related concept of nomenon of exaptation and even granted it "preadaptation.")They are fitfor their current some importance(in assessingthe capacities of role, hence aptus, but theywere not designed the humanmind, for example), but he retained forit, and are thereforenot ad aptus, or pushed a preeminentrole foradaptation and oftendes- EXAPTATION 7 ignated effectsas fortuitousor peripheral- V. Examples of Exaptation "merelyan incidentalconsequence" he statesin A) Feathers and flight-sequentialexaptation one passage (p. 8). in the evolutionof birds.-Consider a common We believethat the adaptationistprogram of scenariofrom the evolution of birds. (We do not modern evolutionarythought (Gould and Le- assertits correctness,but onlywish to examine wontin1979) has been weakeningas a resultof appropriateterminology for a common set of challengesfrom all levels, moleculesto macro- hypotheses.) Skeletal features,including the evolution. At the biochemicallevel, we have sternum,rib basket and shoulderjoint, in late theoriesof neutralismand suggestionsthat sub- Jurassicfossils of Archaeopteryxindicate that stantialamounts of DNA may be nonadaptive this earliestknown bird was probablycapable at the level of the phenotype(Orgel and Crick of only the simplestfeats of flight.Yet it was 1980; Doolittleand Sapienza 1980). Studentsof quite thoroughlyfeathered. This has suggested macroevolutionhave arguedthat adaptations in to many authors that selectionfor the initial populationstranslate as effectsto yieldthe pat- developmentof feathersin an ancestorwas for ternsof differentialspecies diversificationthat the functionof insulation and not for flight may resultin evolutionarytrends (Vrba's effect (Ostrom1974, 1979; Bakker 1975). Such a fun- hypothesis,1980). If nonadaptation(or what damental innovationwould, of course, have shouldbe called nonaptation)is about to assume many small as well as far-reaching,incidental an importantrole in a revisedevolutionary the- consequences. For example, along no descen- ory,then our terminologyof formmust recog- dant lineage of this firstfeathered species did nize its cardinal evolutionarysignificance- (so faras we know)a furrycovering of the body cooptabilityfor fitness(see Seilacher 1972, on evolve. The fixationearly in the lifeof the em- importanteffects of a nonaptivepattern in the bryo, of cellular changes that lead on the one structureand colorationof molluscs). hand to hair, and on the otherto feathers,con- Some colleagues have said that they prefer strainedthe subsequentcourse of evolutionin Bock's broad definitionbecause it is moreeasily body covering(Oster 1980). operational.We can observeand experimentto Archaeopteryxalready had largecontour-type determinewhat good a featuredoes foran or- feathers,arranged along its arms in a pattern ganismnow. To reconstructthe historical path- very much as in the wings of modern birds. way of its originis always more difficultand Ostrom(1979, p. 55) asks: "Is it possible that often(when crucial evidence is missing)intract- the initial (pre-Archaeopteryx)enlargement of able. featherson those narrow hands might have this To we reply that we are not tryingto been to increasethe hand surfacearea, thereby dismantleBock's concept.We merelyargue that making it more effectivein catchinginsects?" it should be called aptation (with adaptation He concludes(1979, p. 56): "I do believe that and as its As it exaptation modes). aptation, the predatorydesign of the wing skeleton in retainsall the favorableproperties for testing Archaeopteryxis strong evidence of a prior enumeratedabove. predatoryfunction of the proto-wingin a cur- Historical genesis is, undoubtedly,a. more sorial proto-Archaeopteryx." Later selectionfor difficult but problem we cannottherefore ignore changes in skeletal featuresand feathers,and it. As evolutionists,we are charged,almost by forspecific neuromotor patterns, resulted in the definition,to regardhistorical pathways as the evolutionof flight. essenceof our subject.We cannotbe indifferent The Black Heron (or Black Egret, Egretta to the factthat similarresults can arise by dif- ardesiaca) of Africa,like most modern birds, ferenthistorical routes. Moreover, the distinc- uses its wingsin flight.But it also uses themin tion betweenad- and exaptation,however dif- an ficult,is not unresolvable.If we ever find a interestingway to prey on small fish: "Its small runningdinosaur, ancestral to birds and fishingis performedstanding in shallow water clothedwith feathers,we will know that early withwings stretched out and forward,forming featherswere exaptations,not adaptations,for an umbrella-likecanopy whichcasts a shadow flight. on the water. In thisway its food can be seen" 8 STEPHEN JAY GOULD & ELISABETH S. VRBA

