What is the nature and justification of an adaptationist programme in evolutionary biology?

Francis Smallwood

I am fully convinced that species are not immutable; but that those belonging to what are called the same genera are lineal descendants of some other and generally extinct species, in the same manner as the acknowledged varieties of any one species are the descendants of that species. Furthermore, I am convinced that Natural Selection has been the main but not exclusive means of modification. (Darwin 1859, p.6) We see these beautiful co-adaptations most plainly in the woodpecker and missletoe; and only a little less plainly in the humblest parasite which clings to the hairs of a quadruped or feathers of a bird; in the structure of the beetle which dives through the water; in the plumed seed which is wafted by the gentlest breeze; in short, we see beautiful adaptations everywhere and in every part of the organic world. (ibid., p.60-61) ...unless profitable variations do occur, natural selection can do nothing. (ibid., p.82) ... there are many unknown laws of correlation of growth, which, when one part of the organisation is modified through variation, and the modifications are accumulated by natural selection for the good of the being, will cause other modifications, often of the most unexpected nature. (ibid., p.85-86) Natural selection will not necessarily produce absolute perfection; nor, as far as we can judge by our limited faculties, can absolute perfection be everywhere found. (ibid., p.206) Adaptationist reasoning is not optional; it is the heart and soul of evolutionary biology. Although it may be supplemented, and its flaws repaired, to think of displacing it from central position in biology is to imagine not just the downfall of Darwinism but the collapse of modern biochemistry and all the life sciences and medicine. (Dennett 1995, p.238) The ground ruleor perhaps doctrine would be a better termis that adaptation is a special and onerous concept that should be used only where it is necessary. (Williams 1966, p.4) The most important function of this book is to echo a plea made many years ago by E. S. Russell (1945) that biologists must develop an effective set of principles for dealing with the general phenomenon of biological adaptation. (ibid., p.19)

Abstract
In this essay I hope to elaborate on the nature of the adaptationist programme in evolutionary biology and to consider its justification. Adaptationism is not a single, unified thesis, but comprises a range of views about both the evolutionary process and the aims of evolutionary biology. The adaptationist programme, as I understand it most generally, is a research programme adopted by many evolutionary biologists, according to which biological systems are investigated as if they were objects designed by natural selection as solutions to environmental problems. The adaptationist programme has been tremendously successful, yielding many truly remarkable discoveries, although it has evidently been irresponsibly implemented by some researchers, giving those more sceptical of the approach cause to air vocal concern. Whilst the adaptationist, in pursuing the programme, must proceed with caution, aware of its pitfalls and the limitations of its various methodologies, there is absolutely no reason to believe that the adaptationist programme should be relinquished to do so would be inconceivable. What I do not think is sufficiently appreciated, or at least sufficiently acknowledged, by the programmes practitioners is the number of assumptions upon which the programme relies, particularly about the availability of variation which requires commitment to various claims about development and evolvability, and the number of requisite conditions which must be met if selection is to be capable of generating adaptation. The results of direct research into development would, as they are doing, provide a means of substantiating these crucial assumptions and justifying the pursuit of the programme. Darwin discovered natural selection and developed his theory of evolution within the tradition of British natural theology. Attempts to justify the pursuit of the adaptationist programme are often made on philosophical or ideological grounds. The adaptationist must realise that the programme can only be justified on scientific grounds, by demonstrating the ability of the programme to generate explanations of the processes which have given rise to the organic world. There must, I think, be a certain amount of personal preference involved in scientific research. It does not seem that there is any means of clearly demonstrating the explanatory pre-eminence of some class of facts over others, and I doubt that there is one single aim of evolutionary biology, other than the general aim to understand the processes which gave rise to the living world, so there is important work in a wide variety of fields to be undertaken, necessitating the enlistment of research programmes which will be capable of generating hypotheses as required. Nevertheless, and as Darwin believed, adaptation is of such pervasive importance in evolution that its investigation is one of unquestionable importance in evolutionary biology. The adaptationist programme offers a successful means of doing so and the evolutionary biologist seems fully justified in its pursuit.

