Exaptation in Human Evolution: How to Test Adaptive Vs Exaptive Evolutionary Hypotheses

doi 10.4436/jass.89015 JASs Invited Reviews Journal of Anthropological Sciences Vol. 89 (2011), pp. 9-23

Exaptation in human evolution: how to test adaptive vs exaptive evolutionary hypotheses

Telmo Pievani & Emanuele Serrelli

University of Milan Bicocca, Piazza dell’Ateneo Nuovo, n. 1 - 20126 Milan, Italy e-mail: [email protected]; [email protected]

Summary - Palaeontologists, Stephen J. Gould and Elisabeth Vrba, introduced the term “ex-aptation” with the aim of improving and enlarging the scientific language available to researchers studying the evolution of any useful character, instead of calling it an “adaptation” by default, coming up with what Gould named an “extended taxonomy of fitness” . With the extension to functional co-optations from non-adaptive structures (“spandrels”), the notion of exaptation expanded and revised the neo-Darwinian concept of “pre- adaptation” (which was misleading, for Gould and Vrba, suggesting foreordination). Exaptation is neither a “saltationist” nor an “anti-Darwinian” concept and, since 1982, has been adopted by many researchers in evolutionary and molecular biology, and particularly in human evolution. Exaptation has also been contested. Objections include the “non-operationality objection”.We analyze the possible operationalization of this concept in two recent studies, and identify six directions of empirical research, which are necessary to test “adaptive vs. exaptive” evolutionary hypotheses. We then comment on a comprehensive survey of literature (available online), and on the basis of this we make a quantitative and qualitative evaluation of the adoption of the term among scientists who study human evolution. We discuss the epistemic conditions that may have influenced the adoption and appropriate use of exaptation, and comment on the benefits of an “extended taxonomy of fitness” in present and future studies concerning human evolution.

Keywords - Exaptation, Pre-adaptation, Spandrels, Adaptationism, Extended taxonomy of fitness, Operationality.

“To paraphrase Mr. Huxley in a famous existence, and at the same time as the process context, I am prepared to go to the stake for of differential survival of members of a biologi- exaptation; for this new term stands in important cal population. Like any concept which defines contrast with adaptation, defining a distinction at both the process and the product of the process, the heart of evolutionary theory, and also plugging adaptation is an ambiguous term. In fact, we an embarrassing hole in our previous lexicon for could define the mechanism of natural selection basic processes in the history of life” completely without using the term “adaptation”. (S.J. Gould, “The Structure of Evolutionary Moreover, “adaptation” is seldom quantified, Theory”, 2002, p. 1234) even today, and the degree of “fitness” is a more satisfying concept in evolutionary biology. Darwin was aware of the teleological remains A pluralistic taxonomy of fitness of the prefix ad- joined with “aptus”, meaning at that time “useful for”, and today “contributing to “Ad-aptation” is a pre-evolutionary term that the fitness of the bearer”. In fact, mixing together survived the Darwinian revolution, being recon- the need to search for the remote causes of the sidered as the feature of a trait which is useful evolution of a trait and the teleological fancy of for the individual involved in the struggle for “ad-adaptation”, any evolutionist runs the risk

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of reconstructing natural processes as “just-so- a widely different purpose, namely, respiration. stories”: eyes evolved “for” sight, legs “for” walk- The swim bladder has, also, been worked in as an ing, and so on. Furthermore, as in George St. accessory to the auditory organs of certain fishes. Mivart’s objection to natural selection, the idea All physiologists admit that the swim bladder is of a progressive adaptation seems to produce a homologous, or “ideally similar” in position and contradiction between the gradualist assumption structure with the lungs of the higher vertebrate about the functioning of natural selection, as a animals: hence there is no reason to doubt that slow and continuous generation-by-generation the swim bladder has actually been converted process, and the assumption of the functionality into lungs, or an organ used exclusively for of any trait that is positively selected. If the wing respiration” (p. 148) evolved gradually, with every stage being functional, what was the early phase of a wing for? Is In the final observations of the second edition it possible to fly with a small part of a wing? And of The various contrivances by which orchids are what about the beginning of a mimicry? fertilized by insects (1877) Darwin seems tempted The anti-evolutionary objection of the alleged to transform the tinkering of natural selection impossibility to use natural selection to explain the with forms and structures in a general principle incipient stages of any complex and useful struc- of the theory of evolution (as proposed, moreo- ture composed by an organization of different ver, by German marine biologist and founder of parts was effectively tackled by Charles Darwin in the Naples Zoological Station, Anton Dohrn, in the sixth chapter of the sixth edition of The Origin his correspondence with Darwin): of Species (1872), where he advanced two different explanatory hypotheses: firstly, a gradual imple- “The regular course of events seems to be that mentation of the structure through natural selec- a part which originally served for one purpose, tion, with a corresponding gradual improvement becomes adapted by slow changes for widely of the same function; secondly, the evolution of different purposes. ... Although an organ may the trait in a frame of primary selective pressures not have been originally formed for some special followed by a “functional cooptation” in a new purpose, if it now serves for this end, we are ecological situation where the same structure, or a justified in saying that it is specially adapted for slightly modified structure, acquires a new func- it. On the same principle, if a man were to make tion, which is independent from the previous one a machine for some special purpose, but were to and unexpected (like a potential “effect” already use old wheels, springs, and pulleys, only slightly held in its form). In order to make the second altered, the whole machine, with all its parts, mechanism possible, Darwin supposed that the might be said to be specially contrived for its relationships between forms and functions are present purpose. Thus throughout nature almost not strictly one-to-one, but potentially redundant every part of each living being has probably and flexible (with cooperation of parts, specializa- served, in a slightly modified condition, for tions, cooptations). diverse purposes, and has acted in the living So we can have classical evolution due to the machinery of many ancient and distinct specific gradual agency of natural selection maximizing forms” (pp. 283-284). the same function, but also the re-use and recy- cling of structures already available and previ- “Almost every part of each living being served ously evolved for other reasons: for diverse purposes” is an impressive general statement about nature. Nevertheless, the role of “The illustration of the swim bladder in fishes … “contrivances” (in other words, the role of trade- shows us clearly the highly important fact that offs between structural internal constraints, an organ originally constructed for one purpose, given by the history of the body plan, and selec- namely, flotation, may be converted into one for tive functions) has been widely underestimated T.Pievani & E. Serrelli 11

