How exaptation completes and rationalizes the terminology of
evolutionary change by functional shifting
Following my idiosyncratic interest in the use of language as an underappreciated guide to the history and relative ranking of concepts, I wish to cite a gaping hole in the logical terminology of Darwinian evolution as primary evidence for this long, and regrettable, undervaluation of quirky functional shift. (This section follows the argument of Gould and Vrba, 1982.)
As a staple of anglophonic biology, long predating Darwin's explanatory spin, and extending back to Paley at the dawn of the 19th century, and to Boyle in the heart of the scientific revolution of the late 17th century, the process [Page 1230] of crafting (usually construed as God's creating) a feature for a particular utility has been called “adaptation” — following the etymology of fashioning for (ad) a use (aptus). No problem so far; only an apt choice of terminology. But if “adaptation” denotes the process of crafting or creating for a use, what shall we call the resulting structure so used. We usually call the structure an “adaptation” as well — again no intrinsic problem, for we often use the same noun for a process and its results (“construction,” “building,” etc. to cite some analogs in the same architectural domain).
But problems may arise in historical systems if the current utility of an adaptation (the noun used for the result) did not arise by the process (also called adaptation) that built the result at its initial appearance — for, under the Nietzsche-Darwin principle of quirky functional shift, the form of the current adaptation (feature) may have arisen by adaptation (process) for a very different role. (Similarly, the building on my corner now serves as a shelter and soup kitchen for homeless people — a utility not directly related to the purpose of its initial building as a church. We may not become confused in this case because we know the short history of this site, and the current use does not stray far from the stated ideals of the broader institution that originally raised the structure. But we could make some serious errors if we maintained a strong interest in long histories with spotty records featuring multiple episodes of functional shifting, and then assumed that the use of a current building automatically revealed the intention of its original building. When we recognized and generalized the error in such reasoning, we might even want to make a terminological distinction between our name for the current object and our name for the process of its original construction.)
In fact, I am not inventing an abstract or overfine distinction here. This very problem has been directly, even urgently, addressed in some of the most widely read and respected writings in evolutionary biology. When Williams (1966) composed his classic defense and explication of adaptation, he wisely identified adaptation as an “onerous” concept, to be invoked only when truly necessary, and restricted to a clear domain of unambiguous definition and use. He recommended, in particular, that the term be applied to a current feature only when we can “attribute the origin and perfection of this design to a long period of selection for effectiveness in this particular role” (1966, p. 6). He even advocated a terminological distinction between the use of such a genuine adaptation (its “function”) and the use, potentially just as crucial to an organism's survival, of a feature not crafted by selection for its current role (and therefore not an adaptation in Williams's restricted terminology). Williams suggested that we call this second form of fortuitous utility an “effect” — giving as an incisive, if somewhat facetious, example the propensity of flying fishes to fall back into the water as an effect (not the function) of the organism's mass. In other words, Williams invoked the term “effect” to designate the operation of a useful character not built by selection for its current role.
Although Darwin never formalized the issue, he clearly intended to restrict “adaptation” to Williams's sense of structures built by selection for their current [Page 1231] utility — for he explicitly denies that an “indispensable” feature of mammalian development should be called an adaptation (1859, p. 197): “The sutures in the skulls of young mammals have been advanced as a beautiful adaptation for aiding parturition, and no doubt they facilitate, or may be indispensable for this act; but as sutures occur in the skulls of young birds and reptiles, which have only to escape from a broken egg, we may infer that this structure has arisen from the laws of growth, and has been taken advantage of in the parturition of the higher animals.”
But if we follow, as I believe we should, this restrictive clarification advocated by Darwin and Williams, what shall we call a feature that initially arose for a reason different from the selective basis of its current operation — even though this present utility may be as crucial to the organism's adaptive success as the function of any organ built directly by selection for its current role? Indeed, and curiously, the lexicon of evolutionary biology, until recently, included no name for a feature that now contributes to an organism's fitness in natural selection, but that arose for a different reason — the very kind of outcome whose explication had been recognized by Nietzsche as “the major point of historical method.” In other words, we cannot claim that the previous absence of such a term merely recorded the irrelevancy or peripheral status of the concept.
Evolutionary biology has long recognized a name for a related aspect of this phenomenon — but I cannot think of a more infelicitous term in our entire lexicon, explicitly so lamented and identified by scores of biologists. Because we have acknowledged the principle of quirky functional shift, if only for Darwin's own need in refuting Mivart's critique, we have felt some pressure to recognize a term for the potential utilities inherent in original uses. What should we call a feather's potential for flight while it still resides on the forearm of a small running dinosaur, functioning only for thermoregulation? Evolutionary biology has generally referred to such latent potentials as “pre-adaptations.”*
For two reasons, “preadaptation” cannot fulfill our need for a term to designate features that arose for reasons different from their current utility. [Page 1232]
1. Preadaptation can only describe a potential future utility of a feature operating in a different manner in an ancestor. The thermoregulating feather may be called a preadaptation for flight. But when birds then coopt feathers as essential components of an airborne wing, we surely cannot continue to call them preadaptations for their current utility! I simply refuse to be called a “wannabe scientist” (or even a “promising scientist”) because I once had a dream, and even (in retrospect) some inherent capacity for its realization, as a kid on the streets of New York.