Contents

1. Adaptation and its discontents 1.1 What is adaptation? 1.2 What is adaptationism? 1.2.1 Optimality 1.2.2 Good design 1.2.3 Evolving evolvability 2. The spandrels of San Marco 2.1 Constraints on perfection 2.2 Robust process explanations 2.3 Misinterpreting Spandrels 3. Natural theology continued... 4. Adaptationist reasoning 4.1 The Panglossian paradigm 4.2 The artefact model 4.3 Storytelling and hypothesising 5. Conclusion

1 1 2 3 4 6 7 7 11 13 14 15 16 17 18 19

Appendix A: The adaptive landscape and the importance of perspective Appendix B: Selection and drift Appendix C: Darwin and adaptation Appendix D: Gould and Conway Morris Bibliography Notes on figures Glossary

1.
1.1

Adaptation and its discontents

What is adaptation?

Adaptation is perhaps defined most basically as the fit between an organism and its environment.1 The term refers to a phenotypic feature of an organism which promotes survival and reproduction, a capacity referred to as reproductive success or fitness. 2 Adaptations, such as wings, hearts and eyes, contribute to fitness because of their effects or functions.3 Adaptation may also refer to the process whereby organisms within a population become adapted, a famous instance being industrial melanism in the peppered moth (Fig. 1, overleaf). 4 Given heritable variation within a population, those organisms better adapted to their environmental conditions will have a higher fitness, and so will tend to produce more offspring than those organisms less well adapted, bequeathing their genes (and the adaptive characteristics they programme) to the next generation. 5 The differential survival and propagation of genes is natural selection. Whilst selection is necessary for adaptive evolution, promoting adaptation as a matter of definition,6 it is not sufficient.7 It is also important to realise that adaptation is relative; how well adapted an organism is depends only on how well adapted the other organisms within the population are. 8 The adaptation of organisms to their environment is often conceived as a problem-solving phenomenon: organisms adapt to occupy a vacant niche in their ecology. Lewontin has
1

For a brief and general introduction to adaptation, see Travis and Reznick 2009. What I particularly like about this essay is the wide range of examples discussed therein which imparts something of the sheer brilliance and prevalence of adaptation. 2 See Mills and Beatty 2006 for a discussion of this propensity interpretation of fitness. 3 Function is a notoriously thorny issue in philosophy and the philosophy of biology. For an excellent discussion of biological function, see Lewens 2004, chap.5. Lewens proposes an understanding of function along the lines of what I have alluded to. 4 See Kettlewell 1956. 5 It is worth reading Darwins (1859, p.61) lucid enunciation of the principle of natural selection: Owing to this struggle for life, any variation, however slight and from whatever cause proceeding, if it be in any degree profitable to an individual of any species, in its infinitely complex relations to other organic beings and to external nature, will tend to the preservation of that individual, and will generally be inherited by its offspring. The offspring, also, will thus have a better chance of surviving, for, of the many individuals of any species which are periodically born, but a small number can survive. I have called this principle, by which each slight variation, if useful, is preserved, by the term of Natural Selection, in order to mark its relation to man's power of selection. We have seen that man by selection can certainly produce great results, and can adapt organic beings to his own uses, through the accumulation of slight but useful variations, given to him by the hand of Nature. But Natural Selection, as we shall hereafter see, is a power incessantly ready for action, and is as immeasurably superior to man's feeble efforts, as the works of Nature are to those of Art. 6 Williams 1966, p.4. 7 Lewontin 1978, p.222-225. 8 This was one of Darwins crucial insights, one which he had well over a decade after he had discovered the principle of natural selection. Throughout the 1830s and 1840s Darwin had believed adaptation to be perfect, albeit in a somewhat limited sense (see Ospovat 1981). However, by the time he came to write the Origin Darwin had realised that adaptation is, in fact, relative; there is no absolute standard of perfection: Natural selection tends only to make each organic being as perfect as, or slightly more perfect than, the other inhabitants of the same country with which it has to struggle for existence. And we see that this is the degree of perfection attained under nature. The endemic productions of New Zealand, for instance, are perfect one compared with another; but they are now rapidly yielding before the advancing legions of plants and animals introduced from Europe. Natural selection will not produce absolute perfection, nor do we always meet, as far as we can judge, with this high standard under nature (Darwin 1859, p.201-202).

criticised such a lock-and-key conception of adaptive evolution, arguing that organisms do not experience environments passively but rather create and define the environment in which they live.9 Lewontin claims that if niches are not pre-existent within the ecology, evolution cannot be described as a process of adaptation because all organisms are already adapted.10 However, whilst there is certainly a complex interplay between organisms and their environments, it would be a mistake to thereby declare adaptation conceptually defunct, as long as organisms are not capable of shaping all aspects of their environment.11 Lewens notes that just so long as the relationship between a lineages response to problems and the consequent modification of those problems is not too chaotic12 the problem-solving conception of adaptation is legitimate.