during the process of unification of Mendelism & Gould (1986) considered as further cases of and the Darwinian theory of evolution by means exaptation type 2 all the effects that an adapta- of population genetics. Only the first Darwinian tion at one level of evolution (genes, organisms, meaning of an improvement by natural selec- groups, populations, species) produces at another tion of one same function ascribed to a structure level: what is an adaptation at one level could be has been stressed, and functional adaptation has an exaptation at another (cross-level spandrels). always been a core concept in the study of human In other words, function does not always evolution, as well as in evolutionary biology in precede form: firstly, in evolution, structures general. In the works of some contemporary could repeatedly change the primary functions authors, this perspective has been stressed even they were initially selected for – the process rec- to the point of conceiving natural selection as an ognized by Darwin in 1872 and later named anthropomorphic “engineering force”, optimiz- “pre-adaptation”, the trait being “pre-adapted” ing the organisms and their behaviours part by for the current utility (a term refused by Gould part. The use of an “adaptationist” language and and Vrba because of its teleological taste) – or, the universal equation between current utility of secondly, they could emerge due to structural a trait and its historical origin were strongly criti- and historical causes, or for random insertions cized around 30 years ago (Gould & Lewontin, (neutral mutations, drifts), being later co-opted 1979), as they would prevent evolutionary biolo- for some function in different frames of selec- gists from being aware of mechanisms that differ tive pressures. That is why a current function from direct functional adaptation by optimiza- of a structure cannot be used as a default expla- tion and yet contribute in shaping living forms. nation of the past origin and evolutionary his- Palaeontologists Stephen J. Gould and tory of that structure. Hence the proposal of Elisabeth S. Vrba (1982) went further and an “extended taxonomy of fitness” comprising proposed the neologism “ex-aptation” (that is, pluralistically: a) standard adaptation (which is “aptus” from a pre-existing, evolved structure or not substituted by other processes); b) exaptation form) to address two mechanisms: 1) functional type 1, i.e. functional shift or the former “pre- shift (‘type 1’ exaptation in our terminology) adaptation”; c) and exaptation type 2, i.e. the in a Darwinian sense, i.e. the re-use by natural engagement by natural selection of non-adaptive selection of a structure with previously differ- traits (for further extensions and specifications ent purposes; 2) functional cooptation from non- see Gould & Vrba, 1982; Vrba & Gould, 1986; aptation (‘type 2’ exaptation in our terminology, Gould, 2002). or “spandrel”), i.e. an evolutionary mechanism In a pluralistic taxonomy the problem is not which, while leading to useful structures (always to choose between alternative explanations con- “aptations”, after all), is not completely described sidered as mutually exclusive in a general sense. as a process of standard functional adaptation Rather, the challenge is that of evaluating case by because the beginning of the emergence of a case the better explanation (adaptive or “exaptive” trait could be non adaptive (like a side effect, a in type 1 or 2), further calculating the relative developmental constraint, a structural effect, or a frequency in nature of one process or another. random insertion). ‘Type 2’ exaptation was only The experimental frequency of exaptations sometimes touched on by Darwin, as in the case (often still called “pre-adaptations” in literature) of the skull sutures: originating as a developmen- is today widely recognized (Arnold, 1994), also tal constraint and then “re-used” in mammals in University textbooks (Ridley, 2004), mainly as an adaptation to delivery. It is important to in fields such as evolutionary developmental remind the reader that “non adaptive” is different biology, the evolution of cognitive faculties and, from “non functional”, because we could argue since François Jacob’s “Evolution and Tinkering” that in many cases the previous “non aptations” (1977, where “the final example of tinkering” was had structural or developmental functions. Vrba “the human brain”), in evolutionary molecular

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specifiability of exaptation. Then we refer to a wide survey (available online) of the use of exaptation in literature since 1982, touching different fields of research in human evolution (morphology and physiology, language, genetics, behaviour etc.). In the final discussion, we draw some conclusions about the epistemic conditions which possibly influence the applicability and operationality of exaptation in different research contexts.

First case study: the scalloped dentino-enamel junction

Daisuke Shimizu and Gabriele A. Macho studied the contact surface, inside teeth, between Fig. 1 - The scalloped appearance of the den- two very different materials: «the hard, brittle tino-enamel junction (DEJ). Drawn following enamel and the much softer dentine» (Shimizu Shimizu & Macho (2007), Fig. 2. & Macho, 2007). This dentino-enamel junction (DEJ) has a “scalloped” appearance in biology. Here we consider the welcoming of an primates (Fig. 1). Recent biomechanical studies “extended taxonomy of fitness” in the study of seemed to indicate a possible function for this human evolution. micromorphological structure, i.e. preventing Some authors (like Dennett, 1995) have delamination which can occur during mastica- criticized the concept strongly because they sup- tion. Through 2D and 3D models, Shimizu and posed it implied a suspension of natural selec- Macho tested the mechanical benefits of scallops, tion: on the contrary, as is clear from its history showing that scallops actually: and its precise meaning, exaptation is not incom- -- reduce and discontinue stress concentra- patible with natural selection, but with an over- tion, with a resulting crack-stopping effect simplified representation of it. Other authors on enamel; (like Pinker, 1994) thought that exaptation does -- reduce sliding between dentine and enam- not represent an alternative mechanism, but can el, so that they are pushed into each other always be traced back to classical neo-Darwinian rather than apart. adaptations. However, as we have seen, this is Being the functional value of scallops ascer- true only for exaptation type 1, not for exapta- tained, it could be easily concluded that scalloped tion type 2 and cross-level spandrels. DEJ is a dietary adaptation for high bite force A more substantial objection to exaptation is and/or hard food, but Shimizu & Macho are cau- that it is not operationally distinguishable from tious in establishing a causal relationship between adaptation: we could call this the non-operationality masticatory loads and DEJ microstructure: objection. To help cast light on the non-operationality objection, we begin by analyzing the use of “inferring functional adaptations in evolutionary exaptation as a working concept in biology: in the biology is complicated. For a feature to constitute next two sections, we briefly review two exemplar an adaptation, it must fulfil a number of studies published in 2007 in Journal of Human criteria” (p. 110). Evolution which touch on exaptation. The section that follows is dedicated to a commentary of One of these criteria, considered and evalu- these two research studies regarding the operational ated by the authors in this case, is the consistency T.Pievani & E. Serrelli 13