2. What term in all our lexicon has ever come to us so inherently “prepackaged” for inevitable trouble and misunderstanding? The motivation behind the name may be clear and fair enough — the desire to recognize a different potential in a current actuality. But in our real world, where we so often allow our hopes for intrinsic meaning to obscure the realities of a natural order — random and senseless in human terms, and replete with “bad things happening to good people” — we guarantee ourselves nothing but trouble when we invent a word with a “plain meaning” of foreordination as a description and definition of our best examples to illustrate the precisely opposite concepts of fortuity and contingency. The resulting, entirely predictable, confusions became legion in biology classrooms, and professors developed a tradition for explicating and apologizing in advance whenever they mentioned “preadaptation.” Terms that automatically evoke such embarrassment must be fatally flawed and fit only for the favored anathematization of my childhood years: “good riddance to bad garbage.”
I could present a catalog of such textbook apologies, but will cite only Frazzetta's lament (1975, p. 212) to prove that my fulminations at least cannot be called idiosyncratic: “The association between the word 'preadaptation' and dubious teleology still lingers, and I can often produce a wave of nausea in some evolutionary biologists when I use the word unless I am quick to say what I mean by it.”
> To rectify this odd situation of a missing term at the center of a key subject in evolutionary biology, Vrba and I proposed that features coopted for a current utility following an origin for a different function (or for no function at all) be called exaptations — that is, useful (or aptus) as a consequence of (ex) their form — in contrast with adaptations, or features directly crafted for their current utility. Adaptations have functions, and exaptations, following Williams's recommendation, have effects. We summarize our recommendations in Table 11-1 (from Gould and Vrba, 1982).
This coinage completes a logical structure that has been recognized ever since Darwin (and made explicit ever since Nietzsche) but that never included a term for one of the central rooms in the edifice. (My reasoning may be both simplistic and self-serving, but I can imagine only one explanation for such a curious situation: following Darwinian traditions, and especially under the orthodoxy of the “hardened” version of the Modern Synthesis, biologists became so accustomed to regarding all evolutionary change as adaptation directed by natural selection that they lost sight of the importance, or even the existence, of an undeniable corollary — that many (indeed most) features, as a
[Page 1233]
Table 11-1. A Taxonomy of Fitness.
Process
Character
Usage
Natural selection shapes the character for a current
use—adaptation
Adaptation
Function
A character previously shaped by natural selection
for a particular function (an adaptation), is co-
opted for a new use—cooptation
Exaptation
Effect
A character whose origin cannot be ascribed to the
direct action of natural selection (a nonaptation),
is coopted for a current use—cooptation
Exaptation
Effect
consequence of quirky functional shift, do not reveal their original evolutionary context in their current utility. If all phenotypic traits are adaptive, and built by adaptation, why bother to make a formal distinction between features crafted, and features merely coopted, for their current utility?
But our renewed respect and attention to structuralist themes now makes such a formal distinction essential. Thus, Vrba and I recommended that features crafted for current use continue to be called adaptations (adopting the restriction advocated by Darwin and Williams), and that features coopted for current use, following an origin for some other reason, be called exaptations. We would also prefer that biologists embrace “aptation” rather than “adaptation” as the general descriptive term for a character now contributing to fitness, with exaptation and adaptation defined as the two sub-categories of aptation, thus designated to recognize the crucial distinction between cooptation and direct shaping in the historical construction of characters.
This simple terminological strategy addresses the fair criticism that we can often only know the current basis of fitness — when we do not have enough evidence to determine whether a character developed as an exaptation or adaptation. In such cases, under our scheme, we refer to the character as an “aptation” and leave the further specification of its origin unaddressed. (Our current terminological conventions operate in this manner after all, for I may call a character an adaptation whether I accept Paley's belief in divine creation or Darwin's mechanism of origin by natural selection. Both authors did, indeed, call useful structures “adaptations.”)
In an ideal world (and if I held the powers of a czar, which would, of course, then make such a world unideal ipso facto) I would fight for the full scheme, and campaign to replace “adaptation” with “aptation” as a base-level description (with no implication about mode of origin) for features now contributing to fitness. But I know the odds against unseating centuries of usage for a word that not only serves as a staple of vernacular speech, but also enjoys unparalleled professional salience as a standard-bearer for our preferred evolutionary theory. I don't play the lottery, and I don't understand the recreational appeal of skydiving or bungee jumping. So I will mortify my desires and learn to live with the traditionally broad use, thus facine with stoicism [Page 1234] all the attendant confusion between “adaptation” as a general “state term” for useful features (whatever their mode of origin), and “adaptation” as a more restricted “process term” for the subset of aptive features that arose in the context of their current utility. However, a few people do win lotteries and survive horrendous falls, so I will not surrender entirely. Dum spiro, spero.