Figure 1 The white-bodied peppered moth (morpha typical) (left) and the black-bodied peppered moth (morpha carbonaria) (right) resting on a lichened tree trunk in Deanend Wood, Dorset. In industrial areas, where pollutants blackened the trunks of trees, the black-bodied carbonaria was camouflaged from predators and so was at a selective advantage due to its melanism

1.2

What is adaptationism?

Adaptationism, as Sterelny remarks, is not a single doctrine, but a cluster of loosely related views13; views about both the evolutionary process and its investigation. Godfrey-Smith has distinguished three strands of adaptationism: empirical, explanatory and methodological. 14

Lewontin 1978, p.215. Ibid. 11 Adaptation itself is a phenomenon which significantly affects the environment, as adaptation in one (intra- or interspecific) instance may frustrate adaptation in another instance. One possible result of this is the eventuation of an arms race (see Dawkins and Krebs 1979). 12 Lewens 2004, p.82. 13 Sterelny 2001, p.16.
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Empirical adaptationism holds that selection is a powerful and ubiquitous force which is more significant than other factors in determining an evolutionary trajectory. Explanatory adaptationism holds that adaptation is the central fact of evolution which is explained by selection. Methodological adaptationism recommends treating biological systems as adaptations as a fruitful investigative procedure. Godfrey-Smith states that these strands are logically independent.15 Nevertheless, I believe that all three forms of adaptationism contribute to an elucidation of the nature and justification of an adaptationist programme. The adaptationist programme proffers a method for investigating biological systems which relies upon numerous empirical assumptions, its primacy dependent on the perceived aims of evolutionary biology. Below, I discuss several of the empirical bases of the adaptationist programme. 1.2.1 Optimality According to Orzack and Sober, adaptationism is a view about the relative importance of selection in evolutionary trajectories, which can be tested using optimality models.16 If within a population the fittest, i.e. optimal, 17 phenotype among a range of alternatives goes to fixation, then it can be inferred that selection was the most important force acting on the population. If, however, the phenotype which has gone to fixation is suboptimal, then some other force, such as drift,18 must have been more important than selection. 19 Optimality models consist of (i) a phenotype set (the range of phenotypic variants); (ii) a set of state equations (parameters of the system); (iii) a fitness measure (the means of measuring relative fitness); and (iv) an assumption about heredity.20 The result of an optimality model is
14

Godfrey-Smith 2001. Lewens (2009) distinguishes seven types of adaptationism, dividing Godfrey-Smiths three up further and distinguishing one further type: epistemological adaptationism, embodied in epistemological optimism that investigators have access to data which will allow them to reliably discriminate between competing evolutionary hypotheses (p.163). 15 Although he adds that to acknowledge their logical independence is not to say tha t none of them supports another, but as far as literal implication goes, any combination of yess and nos is possible (GodfreySmith 2001, p.338). Dawkins, for example, unreservedly endorses explanatory adaptationism, whilst rejecting empirical adaptationism (see 3). 16 Orzack and Sober 1994a,b, 1996. 17 I am following Williams (1992, p.61) suggested that optimality modelling is preferable to optimization, and similarly optimized to optimality, for the reason that the adoption of these terms implies a corrective tendency, rather than a state attained. Whilst I think that this is a sensible recommendation which would probably be less misleading, I shall continue, for the most part, to refer to optimality modelling and optimality. 18 Throughout, I refer to drift as a force despite the inaccura cy of such a referral, although I continue to make such a referral for brevity and because it does not really affect my argument whether drift is or is not a force. Godfrey-Smith (2009, p.59-62) argues that drift is not a force, but that it is not just a matter of ignorance of causal factors either. He suggests instead that drift should be thought of as a descriptor of situations where small phenotypic perturbations do not result in commensurably small increases in fitness, and where fitness is strongly determined by factors external to the organism. 19 Because an optimality model describes the phenotype of an individual, not the adaptation of a group (Orzack and Sober 1994, p.370), within- and between-individual variation within a population must be compared with that predicted by the model to determine whether the optimal phenotype has gone to fixation. 20 Maynard Smith 1978.

most strongly determined by the phenotype set specification, as whether a given phenotype is optimal depends on the available variant phenotypes (see Fig. 2). Adaptationism, then, is tested by the accumulation of successes and failures of specific optimality models.21 The advantage of conceiving of adaptationism in this way is that it presents a clear thesis which can be readily tested using quantitative methods.