between scallop formation and inferred bite force. If for further structural reinforcement […]. In scallops were a functional adaptation: taxa where scallops are not, or are only poorly, -- molars would be expected to have generally developed, other mechanisms that prevent more-pronounced scallops than the ante- delamination must be identified” (ibid.) rior teeth; -- scallops would be expected to be most If DEJ were straight, tensile stresses would push marked in species that exert high bite forces. the two tissues apart, but in such a case sliding could Though scallops are functionally advanta- be prevented through strong structural reinforce- geous, the comparative data available, albeit scant, ments such as von Korff’s fibers (see e.g. Bishop et do not support the latter two predictions. In search al., 1991). In summary, further studies should be of «some other explanatory model», Shimizu and carried out following a pluralistic approach: Macho advance a developmental hypothesis: “To ultimately resolve such issues regarding the “scallops are a by-product of biophysical processes phylogenetic and functional significance of scallops during ontogeny, which, owing to their functional at the DEJ […] a large-scale systematic study of advantage, are unlikely to be selected against. scallop morphology and distribution across taxa, Consequently, they may be viewed as an example sophisticated mechanical testing, and better insights of exaptation in primate biology” (p. 110). into developmental (i.e., morphomechanic) processes need to be brought together”. In particular, scallops may be viewed as a by-product of epithelial folding during odon- It must be noted that the question of the togenesis in development, uncorrelated with origin of scallops (exaptive-adaptive, structural- functional demands in adulthood, governed functional, plastic-genetically determined) is in by morphodynamic processes and mechanical no way trivial in paleo-anthropology, for scallops, forces (Shimizu & Macho specify that these pro- well preserved in fossils, are frequently used to cesses «can be described also without knowledge make inferences about phylogeny (species identi- of genetic networks»). Observations concerning fication and classification, common descent, e.g. thick enamelled species, such as the pronounced Haile-Selassie et al., 2004) and paleo-ecology appearance of scallops in fully formed teeth, (scallops as a predictive tool for diet and paleo- can be explained by additional biophysical pro- environment, e.g. Kay, 1975). cesses upcoming in later stages of ontogeny (e.g. enamel shrinkage during maturation) exaggerat- ing unevenness present at the DEJ during early Second case study: stages of development. In summary, Shimizu & the scaphoid-centrale fusion Macho’s hypothesis is a combination of exaptation (a structural by-product is co-opted for an The fusion of the os centrale to the scaphoid incidental subsequent function) and plasticity (a in hominoid carpus (Fig. 2) has been interpreted structural feature is enhanced during an organ- as a functional adaptation to stress on this joint ism’s ontogeny). during quadrupedal locomotion, which is par- Also, they recognize that, in the absence of ticularly accentuated in knuckle-walking. This scallops, some other structure would be supposed functional hypothesis has led to the suggestion to perform the same function: that the fusion is evidence for a knuckle-walking common ancestor of the hominine clade (Fig. 3). “For hominoids […] scallops may constitute an In modern humans (who are fully bipedal, not- advantageous mechanism that guards against knuckle-walking), the presence of this trait may delamination of enamel from the dentine be either a phylogenetic vestige or an exapta- core during mastication and without the need tion to a novel function: shear stress during

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varying developmental patterns, so Kivell and Begun had to find reliable benchmarks in development to establish the moment when the two bones should be clearly identifiable. Employing a system of age categories based on dental eruption they found that:

“the scaphoid and os centrale can be identified in well-preserved osteological specimens with dP3 as the last erupted tooth” (p. 328).

Kivell and Begun’s study indicated that the fusion appears to be primarily under genetic control, because a clear phylogenetic trend can be found among hominoids: in African apes (Pan, Gorilla) and modern humans fusion

Fig. 2 - Redrawing of a carpal drawing of occurs in almost all individuals (> 95%) and Hylobates leuciscus dating back to 1865 early in ontogeny, whereas in Asian apes (Pongo, (according to Kivell & Begun 2007, Fig. 3). The Hylobates) fusion occurs rarely (circa 7%) and absence of a line between os centrale (oc) and only in adulthood. In non-hominoid primates, scaphoid (arrow) in the original drawing has been interpreted as evidence of fusion between a consistent SC fusion – never reported or stud- these two bones. ied before – has been found in some species of Lemuroidea, but other ontogenetic processes power-grip positions. Since, however, «neither seem to be responsible for it. In fact, it appears to the functional nor the phylogenetic significance be a convergence with African apes, but no direct of scaphoid-centrale fusion is [so] clear», Tracy correlation with function can be found: L. Kivell and David R. Begun reconsidered the whole matter (Kivell & Begun, 2007), question- “Given that most of these […] taxa are only ing the very assumption that the fusion repre- broadly characterized as vertical clingers and sents a functional adaptation. leapers, or include this locomotor behaviour in All apes share a tendency to fuse their scaphoid their positional repertoire, a closer examination and os centrale, but they differ in the frequency of the biomechanics of the postural and locomotor and timing (by heterochrony) of this fusion: there uses of the hands in these taxa is needed to can be a range of intraspecific variability involv- determine the functional implications” (p. 334). ing sexual dimorphism, pathologies and anoma- lies, and lateral or bilateral fusion. One must also Neither phylogeny nor size are significantly check whether the fusion occurs under genetic correlated with the fusion in these Lemuroidea control or as a result of loading (i.e. plasticity). In species. In summary, more in-depth analyses of this regard, Kivell and Begun suspected that avail- carpal ontogeny, positional behaviour, and func- able literature lacked adequate sampling, and that tional morphology of these taxa are required. there were observational biases, and misinterpreta- For Kivell and Begun, «defining a character as tion of ambiguous cases. Therefore, before map- “adaptive” is challenging» (p. 336). Function (in ping the distribution of the trait in a complete this case, that the scaphoid-centrale fusion increases phylogenetic context, they conducted a primary stability during knuckle-walking) has to be demon- investigation on all involved species. strated with several kinds of studies such as: Absolute age cannot be used to evaluate and -- Fossil evidence: «To convincingly dem- compare the SC fusion in different species with onstrate that scaphoid-centrale fusion T.Pievani & E. Serrelli 15