(McLachlan and Liversidge 1978, p. 39, Plate adaptation for storingphosphates needed for 6). This "mantling"of the wingsappears to be metabolic activity.Only considerablylater in a characteristicbehavior pattern, with a genetic evolutiondid bone replacethe cartilaginousen- basis. The wing and featherstructures them- doskeletonand adopt the functionof support selvesdo notseem to be modifiedin comparison forwhich it is now mostnoted. with those of closely relatedspecies, the indi- Thus, bone has two major uses in extantver- viduals of whichdo not huntin thisway (A. C. tebrates:support/protection and storage/homeo- Kemp, pers. comm.). stasis (as a storehousefor certain mineral ions, We see, in this scenario,a sequentialset of includingphosphate ions). The ions in verte- adaptations,each convertedto an exaptationof brate bone are in equilibriumwith those in tis- differenteffect that sets the basis for a subse- sue fluidsand blood, and functionin certain quent adaptation. By this interplay,a major metabolic activities(Scott and Symons 1977). evolutionarytransformation occurs that proba- For instance,in humans, 90% of body phos- bly could not have arisen by purelyincreasing phorusis presentin the inorganicphase of bone adaptation. Thus, the basic design of feathers (Duthie and Ferguson1973). is an adaptationfor thermoregulation and, lat- FollowingHalstead's analysis,the deposition er, an exaptationfor catchinginsects. The de- of phosphatein body tissuesoriginally evolved velopmentof large contourfeathers and their as an adaptationfor a storage/metabolicfunc- arrangementon the arm ariseas adaptationsfor tion. The metabolicmechanism for producing insect catching and become exaptations for bone per se can thus be interpretedas an ex- flight.Mantling behavior uses wingsthat arose aptation for support. The metabolic mecha- as an adaptation for flight.The neuromotor nisms for depositingan increasedquantity of modificationsgoverning mantling behavior, and phosphatesand for mineralization,as well as thereforethe mantlingposture, are adaptations the arrangementof bony elements in an internal forfishing. The wing per se is an exaptationin skeleton,are thenadaptations for support. its currenteffect of shading,just as the feathers C) The evolutionof mammalianlactation.- coveringit also arose in differentadaptive con- Dickerson and Geis (1969) recounthow Alex- textsbut have providedmuch evolutionary flex- ander Fleming,in 1922, discoveredthe enzyme ibilityfor other uses during the evolution of lysozyme.He had a cold and, forinterest's sake, birds. added a fewdrops of nasal mucusto a bacterial B) Bone as storageand support.-The devel- culture.To his surprisehe found,after a few opmentof bone was an event of major signifi- days, that somethingin the mucus was killing cance in the evolutionof vertebrates.Without the bacteria:the enzymelysozyme, since found bone, vertebratescould nothave latertaken up in mostbodily secretions and in largequantities life on land. Halstead (1969) has investigated in the whitesof eggs. Lysozymedestroys many the question: grantingits subsequent impor- bacteriaby lysing,or dissolving,the mucopoly- tance as body supportin the later evolutionof saccharidestructure of thecell wall. The amino vertebrates,why did bone evolve at such an acid sequence of a-lactalbumin,a milk protein earlystage in vertebratehistory? Some authors of previouslyunknown function, was thenfound have hypothesizedthat bone initiallyarose as to be so close to that of lysozyme,that some an osmoregulatoryresponse to life in freshwa- relationship of close homology must be in- ter. Others,like Romer(1963), postulateinitial volved. Dickerson and Geis (1969, pp. 77-78) adaptation of bony "armor" for a protective write: function.Pautard (1961, 1962) pointedout that anyorganism with much muscular activity needs a-Lactalbuminby itselfis not an enzymebut a convenientlyaccessible store of phosphate. was foundto be one componentof a two-pro- Following Pautard, and noting the seasonal tein lactose synthetasesystem, present only cycle of phosphateavailability in the sea, Hal- in mammaryglands duringlactation . . .. stead (1969) suggestedthe followingscenario: The othercomponent (the "A" protein)had Calcium phosphates,laid down in the skin of been discoveredin the liverand otherorgans the earliestvertebrates, evolved initiallyas an as an enzymefor the synthesis of N-acetyllac- EXAPTATION 9