Figure 2 A representation of an optimality model

Sterelny, however, argues that this is a stronger thesis than any real adaptationist needs to run. 22 Whilst Sober and Orzacks adaptationism would be testable (albeit, admittedly timeconsuming), it makes no stipulations about the goodness of organic design. Sterelny remarks that adaptationists are really more interested in function than in optimality, 23 and that We should distinguish between what selection undisturbed would produce and good design. 24 Adaptationists do not merely affirm the relative importance of selection; many are committed to what Lewens calls good-designism, 25 the view that biological systems are well designed. Furthermore, as Sterelny notes, Natural selection is no explanation of adaptation, if adaptation is by definition whatever selection undisturbed produces.26 Sterelny notes that there are two distinct notions of optimality: the first, used by Orzack and Sober, which defines optimality in terms of selection; the second, which explains optimality in terms of selection, where the optimal organism, in that sense, is the well-designed organism.27 1.2.2 Good design Lewens notes that whilst it may be that natures designs are the best of what is available... if what is available is limited, then design quality may be quite awful. 28 In The blind

21 22

Orzack and Sober 1994a, p.365. Sterelny 2001, p.133. 23 Ibid., p.132. 24 Ibid., p.133. 25 Lewens 2009. 26 Sterelny 2001, p.133 (my emphasis). 27 Sterelny 2001, p.134. 28 Lewnes 2009, p.164.

watchmaker,29 Dawkins spends the first chapter marvelling at the complexity of the bats echolocation system, elsewhere describing himself as a neo-Paleyist.30 This strand of adaptationism contains assumptions not just about the relative importance of selection, but also about the range of variation. Consequently, Lewens remarks that the proponent of gooddesignism will tend to find herself committed to various substantive claims about the nature of developmental processes. 31 There is nothing inherent to the selection mechanism which assures good designselection sees only fitness. 32 The adaptationist programme seems to be more involved and less free-standing than it may be at first made to appear. A further strand of empirical adaptationism which Lewens unravels is that of gradualism. 33 Gradualism is closely associated with good-designism. Lewens writes that
What is distinctive in Darwins explanation of the facts of apparent design is not simply the idea that fitter variants will replace the less fit ones in a population. It is the idea that through the accumulation of many small, favourable mutations, the emergence of complex adaptations becomes far more likely than it would be through single saltation. 34

Dawkins lays great emphasis on the statistical improbability of adaptations; it is impossibly improbable that a complex adaptation such as the camera eye should arise by macromutation.35 Gradual, cumulative selection of slight variations can offer the only adequate explanation of complex adaptations by dividing hugely improbable events into many more probable events occurring over many generations. 36 Dawkins refers to the gradualness of evolution as a matter of principle rather than fact :37 the improbability of adaptation poses a riddle and saltation is just a restatement of the riddle. 38 Whilst adaptationists do not deny that macro-mutations may occurMaynard Smith admitted that he always had a soft spot for hopeful monsters39gradualism is intrinsic to the unique explanatory function of selection in explaining adaptation. 40 However, what Lewontin calls continuity must obtain in order for gradual, cumulative selection to occur.41
29 30

Dawkins 1986. Dawkins 1983, p.404. 31 Lewens 2009, p.165. 32 Orr 1996, p.469. 33 Lewens 2009, p.167-168. 34 Ibid., p.167. 35 Nilsson and Pelger (1994) present a model for the gradual evolution of a camera eye from a patch of photocells. 36 This is one of the central themes of Dawkins 1996. 37 Dawkins 1995, p.83. 38 Ibid., p.84. 39 Maynard Smith 1981. 40 Darwin keenly emphasised the gradual, cumulative nature of selection. Due to the intense struggle for existence, those random variations which confer even a slight adaptive advantage to an organism will be preserved by selection, wondrously complex organs forming over many generations by slight increments. Although in many cases it is most difficult to conjecture by what transitions an organ could have arrived at its present state; yet, considering that the proportion of living and known forms to the extinct and unknown is very small, I have been astonished how rarely an organ can be named, towards which no transitional grade is known to lead. The truth of this remark is indeed shown by that old canon in natural history of Natura non facit saltum.... Why, on the theory of Creation, should this be so? Why should all the parts and organs of many independent beings, each supposed to have been separately created for its proper place in nature, be so invariably linked together by graduated steps? Why should not Nature have taken a leap from structure to