Fig. 3 - Up-to-date phylogeny and taxonomy of living higher primates, based on molecular and morphological evidence (drawn after Wood, 2005).

occurred as an adaptation in African apes, continue to support this hypothesis, which is the we need fossil evidence that the appear- only one currently available: ance of this trait (i.e., the most parsimoni- ous hypothesis would suggest this charac- “We propose that this is a synapomorphy of the ter evolved once in the common ancestor hominine clade functionally associated with of the hominine clade) coincided with the digitigrady (knuckle-walking) that is retained appearance of knuckle-walking behaviour in humans as an exaptation for continued (associated with corroborative evidence in stability at the midcarpal and especially lateral other parts of the postcranial morphology)» carpometacarpal joints” (p. 338). (p. 336). «Fossil evidence for the origins of knuckle-walking coinciding with the ap- The adaptive hypothesis is subject to corrob- pearance of scaphoid-centrale fusion will oration through palaeontology as stated before, clarify the adaptive significance of this trait. and more studies are needed to clarify the same Evidence for knuckle-walking in a fossil trait in Lemuroidea. taxon lacking a fused os centrale would weaken or falsify this hypothesis» (p. 338); -- Biomechanical models and experimental data Exaptation: on compressive forces, aided by more and a working concept in biology more sophisticated computer simulations; -- The “convergence approach” analyzing the It may seem odd that even one of the main appearance of that character in unrelated exaptation enthusiasts in human evolution, Ian taxa: «A character correlated with the same Tattersall, seems to expose the argument to the behaviour in taxa that do not share a recent non-operationality objection, dealing with exap- common ancestor is statistically more likely tation as a general pattern of evolution in a broad to be specifically adapted for that behaviour sense and assuming that any evolutionary nov- because the effects of phylogeny have been elty must be an exaptation: removed» (p. 337). None of these, however, can conclusively “Strange though this might seem, [exaptation] support the functional hypothesis that the SC actually reflects a general pattern in evolutionary fusion is an adaptation for stability and com- history. I have already noted that, in evolution, pression during knuckle-walking. However, at form must precede function and that innovation this point of their research, Kivell and Begun itself cannot be driven by natural selection.

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Any novelty has to arise spontaneously as an observations and tests, aided by new digital exaptation, a structure existing independently of techniques for visualization and modelling, any new function for which it might later be co- are needed to better understand and evaluate opted” (Tattersall, 2004, p. 25). the supposed functional value of structures. 2) To test for effective correspondence between Ian Tattersall used exaptation as a power- structure and function in living and fossil spe- ful explanatory hypothesis for a clearly defined cies: the two studies above are examples of subject, though crucial, such as the emergence of the fact that adaptive hypotheses need to symbolic intelligence in Homo sapiens during the be supported by consistency between the Palaeolithic Revolution. However, in the citation considered structure and function (scallops above he expressed a more radical perspective and high bite force; SC fusion and knuckle- seeing exaptation (in prevalence type 2) as a gen- walking). If the distribution of a trait such as eral evolutionary pattern. It is noteworthy that the SC fusion is random regarding locomo- Stephen J. Gould himself assumed a similar posi- tor behaviour and lifestyle, an adaptive hy- tion at various points in his work. Interestingly, pothesis is undoubtedly weakened. On the the statement below occurs in the very work contrary, the “convergence approach” cited where he examined most of the points we make by Kivell and Begun can potentially give here about the operationality of exaptation: strong support to an adaptive hypothesis. The amount of intra-specific variation of the “I cannot present a ‘review article’ of empirical structure has to be taken into account and cases of exaptation, for the defining notion of studied. Tighter tests can be done by map- quirky functional shift might almost be equated ping the occurrence of the structure within with evolutionary change itself, or at least with the organism (e.g. scallops only in molars). the broad and venerable subject of, in textbook 3) To explore multiple functions of a structure: parlance, ‘the origin of evolutionary novelties’” functions that are now secondary (and may- (Gould, 2002, p. 1234). be underestimated by researchers) could have been primary in the evolutionary But, if exaptation type 2 aspires to the role of past. As a Darwinian process, exaptation general and ubiquitous pattern, replacing adapta- is bound to functional redundancy which tion and relegating natural selection as a second- allows for gradual shift between functions. ary force of refinement, then a really pluralistic For example, Shimizu and Macho state that and integrative perspective is avoided, and two researchers have considered scallops primar- possible options remain: either (1) to use the term ily as a crack-stopping mechanism. Now exaptation in place of adaptation; or (2), more experimental studies reveal that the latter probably and economically, to drop the newest function has been overestimated: scallops term. However, contrary to this dichotomy, the prevent delamination of enamel as their two studies described above show that at least six primary function, with crack-stopping as directions of research can effectively contribute an indirect effect. to operationally discern exaptation from adapta- 4) To explore structural alternatives for the con- tion case by case (see also Gould, 2002): sidered function: e.g. in taxa with poorly de- 1) To employ biomechanical studies and models veloped scallops, or no scallops at all, other to analyze function: driven by an adapta- structural reinforcement such as Korff’s fib- tionist and selectionist metaphor – accord- ers can prevent teeth enamel delamination. ing to which adaptation has no need to be The existence of actual structural alterna- tested for – several studies may have too tives for the same function can weaken the easily attributed functions to structures. The structure-function correspondence neces- two we described above show that further sary for a strictly adaptive hypothesis. T.Pievani & E. Serrelli 17