tosaminefrom galactose and NAG. But the unconsciouslyforced previous authors into this combinationof the A proteinand a-lactal- erroneousconceptual bind. buminsynthesizes the milk sugar lactose from Kruuk (1972), the leading studentof spotted galactose and glucose instead. The non-cat- hyenas, for example, notes that the enlarged alytica-lactalbumin evidently acts as a con- sexual organsof femalesare used in an impor- troldevice to switchits partnerfrom one po- tant behavior know as the meetingceremony. tentialsynthesis to another.... It appears Hyenas spend long periodsas solitarywander- thatwhen a milk-producing-systemwas being ers searchingfor carrion,but theyalso live in developedduring the evolutionof mammals, well integratedclans that defendterritory and and when a need for a polysaccharide-syn- engagein communalhunting. A mechanismfor thesizingenzyme arose, a suitable one was reintegratingsolitary wanderers into their prop- found in part by modifyinga pre-existing er clan mustbe developed. In the meetingcer- polysaccaride-cuttingenzyme. emony,two hyenasstand side to side, facingin opposite directions.Each liftsthe inside hind Thus, lysozyme,in all vertebratesin which leg, exposingan erectpenis or clitoristo itspart- it occurs,is probablyan adaptationfor the func- ner'steeth. They sniffand lick each other'sgen- tion of killing bacteria. Furtherevolution in itals for 10 to 15 seconds,largely at the base of mammals (alterationof a duplicated gene ac- the penis or clitorisand in frontof the scrotum cordingto Dickerson and Geis, 1969) resulted or false scrotum. in a-lactalbumin,an adaptation(together with Having discovereda currentutility for the the A protein)for the functionof lactose syn- prominentexternal genitalia of females,Kruuk thesis and lactation. Human lysozyme,in this (1972, pp. 229-230) infersthat they must have scenario, is an adaptation for lysing the cell evolved forthis purpose: bacteria, and an exaptationwith re- walls of It is impossibleto thinkof any otherpurpose to the lactose synthetasesystem. spect forthis special femalefeature than foruse in D) Sexual "mimicry"in hyenas.-Females of the meetingceremony . . . It may also be, the spottedhyena, Crocuta crocuta, are larger then,that an individualwith a familiarbut males and dominantover them. Pliny, and than relativelycomplex and conspicuousstructure otherancient writers, had alreadyrecognized a sniffedat duringthe meetinghas an advan- relatedand unusual featureof theirbiology in tage over others;the structurewould often calling them hermaphrodites(falsely, as Aris- facilitatethis reestablishmentof social bonds totleshowed). The externalgenitalia of females by keeping partnerstogether over a longer are virtuallyindistinguishable from the sexual meetingperiod. This could be the selective organsof males by sight.The clitorisis enlarged advantage that has caused the evolutionof and extended to form a cylindricalstructure the females'and cubs' genitalstructure. witha narrowslit at itsdistal end; it is no small- er thanthe male's penisand can also be erected. Yet another hypothesis,based upon facts The labia majora are folded over and fused known to every Biology I student, virtually along the midline to forma false scrotal sac cries out forrecognition. The penis and clitoris (though withouttesticles of course), virtually are homologousorgans, as are the scrotumand identicalin formand positionwith the male's labia majora. We know thathigh levels of an- scrotum(Harrison Matthews 1939). drogen induce the enlargementof the clitoris The literatureon thissexual "mimicry"is full and thefolding over and fusionof the labia until of speculationsabout adaptive meaning. Most theyresemble penis