1.2.3 Evolving evolvability The preceding discussion of adaptationism has attempted to elaborate on the empirical bases of the adaptationist programme. Proponents of the programme believe selection to be powerful and ubiquitous, capable of creating remarkably complex adaptive designs which would otherwise be hugely improbable were it not for the gradualness of evolutionary trajectories. Such a conception of adaptationism contains numerous ancillary assumptions, particularly about the availability of variation. Lewens writes that although selective forces explain adaptation, they do not do so alone. The right kind of developmental organization is also needed if systems are to be apt for cumulative evolution. 42 Wagner and Altenberg argue that the study of the origin of variation is fundamental to evolutionary biology; an understanding of how the genotype maps onto the phenotype. They note the distinction between variation and variability: variation being the property of a class; variability being the propensity of a class to vary. They write that variational properties of the phenotype are a level of phenomenon distinct from phenotypic adaptation, 43 as they are necessary for adaptation. The range of variation within a population is determined by the variability of the population, and because variability is under genetic control it may thus evolve. 44 Evolvability, the genomes ability to produce adaptive variants when acted upon by the genetic system,45 is a prerequisite for adaptive evolution. In order to carry out an effective search of the adaptive landscape, a population must be sufficiently variable. A major feature of the genotype-phenotype map is modularity. Intefering with the expression of the gene eyeless in Drosophila resulted in complete ectopic eyes sprouting on wings, legs and antennae, showing the gene to be a master control of eye development.46 Such organisation of the developmental system into semiautonomous units Wagner and Altenberg describe as a phenomenon distinct from adaptation itself, 47 as it is a prerequisite to adaptation. Dawkins refers to innovations in developmental systems, such as the emergence of segmentation, as evolutionary Figure 3 Scanning electron micrograph of ectopic watersheds which open the floodgates to future 48 evolution. Evolutionary watersheds, whilst they eyes sprouted underneath a wing (arrow) and on
an antennae (arrowhead) of a fruit fly structure? On the theory of natural selection, we can clearly understand why she should not; for natural selection can act only by taking advantage of slight successive variations; she can never take a leap, but must advance by the shortest and slowest steps (Darwin 1859, p.194). 41 Lewontin 1978, p.230 42 Lewens 2004, p.37. 43 Wagner and Altenberg (1996, p.968). 44 Ibid., p.969. 45 Ibid., p.970. 46 See Halder, Callaerts and Gehring 1995. 47 Ibid. 48 Dawkins 1988, p.218.

may differ in magnitude, are evolutionarily pregnant, 49 enabling forays into previously uncharted biological spaces. The role of selective explanations in the evolution of evolvability may at first appear unproblematic, as lineages which were more variable would be more successful than those lineages less variable, as they would be capable of performing a more comprehensive search of biological space. However, Lewens considers the inability of selection to shape developmental systems which are not themselves apt for cumulative evolution, securing the prospective role of non-selective explanations in the origins of such systems.50 Nevertheless, however developmental systems originate, one can conceive a cumulative selection process resulting in the evolution of evolvable lineages. The evolution of evolvability, whilst unlike the evolution of adaptations, could be similarly cumulative as more evolvable lineages will adaptively radiate in directions inaccessible to less evolvable lineages, allowing daughter lineages to radiate even further. Dawkins writes that After a given innovation in embryology has become selected for its evolutionary pregnancy, it provides a climate for new innovations in embryology. 51 The adaptive potential of evolvable lineages is greater than that of less evolvable lineages. I have attempted to show that the adaptationist programme contains assumptions about the range of variation, which involves making substantive claims about development, which developmental research would offer a means of substantiating. Below, I consider various attacks upon these ancillary assumptions which are integral to the justification of the pursuit of the adaptationist programme.