On the other hand, and to paraphrase Mr. Huxley in a famous context, I am prepared to go to the stake for exaptation — for this new term stands in important contrast with adaptation, defining a distinction at the heart of evolutionary theory, and also plugging an embarrassing hole in our previous lexicon for basic processes in the history of life.
Key criteria and examples of exaptation
I cannot present a “review article” of empirical cases of exaptation, for the defining notion of quirky functional shift might almost be equated with evolutionary change itself, or at least with the broad and venerable subject of, in textbook parlance, “the origin of evolutionary novelties.” I will therefore focus on the fate and utility of “exaptation” as a term for describing the evolutionary result of functional cooptation from a different source of origin. Our term (first defined in Gould and Vrba, 1982, p. 4) has not swept the field, as I might have hoped in my arrogant or naive mode, but “exaptation” has certainly attracted a good share of attention and fruitful use — and may therefore be designated as adaptive for its original “intent.”
Above all, biologists have subjected the term to intense criticism and scrutiny (see, for example, Coddington, 1988, and Buss et al., 1998), from which “exaptation” has emerged with strength and proven utility. In my opinion (partisan, of course), Arnold (1994) has presented the best single illustration of exaptation's importance as a concept and its operationality as a tool of research. He begins by recognizing the need to distinguish exaptation from adaptation as subcategories of the more general phenomenon of “aptation” (for he accepts and utilizes our suggested name for the encompassing concept as well). He also emphasizes the crucial methodological point, as previously discussed for the comparable case of the invisibility of stasis under conventional definitions of evolution (Chapter 9), that exaptation must be explicitly defined within a revised theoretical framework, and cannot simply be “discovered” by researchers working within the paradigm of the hardened Modern Synthesis — because anything that “works” will be called an “adaptation” in the conventional theory, and will therefore be scrutinized no further for its potentially exaptive status (Arnold, 1994, p. 128): “One of the main reasons for trying to recognize exaptations is precisely because they are so easily mistaken for adaptations. If the two kinds of aptation are not differentiated, we risk the possibility of exaggerating the undoubted importance of adaptation in fitting organisms to their environments and of ignoring a phenomenon which, like advantageous mutation, is one of the main sources of beneficial accident in the evolutionary process.”
Arnold then turns to the operational utility of exantation, first refurinp the [Page 1235] arguments of those who found the concept intelligible, even interesting, but doubted that sufficient information could generally be obtained about the history of evidently functional features to make a proper distinction based upon inferences about prior states. Arnold argues that several advances, particularly the codification of cladistic techniques for phyletic ordering, have made the distinction operational in a sufficiently high percentage of cases: the formerly broad definition of “adaptation for all useful traits whatever their origin was reasonable at a time when it was difficult to find out how advantageous traits had arisen, unless this had been observed in recent populations. However, phylogeny reconstruction now allows many individual exaptations t
o be recognized with some certainty, and makes distinction of exaptive and adaptive origin of performance advantage appropriate” (p. 126).
The relative timings for the origin of a form and for the inception of its current function — as inferred either from the branching points of a cladistic analysis, or from direct knowledge of historical sequences — provide the main criteria for distinction of exaptation from adaptation. “For adaptation,” Arnold writes (p. 132), “a hypothesis is refuted if the new trait develops before the relevant selective regime. If the test is passed, it is possible to check whether the new trait really confers an advantage in the new regime that its plesiomorphic state does not.”
Arnold then asks how we should interpret the opposite phenomenon “in which a derived trait and a regime in which it gives a performance advantage first appear concurrently on the same node on a lineage” (p. 133). This situation of coincidence in cladogeny between form and function would seem to point to adaptation, but Arnold notes (p. 133) that an imperfect record must fail to provide evidence for several (probably most) events of speciation, and that traits may arise before selective regimes at these missing nodes, and then be compressed into coincidence with a current selective basis at the first recorded node of their joint occurrence. I accept this point as evidently valid, but favorable for tests of the importance of exaptation. As emphasized in other contexts within this book, ineradicable biases in testing a hypothesis present little problem, and may even constitute a blessing in disguise, when their direction works against the hypothesis under test — because the hypothesis gains stronger affirmation by success in the face of such unfavorable odds. Since missing nodes must, by Arnold's argument, induce an underestimate for the frequency of exaptations by redirecting some genuine cases into the opposite category of adaptations (sensu stricto), this bias does not pose problems for tests of exaptation. For example, and using these twinned criteria, Arnold found 70 percent of 61 apomorphies in the lacertid lizard genus Meroles to be “concurrent with occupation of the environmental situation” (p. 133) of their present function — therefore requiring that they be ranked as adaptations.
The Structure of Evolutionary Theory Page 196