and scrotalsac respectively. of these argumentshave conflatedcurrent util- (In fact,in an importantsense, theyare thena ity and historicalgenesis in assumingthat the penis and scrotal sac, given the homologies.) demonstrationof modern use (Bockian adap- Human baby girlswith unusually enlarged ad- tation) specifiesthe path of origin(adaptation renals secretehigh levels of androgen,and are as used by Williams and Darwin, and as ad- bornwith a peniformclitoris and an emptyscro- vocated in thispaper). We suggestthat the ab- tal sac formedof the fusedlabia. senceof an articulatedconcept of exaptation has Female hyenas are larger than males and 10 STEPHEN JAY GOULD & ELISABETH S. VRBA dominantover them. Since these featuresare that the architectureof geneticmaterial might oftenhormonally mediated in mammals,should fitall theirpresuppositions about evolutionary we not conjecturethat females attain their sta- processes.The linearorder of nucleotidesmight tus by secretingandrogens and that the peni- be the beads on a stringof classical genetics: formclitoris and falsescrotal sac are automatic, one gene, one enzyme;one nucleotidesubstitu- secondaryby-products. Since theyare formed tion,one minutealteration for natural selection anyway,a laterand secondaryutility might en- to scrutinize.We are now, not even 20 years sue; theymay be coopted to enhancefitness in later,faced withgenes in pieces, complexhier- the meeting ceremonyand then secondarily archies of regulation and, above all, vast modifiedfor this new role. We suggestthat the amountsof repetitiveDNA. Highlyrepetitive, peniformclitoris and false scrotalsac arose as or satellite,DNA can existin millionsof copies; nonaptiveconsequences of highandrogen levels middle-repetitiveDNA, withits tens to hundreds (a primaryadaptation related to the unusual of copies, formsabout one quarter of the ge- behavioralrole of females). They are, therefore, nome in both Drosophila and Homo. What is exaptationsfor the meeting ceremony, and their all the repetitiveDNA for (if anything)?How effectin enhancingfitness through that cere- did it get there? monydoes not specifythe historicalpathway of A surveyof previousliterature (Doolittle and theirorigin. Sapienza 1980; Gould 1981) revealstwo emerg- Yet this obvious hypothesis,with its easily ing traditionsof argument,both based on the testablecardinal premise, was not explicitlyex- selectionistassumption that repetitiveDNA amined until 1979 after,literally, more than must be good for somethingif so much of it 2000 yearsof speculationin the adaptive mode exists.One tradition(see Brittenand Davidson (both ancient authors and medieval bestiaries 1971 forits locus classicus) holds that repeated tried to inferGod's intentin creatingsuch an copies are conventionaladaptations, selected odd beast). Racey and Skinner(1979) foundno foran immediaterole in regulation(by bringing differencesin levels of androgenin blood plas- previouslyisolated parts of the genome into new ma of male and femalespotted hyenas. Female and favorablecombinations, for example, when fetusescontained the same highlevel of testos- repeated copies disperse among several chro- teroneas adultfemales. In theother two species mosomes).We do not doubt that conventional of the familyHyaenidae, however, androgen adaptation explains the preservationof much levels in blood plasma are much lower for fe- repeatedDNA in thismanner. males than formales. Females of these species But many molecular evolutionists now are notdominant over males and do notdevelop stronglysuspect that directadaptation cannot peniformclitorises or false scrotalsacs. explain the existence of all repetitiveDNA: We do not assertthat our alternativehypoth- thereis simplytoo much of it. The second tra- esis of exaptationmust be correct.One could ditiontherefore holds that repetitive DNA must run the scenarioin reverse(with a bit of forcing exist because evolutionneeds it so badly for a in our judgment): females "need" prominent flexiblefuture-as in thefavored argument that genitaliafor the meetingceremony; they build "unemployed,"redundant copies are freeto al- themby selectionfor high androgen levels; large terbecause theirnecessary product is stillbeing size and dominanceare a secondaryby-product generatedby the originalcopy (see Cohen 1976; of the androgen. We raise, rathera different Lewin 1975; and Kleckner 1977, all of whom issue: whywas thisevident alternative not con- also follow the firsttradition and argue both sidered,especially by Kruukin his excellentex- sides). While we do not doubt thatsuch future haustivebook on the species?We suggestthat uses are vitallyimportant consequences of re- the absence of an explicitlyarticulated concept peated DNA, theysimply cannot be the cause of exaptationhas constrainedthe range of our of itsexistence, unless we returnto certaintheis- hypothesesin subtleand unexaminedways. tic views that permit the control of present E) The uses of repetitiveDNA.-For a few eventsby futureneeds. years afterWatson and Crick elucidated the This second traditionexpresses a correctin- structureof DNA, many evolutionistshoped tuitionin a patentlynonsensical (in its nonpe- EXAPTATION 11 jorativemeaning) manner. The missingthought formedin a differentway (thermoregulationfor that suppliessense is a well articulatedconcept feathers,for example). Yet we traditionally of exaptation.Defenders of thesecond tradition apologizefor "preadaptation" in our textbooks, understandhow importantrepetitive DNA is to and laboriouslypoint out to studentsthat we do evolution,but onlyknow the conventionallan- not mean to implyforeordination, and that the guage of adaptationfor expressing this convic- word is somehowwrong (though the conceptis tion.But sinceutility is a futurecondition (when secure). Frazzetta (1975, p. 212), for example, theredundant copy assumes a differentfunction writes:"The associationbetween the word 'pre- or undergoessecondary adaptation for a new adaptation' and dubious teleologystill lingers, role), an impasse in expressiondevelops. To and I can oftenproduce a wave of nausea in break this impasse, we mightsuggest that re- some evolutionarybiologists when I use the peated copies are nonaptedfeatures, available word unlessI am quick to say what I mean by forcooptation later, but not servingany direct it." functionat the moment.When coopted, they Indeed, theword is wrongand our longstand- will be exaptationsin theirnew role (with sec- ing intuitivediscomfort is justified(see Lam- ondaryadaptive modificationsif altered). bert,MS). For if we divide the class of features What thenis the sourceof theseexaptations? contributingto fitnessinto adaptationsand ex- Accordingto the firsttradition, they arise as aptations,and if adaptationswere constructed trueadaptations and laterassume their different (and exaptationscoopted) for their current use, function.The second tradition,we have ar- then featuresworking in one way cannot be gued, must be abandoned. A thirdpossibility preadaptationsto a differentand subsequent has recentlybeen proposed (or, rather,better usage: the termmakes no sense at all. codifiedafter previous hints): perhaps repeated The recognitionof exaptationsolves the di- copies can originatefor no adaptive reasonthat lemma neatly,for what we now incorrectlycall concernsthe traditional Darwinian level of phe- "preadaptation"is merelya categoryof exap- notypicadvantage (Orgel and Crick 1980; Doo- tation consideredbefore the fact. If feathers littleand Sapienza 1980). Some DNA elements evolved forthermoregulation, they become ex- are transposable; if these can duplicate and aptationsfor flight once birdstake off.If, how- move,what is to stoptheir accumulation as long ever, with the hindsightof history,we choose as they remain invisible to the phenotype(if to look at featherswhile theystill encase the theybecome so numerousthat they begin to ex- running,dinosaurian ancestorsof birds, then ertan energeticconstraint upon the phenotype, theyare onlypotential exaptations for flight, or thennatural selection will eliminatethem)? Such preaptations(that is, aptus-or fit-beforetheir "selfishDNA" may be playingits own Darwin- actual cooptation).The term "preadaptation" ian game at a genic level, but it representsa should be dropped in favor of "preaptation." truenonaptation at the level of the phenotype. Preaptationsare potential,but unrealized,ex- Thus, repeatedDNA may oftenarise as a nonaptations;they resolve Mivart's major challenge aptation. Such a statementin no way argues to Darwin. againstits vital importancefor evolutionary fu- B) Primary exaptationsand secondary ad- tures. When used to great advantage in that aptations.