2.
2.1

The spandrels of San Marco

Constraints on perfection

In their widely read and oft-cited paper The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme, 52 Gould and Lewontin chastised adaptationists for espousing an unsound research programme which they claimed was based on faith in the power of natural selection as an optimizing agent,53 according to which organisms were atomised into unitary traits and spurious adaptive explanations were proposed to account for each trait individually.54 Gould and Lewontin proposed an alternative programme55 which seeks to uncover the Bauplne (body plans) of organisms. They wrote that Bauplne are so integrated and so replete with constraints upon adaptation that conventional styles of selective arguments can explain little of interest about them,56 averring that constraints restrict possible paths and modes of change so strongly that the
49 50

Ibid. Lewens 2004, p.36. 51 Dawkins 1988, p.219. 52 Gould and Lewontin 1979. 53 Ibid., p.581. 54 Ibid. Despite the ability to investigate certain traits individually, such as beak type (see Grant 1986), biologists have long appreciated that organisms cannot be treated simply as a summation of individual traits. Dobzhansky (1956, p.340) emphasised that it cannot be stressed too often that natural selection does not operate with separate traits. 55 Gould (1980a) has referred to this alternative programme as structural integration. 56 Gould and Lewontin 1979, p.594.

constraints themselves become much the most interesting aspect of evolution. 57 They discussed two main classes of constraints, phyletic and developmental, of which they claimed that developmental constraints may hold the most powerful rein of all over possible evolutionary pathways.58 Maynard Smith et al. define developmental constraint as a bias on the production of variant phenotypes or a limitation on phenotypic variability caused by the structure, character, composition, or dynamics of the developmental system. 59 Gould and Lewontin illustrated their view with an architectural example: the pendentives of St. Marks Basilica (Fig. 3). Pendentives are the triangular spaces between adjacent rounded arches supporting a dome. The pendentives in the Basilica are lavishly decorated and they seem to be specially designed as decorative spaces. Gould and Lewontin argued, however, that pendentives (what they mistakenly referred to as spandrels) arise purely incidentally as an unintended by-product: the design represents an adaptation, but the architectural constraint is clearly primary.60 Assuming that the pendentives were intentionally designed, i.e., adaptive, is to make the same mistake that the adaptationist makes when, confronted with a novel feature, he assumes the feature must have an adaptive explanation, when actually the feature has not arisen for any adaptive utility but merely as an incidental architectural byproduct. Their metaphor is dubious, however. 61

Figure 4 One of the beautifully decorated pendentives in St. Mark's Basilica

Gould and Lewontins criticism of the adaptationist programme rests upon a belief about the tight integration of developmental systems:
If development occurs in integrated packages, and cannot be pulled apart piece by piece in evolution, then the adaptationist programme cannot explain the alteration of developmental programmes underlying nearly all changes of Bauplan.62

Maynard Smith et al. note that a significantly high degree of quasi-independence is prerequisite to the evolution of complex adaptation; it must be possible to change single

57 58

Ibid., p.594. Ibid. 59 Maynard Smith et al. 1985, p.266. 60 Ibid., p.583. 61 Daniel Dennett (1995, p.274) argues, conversely, that the pendentives are, in fact, adaptations, chosen from a set of equipossible alternatives in order to provide suitable surfaces for the display of Christia n iconography. Conway Morris (1998, p.11) has aired a similar view. Whilst there are problems with such an interpretation (see Mark 1996), pendentives are not as non-adaptive as one might think, and, as Dennett (1995, p.275) notes, whatever a spandrel is, it is supposed to be a non-adaptation. 62 Gould and Lewontin 1979.

traits without disturbing others in a way that reduces overall fitness. 63 Pleiotropy is a prevalent phenomenon which lowers quasi-indepdence. They discuss five sources of developmental constraints,64 which Reeve and Sherman reduce to two: (a) selection against disruptive developmental processes; and (b) lack of genetic variation.65 As Reeve and Sherman note, (a) cannot be used to dethrone the adaptationist approach, 66 as developmental constraints so derived are themselves the result of selection. However, they concede that (b) may be conceived as an alternative explanation of trait persistence to selection.67 Dawkins admits that we need to pay more attention to the problem of the limitations of available genetic variation. 68 Reeve and Sherman note that developmental constraints must be shown to oppose or bias selection in order fo r developmental constraint explanations to compete with selective explanations; they cannot be a mere descriptor of developmental processes that are conserved through evolutionary time. 69 The adaptationist does not deny the existence of constraints,70 although they may not readily assume their significance. Maynard Smith et al. discuss shell coiling to illustrate how one might determine whether selective or developmental constraint explanations offer more appropriate answers to a question of phenotype existence.71 In Figs. 5 and 6, whorls to the left of the curved line overlap and whorls to the right do not. Since both forms are possibly existent (Fig. 6), the distribution of forms appears to be best explained by selection, the reason being that open whorls are structurally weaker than involute whorls. Maynard Smith et al. then go on to consider boring pholads which have shells which can be considered optimal only if one accepts the idea that the animal is constrained to maintain the basic logarithmic spiral.72 One can see, then, that selective and developmental constraint explanations are not mutually exclusive; both may be required to provide an accurate account of phenotype existence.