5) To enlarge phylogenetic context and improve a general process, but within a pluralistic frame knowledge: an accurate account of the oc- of “interconnected adaptations” and appropri- currence of the considered trait in a com- ately applied to specific cases, like the evolution plete phylogenetic tree is the foundation to of bipedalism or the exaptive effects of develop- understand the balance between phyloge- mental mutations in Homo sapiens. netic information (common descent) and We will comment below on the amount of functional information (features relative to work needed to discern adaptation and exapta- environment and lifestyle) carried by the tion. We note here that such investigations can trait. Previously unincluded species (such deepen our knowledge of considered traits and as Lemuroidea in the SC fusion example) evolutionary processes, avoiding some misinter- can be added as an external group to the pretations about phylogeny and functionality in analysis to discern exaptive and adaptive species and organisms. processes. Random distributions could be found, and can be either accepted or used as a basis for further research (as in the case A survey of literature of the SC fusion in Lemuroidea). 6) To improve knowledge concerning ontogenetic Our survey is fully available online at the and developmental processes underlying the URL http://hdl.handle.net/10281/19392 (com- structure: adaptationist views often rely on plement part I). In the present section, we refer the assumption of direct genetic control to publications listed therein through bracketed upon structures. The two studies presented numbers [] followed by the year of publication. above employ a more integrated view of on- Classic model examples like the Panda’s togeny and development. Structures like the thumb (Gould, 1980) and very recent articles SC fusion or a scalloped DEJ can result from (see cases above) elect morphological and physi- usage through the life of organisms, so a ological aptations as a field for a clear and fruit- study on the timing of the structure (particu- ful employment of the exaptation concept. For larly, but not only, the timing before or after many years, however, the use of exaptation in birth) can give important clues about the de- this domain was limited to some publications in gree of genetic control. Shimizu & Macho’s cultural anthropology ([57] 1983; [112] 1984; hypotheses concerning «morphodynamic [113], [137] 1986; [141] 1994; [47], [95] 1995) processes and mechanical forces» show that and medicine ([72] 1985; [67] 1997; [19] 2002; «genetic networks» are only one level of fac- [12] 2003; [23], [159] 2004; [160], [20], [158] tors acting in pre-natal development, which 2005; [102], [125] 2007; [148], [62] 2009), the thus requires multiple levels of analysis. latter expressing detailed speculative hypotheses The two studies we considered share a com- about human morphological and physiological mon attitude towards adaptation: if adapta- exaptations. There are a few interesting excep- tion is one of the possible processes leading to tions, which deal with the evolution of physi- a structure in evolution, it cannot be taken for ological traits in humans ([121] 1985; [135] granted and must be demonstrated, and this 1996), paleoecology ([65] 1987; [66] 1988), and demonstration is often challenging and demand- of morphological traits in our primate relatives ing. According to an “extended taxonomy of fit- ([48] 1986; [142] 1990; [29] 1992; and more ness”, a trait contributing to fitness should be recently, [122] 2004; [118] 2009). Despite some named “aptation” in absence of a corroborated exceptions ([143] 1986), paleoanthropologists theory about the evolutionary mechanism(s) did not really begin to use the concept in their responsible for it (adaptive or exaptive). Also in empirical work until recently ([152] 2002; [10], Giorgio Manzi’s reconstruction of human evolu- [58] 2007; see also, of course, [74], [136] 2007, tion (2007), we see that exaptation is handled as together with the related [110] 2005, and the

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anticipatory [117] 1996), with promising results now integrated in the frontier of research into the (cf. e.g. [109] 2011). origin of language ([91] 2006; [64] 2008). It is useful to divide the field of human lan- (2) In 1990, the linguist, Roger Lass, intro- guage into two non-overlapping sub-areas: (1) duced an approach in the study of language studies on language origin and (2) studies on change which used biological evolution as a language change. model, and considered exaptation as a mecha- (1) Since 1990, exaptation has been exten- nism with a high relative frequency. He suggested sively employed in discussions about the evolu- that language contains much “morphological tionary origin of language ([111] 1989; [114] junk” that «as an alternative to being scrapped, 1990; [90] 1991; [105] 1993; [155] 1995; [31] gets put to use – albeit a kind of use that has 1999; [27], [75] 2000; [8], [24] 2002; [108], little to do with either efficient communication [21] 2007). Our survey shows that contribu- or the organization of extralinguistic experience» tors in this field, although sharing the concept ([83] 1990, p. 814). Lass’s approach was largely whereby exaptation has played a role in the origin welcomed in subsequent years, being applied in of language, spent considerable time and energy the explanation of several peculiar traits of differ- in trying to make it clear what could actually have ent languages around the world ([70] 1994; [28] been exapted in such an evolutionary process 2000; [5], [103] 2002; [41] 2003; [50] 2004). (e.g. “cognitive systems”? “calculus categories”? More general works have also been published “motor control processes”? “underlying neural ([13], [144] 2006). Despite general critiques to organization”? “brain areas”?…). For example, the application of evolutionary thinking in lin- in recent years a remarkable debate started in guistics ([34] 2006), exaptation has come to be Science ([61] 2002) and has continued in other regarded as a key concept in understanding some journals ([115], [45], [69] 2005; [13] 2006), important aspects of language change. where the focus quickly shifted from exaptation Genetics and molecular biology appear to be to the general framework concerning the model- the fields of greatest success of exaptation: a lot ling of language. This situation led some authors of studies have been published showing evidence interested in exaptation and language to point of functional cooptation of genetic sequences and out that the lack of a general theory of language genomic features, and functional shift of (multi- definitely prevents the evaluation of exaptive ple copies of) existing genes (some examples are hypotheses concerning its origin (see [16] 2001; [22] 1999; [99], [123] 2000; [82] 2002; [124] [17] 2002). Meanwhile, a neuro-anatomical 2003; [79], [18] 2005; [133] 2004; [52] 2006; approach emerged that began to search for “neu- [76], [49], [87], [86], [157] 2007; [32] 2008). ral substrates” underlying human language. Born Moreover, Evo-devo recently showed that evo- in the 1980s, this research flourished in the late lutionary novelties often consist in differing ‘90s ([2] 1997). Even in absence of a complete modulation and genetic regulation of conserved and shared theory of language, clues coming from developmental processes ([1] 2007; [30] 2005). analogies and homologies between humans and Due to their very nature, studies in this field primates ([38] 1998; [35] 2005; [51] 2006) and involve humans together with wide taxa such as functional imaging of neural activity and mirror mammals (e.g. [140] 1999; [4], [88] 2004; [139] systems ([9] 2003; [37] 2005; [104], [101] 2007) 2006; [80], [128] 2007) or vertebrates (e.g. [97] strengthened the hypothesis that the evolutionary 2005; [11] 2006; [98] 2007). Some papers deal- origin of human language happened by coopta- ing specifically with human genes, or referring tion for novel functions of pre-existing neural explicitly to human evolution are: [59] 1996; structures and processes (modern human Broca’s [94], [81] 2001; [134], [78] 2004; [79] 2005; area homologous to area F5 in macaques, mirror [60] 2006; [116], [132] 2007; [68], [150] 2008. systems, motor control mechanisms). Our survey A complex situation can be found in stud- shows that a theory of multiple exaptations is ies on human behaviour, cognition, culture, T.Pievani & E. Serrelli 19