-Feathers, in theirbasic design, are future,these repeated copies are exaptations. exaptationsfor flight, but once this new effect was added to the functionof thermoregulation VI. Significanceof Exaptation as an important source of fitness, feathers A) A solution to the problemof preadapta- underwenta suite of secondary adaptations tion.-The conceptof preadaptation has always (sometimescalled post-adaptations)to enhance been troublingto evolutionists.We acknowl- theirutility in flight.The order and arrange- edge itsnecessity as theonly Darwinian solution mentof tetrapodlimb bones is an exaptationfor to Mivart's(1871) old tauntthat "incipient stages walkingon land; many modificationsof shape of usefulstructures" could not functionas the and musculatureare secondaryadaptations for perfectedforms do (whratgood is 5% of a wing). terrestriallife. The incipientstages, we argue,must have per- The evolutionaryhistory of any complexfea- 12 STEPHEN JAY GOULD & ELISABETH S. VRBA turewill probablyinclude a sequentialmixture etymologyrequires a differentname forpreap- of adaptations, primaryexaptations and sec- tationsafter they are established.Exaptations ondaryadaptations. Just as any featureis ple- that began as nonaptationsrepresent the miss- siomorphicat one taxonomiclevel and apo- ing concept.They are not coveredby the prin- morphic at another (torsion in the class ciple of preaptation,for they were not adapta- Gastropoda and in the phylumMollusca), we tions in ancestors.They trulyhave no name, are not disturbedthat complexfeatures are a and conceptswithout names cannotbe properly mixtureof exaptationsand adaptations. Any incorporatedin thought.The great confusions cooptedstructure (an exaptation)will probably ofhistorical genesis and currentutility primarily not arise perfectedfor its new effect.It will involve useful featuresthat were not adapta- thereforedevelop secondaryadaptations for the tionsin ancestors-as in our examplesof sexual new role. The primaryexaptations and second- "mimicry"in hyenasand the uses of middle-re- ary adaptations can, in principle,be distin- petitiveDNA. guished. D) The ironyof our terminologyfor nonap- C) The sources of exaptation.-Features tation.-It seems odd to definean important coopted as exaptationshave two possible pre- thingby whatit is not. Studentsof early geology vious statuses.They mayhave been adaptations are rightlyoffended that we referto 5/6 of earth for anotherfunction, or they may have been historyas Precambrian.Features not now con- non-aptivestructures. The firsthas long been tributingto fitnessare usuallycalled nonadap- recognized as important,the second under- tations. (In our terminologythey are nonapta- played. Yet the enormouspool of nonaptations tions.)This curiousnegative definition can only must be the wellspringand reservoirof most recorda feelingthat the subjectis "lesser"than evolutionaryflexibility. We need to recognize the thingit is not. We believe that this feeling the centralrole of "cooptabilityfor fitness" as is wrong,and that the size of the pool of non- the primaryevolutionary significance of ubiq- aptationsis a centralphenomenon in evolution. uitous nonaptationin organisms.In this sense, The term"nonadaptive" is but anotherindica- and at its level of the phenotype,this nonaptive tion of previous-and in our view false-con- pool is an analog of mutation-a sourceof raw victions about the supremacyof adaptation. materialfor further selection. The burden of nomenclatureis already great Both adaptations and nonaptations,while enough in this paper and we do not propose a theymay have non-randomproximate causes, new termfor featureswithout current fitness. can be regardedas randomlyproduced with re- But we do wish to recordthe irony. spect to any potentialcooptation by furtherre- E) Process and state-of-being.-Evolutionary gimes of selection.Simply put: all exaptations biologistsuse the term adaptation to describe originaterandomly with respect to theireffects. both a currentstate-of-being (as discussed in Together,these two classes of characters,ad- this paper) and the processleading to it. This aptations and nonaptations,provide an enor- dualitypresents no problemin cases of truead- mous pool of variability,at a level higherthan aptation,where a process of selectiondirectly mutations,for cooptation as exaptations.