63 64

Maynard Smith et al. 1985, p.266. Ibid., p.270-271. 65 Reeve and Sherman 1993, p.21. 66 Ibid. 67 Ibid., p.22. 68 Dawkins 1982, p.43. Furthermore, given the nature of a lineages traversal of the adaptive landscape, Once a lineage has begun to evolve in a given direction, this may in itself close options that were formerly available, sealing off access to a global optimum, such that lack of available variation does not have to be absolut e in order to become a significant constraint on perfection (ibid., p.45). 69 Reeve and Sherman 1993, p.21. 70 Dawkins writes that, Only a minority of the things that conceivably could evolve are actually permitted by the status quo of existing developmental processes (p.311), and that, The variation that is available for selection is constrained by the processes of embryology, as they actually exist (p.312). Dennett (1994, p.223) considers an analogy with sonnet-writing. Whilst the structure of the sonnet format exerts a significant constraint on the creativity of the poet, this does not mean that something beautiful cannot be produced: Saying something meaningfullet alone beautifulwithin the rigid constraints of the sonnet form is a frustrating exercise. No sooner do you tentatively fix one line than you have to revise many of the other lines, and that forces you to abandon some hard-won excellences, and so forth, round and round in circles, searching for an overall good fitor, we might say, searchin g for overall good fitness. Constraints are real, but that does not entail that there can be no good design. 71 Maynard Smith et al. 1985, p.278-281. 72 Ibid., p.280.

Figure 5 Sketches of ideal shells. The W = 1/D line delineates overlapping whorls from non-overlapping whorls

Figure 6 The occurrence of about 400 extinct ammonoid genera contoured in the same format as in Fig. 5. Again, the W = 1/D line delineates overlapping whorls from nonoverlapping whorls

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2.2

Forms of explanation

Gould and Lewontins discussion suggests that developmental constraint explanations are in direct competition with adaptive explanations. However, Sterelny has argued that notions of explanatory combat are redundant. Drawing on a discussion by Jackson and Pettit,73 Sterelny distinguishes what he calls actual-sequence explanations and robust process explanations, both of which perform different modal functions. 74 Actual-sequence explanations involve detailed information about the particulars of the actual world, considering differences between the actual world and possible worlds, whereas robust process explanations consider similarities between the actual world and possible worlds. The two forms of explanation are not mutually exclusive:
We could know the precise sequence of the development of some aspect of an organisms phenotype without knowing something very important: whether that sequence is canalised, or in some other way buffered so that different paths give functionally equivalent outcomes.75

Actual-sequence explanations provide contrastive information, in great detail, about the causal history of whatever phenomenon is being investigated, whilst robust process explanations provide comparative information, in less detail, about causal histories. Jackson and Pettit favour explanatory ecumenism, as preference for one form of explanation over another depends on what ones perspective or purpose is. 76 An actual-sequence explanation of the evolution of a trait will involve selection, drift, phylogeny, etc. The adaptationist does not object to such a form of explanation. In proposing an adaptive hypothesis the adaptationist is making a claim about the robustness of evolutionary trajectories:77 an adaptive explanation of a trait, from a coarse grain of analysis, does not disallow that nonselective forces influenced an evolutionary trajectory, but, rather, claims that selection exerted a significant influence on the evolutionary trajectory, such that in other worlds where similar selective forces obtained, whilst other parameters were varied, one could expect similar (adaptive) outcomes. Sterelny writes,
73 74