social organization, which we can group here authors to use the concept in making sense of under the general label of anthropology (seen as particular, apparently non-adaptive behaviours a strongly interdisciplinary field). Early papers such as geophagy ([154] 1998), suicide ([129] used exaptation in studying human behaviours 2005), or homosexuality ([73] 2000). See also such as tool making, hunting, food cooking and [93] 1996. Exaptation was used in philosophi- sharing, early weaning, social structure, and the cal, psychological and neuro-scientific studies evolutionary origin of culture ([14] 1983; [119], on particular “human universals” such as dreams [138] 1989; see also [42] 1994; [120] 1998; [6], ([46] 1995), art ([39] 2004), creative thought [3] 2003; [71] 2005; [85], [43], [156] 2008). ([131] 2005), the “rule of thumbs” ([126] 2005). Despite this interest, it seems that initially exap- The exaptation concept was also “co-opted” in tation was poorly known, and some authors tried the context of organizational and societal stud- to introduce the term in debates in order to re- ies ([92] 2002). Regarding language, a growing label processes described by others. Meanwhile, emphasis is being put on neuroscience, and in exaptation was viewed as a potential source of particular on ancestral features like mirror neu- conceptual change in cognitive sciences as well as rons, cortical maps, motor activity co-opted in in evolutionary theory ([111] 1989; [77] 1999). modern humans ([38] 1998; [21], [36] 2007). Various papers have employed exaptation in evo- Archaeology ([106] 1992; [107], [96] 1998) and lutionary hypotheses about the origin of human technological studies ([33] 2002; [130] 2006; cognition ([44] 1993; [84], [149] 1996; [26] [40] 2007) also became interested in exapta- 2000; [7] 2007). tion. To sum up, we find here an early appeal In particular, paleoanthropologist, Ian and a gradual acceptance of the concept, which Tattersall (e.g. [145] 2000; [146] 2002; [147] appeared to be a possible explanation in cases 2004), strongly proposed exaptation as the mech- where classical selectionist and adaptationist anism for the origin of modern human behaviour: explanations fail. current physical abilities of human beings seem to have emerged together with the appearance of anatomically modern humans around 200 000 Discussion: epistemic conditions - 150 000 years ago. However, they remained influencing the use of exaptation hidden until some other mechanisms activated them; probably, a cultural stimulus (articulated Our survey demonstrates there is a general language) was the main factor that triggered the acceptance and use of exaptation in all fields of development of abstractive and symbolic think- study of human evolution. At the same time, the ing. Therefore, new behavioural and cognitive survey allows us to consider the epistemic condi- modes in modern humans would seem to have tions which possibly influence its application. arisen as exaptations, and this remains one of First of all, the strong persistence, in litera- the most effective and promising explanations ture, of the term “pre-adaptation” (or “preadap- for the apparent gap between the evolution of tation”) must be taken into account as a general anatomically modern humans and the rapid and condition. In a rough count of the occurrences of global emergence of cognitively modern humans the two terms in some journals and databases, we (see also [100] 1989). found both in varied relative frequencies, with The emergence of human behaviours by a prevalence of pre-adaptation (exact ratios can exaptation compromises strictly gene-based and be found in the online complement, part II, at selectionist explanations of specific behavioural http://boa.unimib.it/handle/10281/19392). traits in humans. On the one hand, this con- Presently, “pre-adaptation” is preferred by several sequence was actively contrasted by evolution- authors, despite being only partially synonymous ary psychologists ([25] 1998; [63] 2003; [127] to exaptation. As we have seen, Gould & Vrba 2008). On the other hand, it induced several (1982) proposed exaptation as a substitution of