(Lam- produces the state of fitness.Exaptations, on bert,MS, has discussedthis with respect to pre- the otherhand, are not fashionedfor their cur- adaptations only-preaptations in our termi- rent role and reflectno attendantprocess be- nology. He explored the evolutionary yond cooptation(Table 1); theywere built in implicationsof the notionthat for any function, the past eitheras nonaptiveby-products or as resultingdirectly from natural selection at any adaptationsfor different roles. one time,there may be multipleeffects.) Perhapswe should beginour analysisof pro- If all exaptationsbegan as adaptations for cess witha descriptiveapproach and simplyfo- another functionin ancestors,we would not cus upon the set of featuresthat increasetheir have writtenthis paper. For the conceptwould relativeor absolute abundance withinpopula- be coveredby theprinciple of "preadaptation"- tions,species or clades by the onlygeneral pro- and we would only need to point out that cesses that can yield such "plurifaction,"or "preaptation"would be a betterterm, and that "more making": differentialbranching or per- EXAPTATION 13 sistence(see Arnold-and Fristrup,MS). This the flexibilityof phenotypiccharacters as a pri- descriptiveprocess of plurifactionhas two basic maryenhancer of or damper upon futureevo- causes. First, featuresmay increasetheir rep- lutionarychange. Flexibilitylies in the pool of resentationactively by contributingto branch- featuresavailable for cooptation(either as ad- ing or persistenceeither as adaptationsevolved aptationsto somethingelse that has ceased to by selectionfor theircurrent function, or ex- be importantin new selectiveregimes, as adaptationsevolved by anotherroute and coopted aptationswhose originalfunction continues but fortheir useful effect. Secondly, and particular- whichmay be cooptedfor an additionalrole, or ly at the higherlevel of species withinclades, as nonaptationsalways potentiallyavailable). featuresmay increasetheir own representation The paths of evolution-both the constraints fora hostof nonaptive reasons, including causal and the opportunities-mustbe largelyset by correlationwith features contributing to fitness, the size and natureof thispool of potentialex- and fortuitouscorrelation found at such sur- aptations.Exaptive possibilitiesdefine the "in- prisinglyhigh frequency in randomsimulations ternal" contributionthat organismsmake to by Raup and Gould (1974). These nonaptive theirown evolutionaryfuture. featuresestablish an enormous-poolfor poten- A. R. Wallace, a strictadaptationist if ever tial exaptation. therewas one, nonethelessdenied that natural selectionhad builtthe humanbrain. "Savages" VII. Conclusion (living primitives),he argued, have mental The ultimatedecision about whetherwe have equipmentequal to ours, but maintainonly a writtena trivialessay on terminologyor made rude and primitiveculture-that is, theydo not a potentiallyinteresting statement about evo- use mostof theirmental capacities and natural lution must hinge upon the importanceof ex- selectioncan onlybuild forimmediate use. Dar- aptation,both in frequencyand in role. We be- win, who was not a strictadaptationist, was lieve that the failureof evolutioniststo codify both bemusedand angered.He recognizedthe such a conceptmust record an inarticulatedbe- hidden fallacyin Wallace's argument:that the liefin its relativeinsignificance. brain,though undoubtedly built by selectionfor We suspect, however, that the subjects of some complexset of functions,can, as a result nonaptationand cooptabilityare of paramount of its intricatestructure, work in an unlimited importancein evolution. (When cooptability numberof ways quite unrelatedto the selective has been recognized-in the principleof "pre- pressurethat constructed it. Many ofthese ways adaptation"-we have focussed upon shiftin mightbecome important,if not indispensable, role for featurespreviously adapted for some- forfuture survival in later social contexts(like thingelse, noton the potentialfor exaptation in afternoontea for Wallace's contemporaries). nonapted structures.)The flexibilityof evolu- But currentutility carries no