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the term (because of its misleading finalistic fla- whole or specific components of it, and whether vour) and an extension of the concept of pre-adap- they regard exaptation type I (“preadaptation or tation, including functional cooptation of struc- functional shift”, Botha, 2002) or type II (“by- tures which did not originate by direct action of product conceptions of language origin”, Botha, natural selection. The choice by some authors 2001). In such a situation, a sufficiently restric- and some fields of using “exaptation” instead of tive theory of exaptation is not possible, and “pre-adaptation” can be seen as a welcoming of exaptive hypotheses cannot be properly tested: one or both of these arguments. Secondly, the possibility to identify structures “…a concise definition of the term “exaptation” appears to be a conditio sine qua non for stud- or “preadaptation’” accompanied by little more ies on exaptation to be continued. Based on than a referential bow in the direction of Charles decoupling between structure and function, Darwin, cannot suffice […] we require a theory these studies are hardly viable in situations where of language genesis that assigns a given feature structures and substructures are not clearly dis- of language the status of “exaptation” in a non- tinguishable. As we have seen in our survey, in ad hoc and non-arbitrary way […] a theory of the study of the evolutionary origin of language, evolution which places general constraints on exaptation did have to wait for the appearance assigning the status of ‘exaptation’ rather than of new approaches and (in specific, neuro-scien- that of ‘adaptation’ to an arbitrary character or tific) technologies capable of identifying structures structure” (Botha, 2001, pp. 32-33). to be studied – i.e. what can possibly have been exapted – in order to fully develop its explain- In absence of such a theory – which is, we ing potential. Differently, exaptation was rap- can say, operationally specifiable – it is unclear idly spread in evolutionary models of language «what kinds of evidence are properly relevant to change (where many recognizable linguistic the appraisal of exaptationist claims». We can structures are available) as well as in genetics observe that, in general, the strength of the non- and molecular biology (where genetic sequences operationality objection to exaptation appears to allow a remarkably precise identification). Where be relative to the particular field and moment of conditions do not make it possible to identify study, qualified by the possibility of recogniz- structures and substructures (as in non-neurosci- ing structures and performing various kinds of entific studies of language or in the last examined research. In every field of human evolution, such field of anthropology), exaptation bears a mark- conditions are constantly susceptible to change: edly speculative status, although it still continues even in the study of morphological and physi- the important function of stimulating debate on ological features, as we have seen, novel tech- general evolutionary models, anticipating and nologies for modelling, visualizing and analyzing directing further research. features today open new possibilities of research. Thirdly, tightly bound to the second, is the Considering examples of morphological and possibility of doing research in the multiple direc- physiological features makes it evident that the tions we enumerated in the section “Exaptation: acceptance of an extended taxonomy of fitness seems a working concept...” above. Again, language ori- to be very demanding for researchers: the possi- gin offers an example. In 2001 and 2002, in eval- bility of exaptation implies a greater amount of uating several exaptive hypotheses on the origin multidirectional work (to identify structures, dis- of language, the linguist Rudolf P. Botha com- cuss and evaluate exaptive vs. adaptive hypoth- plained about the impossibility to perform stud- eses) than a default acceptance of adaptation. ies about “historical order” (which can be likened This is even more evident in studies on small to our point 2) and “comparative anatomy” (5) and seemingly minor traits such as the dentino- to test exaptive hypotheses (here Botha follows enamel junction or the scaphoid-centrale fusion. Gould, 1997), whether about language as a We hypothesize that this can influence, and T.Pievani & E. Serrelli 21

more specifically delay, the acceptance and use of taxa (i.e. if we are supporting the exap- exaptation together with context-dependent con- tation of certain pre-existing structures straints such as the availability of resources and in the origin of human communication, time. From a theoretical point of view, however, we are not bound by principle to find a these constraints cannot justify the dropping of a fixed, high continuity or identity between concept which can help to clarify important epis- humans and modern primates. Important temological and methodological issues. The suc- modification of structures could, in fact, cess of broad and demanding studies employing have led to large gaps, so, while exapta- exaptation in extending knowledge about mor- tion is suitable to explain particular con- phological and physiological traits and evolution- tinuities, continuity vs. discontinuity is a ary processes is supposed to positively influence completely separate issue, and hypotheses the adoption of an extended taxonomy of fitness, in the two domains cannot be hastily used at least in the promising field of human mor- to support each other); phology and physiology. b) graduality vs. saltation: although exapta- In literature, there are particular situations tion can contribute to explain abrupt evo- in which adoption of exaptation seems to be a sort lutionary changes, such as the emergence of fall back, forced by the failure of preferred of “human consciousness” in Tattersall’s adaptationist explanations. These cases are fre- hypothesis, the speed of the process is a quent, for example, in the multidisciplinary field separate issue, whereas even «a qualita- of anthropology, where conditions second and tive discontinuity between extant species third (above) are particularly problematic. Our could have evolved gradually, involving review shows that the situation leads researchers no discontinuities during human evolu- to stress, instead of the exaptation mechanism tion». In other words, the possibility of a itself, two aspects related to it: a particular con- rapid change is a particular, unnecessary sequence and a correlated theme. It seems that consequence of exaptation. Moreover, such an emphasis can lead to possible miscom- historically the term “discontinuity” in prehension of the concept: evolutionary biology opens the possibility 1) The stressedparticular consequence of exap- of “saltationist”, anti-Darwinian interpretation is the possibility of accelerated evolu- tations which are absolutely unintended tionary change: it appears that the sudden and largely unaccepted by the scientific appearance of complex traits such as “hu- community at present. man consciousness” cannot be explained by 2) Often, when exaptation is evoked in ex- gradual adaptation. In such cases, exapta- plaining rapid change (or, for example, tion seems to be a sort of emergency back deep continuities between taxa), it happens door to be used in evolutionary explana- that its core – functional shift or cooptations. But it has to be pointed out that the tion – becomes lost in favour of a corre- distinctive mark of exaptation is change of lated theme: the one about non aptations, function (by shift or cooptation), and the constraints and sub-optimality. Exaptation latter must be kept distinct from the two type II implies existence and relevance, in other – however correlated – problems organisms, of: non-aptations, i.e. structures which are clearly indicated in an article by with no function, neutral to fitness, which Marc Hauser, Noam Chomsky and Tecum- are the raw material to be co-opted for novel seh Fitch (2002, p. 1570): functions; structural constraints, by which a) continuity vs. discontinuity: exaptation of side-effects propagate in the organisms sub- a structure occurring in a taxon does not sequent to every selective pressure, produc- imply any particular kind or degree of ing by-products and non-aptations. More continuity between that taxon and related generally, exaptation (both types) gives an

www.isita-org.com 22 Exaptation in human evolution

image of evolution as a suboptimal process, http://boa.unimib.it/bitstream/10281/19392/1/ dealing with constrained structures and PievaniSerrelliJASS2011online_complement.pdf. working like a tinkerer, with limited avail- We thank our anonymous referees for their very help- able material which is ever-changing. For ful comments and corrections. these correlated themes, it is easily under- standable for exaptation to draw the atten- tion of researchers who try to make sense References of maladaptive, suboptimal, or just bizarre traits. Exaptation has, indeed, much to do Arnold E.N. 1994. Investigating the origins of with constraints and non-adaptive effects. performance advantage: Adaptation, exaptation However, this explanatory route ends up, and lineage effects. In P. Eggleton & R. Vane- once again, neglecting the specific core of Wright (eds): Phylogenetics and ecology, pp. 123- the concept: functional shift and cooptation 168, Academic Press, London. (see several articles in our review, e.g. [47]). Bishop M.A., Malhotra M. & Yoshida S. 1991. The meaning of the notion appears to be Interodontoblastic collagen (von Korff fib- reduced to “no adaptation” or “oddities”. ers) and circumpulpal dentin formation: an In conclusion, since 1982 exaptation has ultrathin serial section study in the cat. Am. J. been welcomed and used in research on human Anat., 191: 67-73. evolution. Examples show that it can be a work- Botha R.P. 2001. How much of language, if any, ing concept in biology, operationally specifiable came about in the same sort of way as the and helpful in better understanding human traits brooding chamber in snails? Lang. Comm., 21: and evolutionary processes. A comprehensive lit- 225-243. erature review reveals various situations: while Botha R.P. 2002. Are there features of language exaptation has become a key concept in several that arose like birds’ feathers? Lang. Comm., 22: fields, different epistemic conditions of applica- 17–35. bility of the concept can be found. But research Darwin C. 1859. On the origin of species, 1st ed. in all fields of human evolution appears itself to John Murray, London (sixth ed. quoted, 1872). be in a state of flux, and the correct adoption Darwin C. 1877. The various contrivances by of the ‘exaptive’ terminology, wherever present, which orchids are fertilized by insects, 2nd ed. offers an important conceptual and operational John Murray, London. clarification. It is thus recommendable to main- Darwin C. & Dohrn A. 1982. Charles Darwin tain an effort for the diffusion and the correct Anton Dohrn correspondence. Macchiaroli, interpretation of this possible “extended taxon- Napoli, ed. by C. Groeben. omy of fitness”. Dennett D.C. 1995. Darwin’s dangerous idea: Evolution and the meanings of life. Simon & Schuster, New York. Acknowledgements Gould S.J. 1980. The panda’s thumb. W. W. Norton, New York. This paper is part of the Italian National Research Gould S.J. 1997. The exaptive excellence of span- Project named “The Adaptive Behaviour of Biologi- drels as a term and prototype. Proc. Natl. Acad. cal Systems and the Scientific Method” co-funded by Sci. U.S.A., 94: 10750-10755. the Italian Ministry of Education, University and Gould S.J. 2002. The structure of evolutionary Research (MIUR) and – for what concerns our local theory. Belknap-Harvard, Cambridge, Mass.. research unit – by the University of Milano Bicocca. Gould S.J. & Lewontin R.C. 1979. The spandrels The complementary material referred to herein can of San Marco and the Panglossian paradigm: a be found at the URL http://boa.unimib.it/han- critique of the adaptationist programme. Proc. dle/10281/19392. Direct download is also available: R. Soc. Lond. B Biol. Sci., 205: 581–98. T.Pievani & E. Serrelli 23

Gould S.J. & Vrba E.S. 1982. Exaptation – a missing Pievani T. (in press). Born to cooperate? Altruism term in the science of form. Paleobiology, 8: 4-15. as exaptation, and the evolution of human soci- Haile-Selassie Y., Suwa G. & While T.D. 2004. ality. In R.W. Sussman & C.R. Cloninger (eds): Late Miocene teeth from Middle Awash, Origins of Cooperation and Altruism. Springer, Ethiopia, and early hominid dental evolution. New York. Science, 303: 1478-1480. Pinker S. 1994. The language instinct. Penguin, Hauser M.D., Chomsky N. & Fitch W.T. 2002. London. The faculty of language: what is it, who has it, Ridley M. 2004. Evolution. Blackwell Science, and how did it evolve? Science, 298: 1569-1579. London. Jacob F. 1977. Evolution and tinkering. Science, Shimizu D. & Macho G.A. 2007. Functional 196: 1161-1166. significance of the microstructural detail of the Kay R.F. 1975. The functional adaptations of pri- primate dentino-enamel junction: A possible ex- mate molar teeth. Nat. Mater., 3: 229-232. ample of exaptation. J. Hum. Evol., 52: 103-111. Kivell T.L. & Begun D.R. 2007. Frequency and Tattersall I. 2004. What happened in the origin timing of scaphoid-centrale fusion in homi- of human consciousness? Anat. Rec. B, 276B: noids. J. Hum. Evol., 52: 321-340. 19–26. Manzi G. 2007. L’evoluzione umana. Il Mulino, Vrba E.S. & Gould S.J. 1986. The hierarchical Bologna. expansion of sorting and selection: Sorting and Pievani T. 2003. Rhapsodic evolution: Essay on exap- selection cannot be equated. Paleobiology, 12: tation and evolutionary pluralism. World Futures. 217-228. The Journal of General Evolution, 59: 63-81. Wood B. 2005. Human evolution: a very short in- Pievani, T. 2009. The World after Charles R. troduction. Oxford University Press, New York. Darwin: Continuity, Unity in Diversity, Contingency. Rend. Lincei-Sci. Fis., 20: 355-361. Editor, Giovanni Destro-Bisol