automaticimpli- tionlies in the rangeof raw materialpresented cationabout historicalorigin. Most of what the to processesof selection.We all recognizethis brain now does to enhance our survivallies in in discussingthe conventional sources of genetic the domain of exaptation-and does not allow variation-mutation, recombination,and so us to make hypothesesabout theselective paths forth-presentedto natural selectionfrom the of human history.How much of the evolution- geneticlevel below. But we have notadequately ary literatureon human behavior would col- appreciated that features of the phenotype lapse if we incorporatedthe principleof exap- themselves(with theirusually complexgenetic tationinto the core of our evolutionarythinking? bases) can also act as variantsto enhance and This collapse would be constructivebecause it restrictfuture evolutionary change. Thus the would vastlybroaden our rangeof hypotheses, importantstatement of Fisher's fundamental and focusattention on currentfunction and de- theoremconsiders only geneticvariance in re- velopment(all testablepropositions) instead of lation to fitness:"The rate of increasein fitness leading us to unprovablereveries about primal of any organismat any timeis equal to its ge- fratricideon the Africansavanna or dispatch- netic variance in fitnessat that time" (Fisher ing mammothsat the edge of greatice sheets- 1958). In an analogous way, we mightconsider a valid subject,but one bettertreated in novels 14 STEPHEN JAY GOULD & ELISABETH S. VRBA that can be quite enlighteningscientifically is not anti-selectionist,and we view this paper (Kurten 1980). as a contributionto Darwinism,not as a skir- Consideralso the apparentlycrucial role that mish in a nihilisticvendetta. The main theme repeated DNA has played in the evolutionof is, afterall, cooptabilityforfitness. Exaptations phenotypiccomplexity in organisms.If each are vital componentsof any organism'ssuccess. gene codes foran indispensableenzyme (or per- formsany necessaryfunction), asks Ohno (1970) Acknowledgments in his seminal book, how does evolutiontran- The followinghave commentedon the manu- scend meretinkering along establishedlines and script:C. K. Brain, C. A. Green,A. C. Kemp, achieve the flexibilityto build new typesof or- H. E. H. Paterson.One of us (E.S.V.) owes a ganization.Ohno arguesthat this flexibility must debt to Hugh Patersonfor an introduction,dur- arise as theincidental result of gene duplication, ing extensivediscussions, to the terminologyof with its productionof redundantgenetic mate- effects(sensu Williams).We boththank him for rial: "Had evolution been entirelydependent referringus to the examplesof mantlingbehav- upon naturalselection, from a bacteriumonly ior in the Black Heron and lysozyme/a-lactal- numerous forms of bacteria would have bumin evolution.D. M. Lamberthas given us emerged.. . . Only the cistronwhich became access to an unpublishedmanuscript, and has redundantwas able to escape fromthe relentless discussedwith us the ubiquitouspresence, and pressureof naturalselection, and by escaping, enormousimportance, in evolutionof what he it accumulatedformerly forbidden mutations to and otherscall preadaptation. emergeas a new gene locus" (fromthe preface to Ohno 1970). LiteratureCited We argued in sectionVE that much of this repetitiveDNA may arisefor nonaptive reasons ABERCROMBIE, M., C. H. HICKMAN, AND M. L. JOHNSON. 1951. at the level of the individualphenotype (as in A Dictionary of Biology. 5th edition, 1966. Hunt Bernard and Co. Ltd., Aylesbury,Great Britain. the "selfishDNA" hypothesis).The repeated ARNOLD, A. J. AND K. FRISTRUP. 1982. The hierarchical basis for copies are thenexaptations, coopted for fitness a unified theory of evolution. Paleobiology, in press. and secondarilyadapted for new roles. And BAKKER, R. T. 1975. Dinosaur renaissance. Sci. Am. 232(4):58-78. BOCK, W. 1967. The use of adaptive characters in avian classifi- theyare exaptationsin the interestingcategory cation. Proc. XIV Int. Ornith.Cong., pp. 66-74. of structuresthat arose as nonaptations,when BOCK, W. 1979. A syntheticexplanation of macroevolutionary the "selfishDNA" hypothesisapplies. change-a reductionisticapproach. Bull. Carnegie Mus. Nat. Hist. No. 13:20-69. 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