Jackson and Pettit 1992. Sterelny 1996. 75 Ibid., p.131. 76 Jackson and Pettit 1992, p.16. 77 Dennett (1983, p.387) writes that If one looks closely enough at evolution, one sees plenty of important perturbations and exceptions to adaptation; lots of noise, some of which gets amplified by procreation. So evolution is not always adaptive. Q.E.D. But if we step back a bit, we can say, without denying what has just been granted, that evolution is always a noisy adaptive process, always adaptive in the long run. Is one an adaptationist if one chooses to look at the whole process that way? If so, is it a mistake? Perhaps Lewontin would say that it is always a mistake to look less closely at evolutionary processes than one can, but that is an implausible methodological canon. It is often useful to abstract - to say (rigorous, falsifiable) things about the forest and let someone else worry about the trees. Both actual-sequence and robust process explanations are necessary to understand an evolutionary trajectory. It is simply a mistake to imagine that one form of explanation is sufficient or preclusive of the other. Whether an investigator should favour one form of explanation over the other depends on their aims, which may not be the aims of another investigator. It seems that much of the controversy over the pursuit of an adaptationist programme is due to a difference in researchers aims, and consequently their explanatory preferences, where aims and explanatory preferences are either construed as mutually exclusive or are conflated. An adaptationist hypothesis about an evolutionary trajectory will contain a (robust process) claim about the causal importance of selection in determining the trajectorys outcome, but may make no mention of the other non -selective factors which contributed to the form of the evolutionary trajectory.

11

Suppose that we vary phylogeny, population size, genetic variation, sampling noise but not selective regime. Then the adaptationist believes that all those possible trajectories will share an important property. They will not be the same, even to the first approximation. But they will have something important in common. 78

Gould and Lewontin seem to construe adaptive hypotheses as actual-sequence explanations, rather than robust process explanations. In claiming selective forces to have been important in the evolution of a trait, the adaptationist is not suggesting that there were no operative constraints which significantly influenced the evolutionary trajectory or that non-selective forces, such as drift, were unimportant;79 rather, they are making a claim about the robustness of the evolutionary trajectory, arguing that selective forces were responsible for shaping the functional properties of the trait. Construed as robust process explanations, adaptationist explanations do not preclude historical explanations. 2.3 Misinterpreting Spandrels

Gould and Lewontins paper has received a great deal of attention,80 although Dennett has remarked that it has been widely misinterpreted.81 The paper has assumed a mantle as the definitive critique of adaptationism. Dennett recalled a critic telling him that Gould and Lewontin had shown adaptationism to be completely bankrupt.82 Queller has called the paper an opinion piece, a polemic, a manifesto, and a rhetorical masterpiece. 83 This characterisation acknowledges the papers unusual style.84 As Dennett emphasises, Gould and Lewontins critique is a call for pluralism raised against a surfeit of spurious adapti ve hypothesising. Far from rejecting the adaptationist programme, their grievance is with the undue neglect of alternative research methods. Dennett blames the mismatch between the rhetoric... and the mildness of their conclusions and recommendations 85 for the misinterpretation of their paper as a renunciation of adaptationism. Whilst Gould seemed to style himself as a revolutionary, challenging the orthodoxies of evolutionary theory,86 of
78 79

Sterelny 1996, p.139. See Appendix B: Selection and drift. 80 Indeed, the publication of a collection of essays entitled Understanding scientific prose (Selzer 1993) is testament to the prominence of the paper. Gould (1993, p.330) noted that it was the most widely cited of his published articles. 81 Dennett (1983, p.351). 82 Ibid. Dennett (1995, p.239-240) later revealed the critic to be philosopher Jerry Fodor, who, with cognitive psychologist Massimo Piattelli-Palmarini, has recently authored a critique of evolutionary theory entitled What Darwin got wrong (Fodor and Piattelli-Palmarini 2010). 83 Dennett 1983, p.351. 84 Gould (1993, p.321) agreed that the paper was somewhat unsual. He wrote that the paper was neither a data paper nor a review article, but insisted that there exists a third genre: the opinion piece, with its inevitable personality and point of view. He remarked, however, that because evolutionary biology must struggle with deep questions of an essentially philosophical nature... opinion pieces have a long history in the evolutionary literature. Indeed, he believed that the success of Spandrels arises not so much from its pure science, or even from the logic of its argument, but most of all from its rhetoric (in the honourable, not pejorative, sense) and its humanistic imagery (p.333). 85 Dennett 1983, p.351. 86 See, for example, Gould 1980b. Despite frequent avowals of the inadequacies of evolutionary theory and forewarnings of its imminent overthrow, Goulds actual views, which were often obscured by effuse rhetoric, failed to deliver such a fatal blow, as his critics were wont to point out. Conway Morris, whose work on the reassessment of the Burgess Shale fossils was praised by Gould in his interpretation of the fossil bed in his book

12

which adaptationism became a central target, he admitted that he did not deny either the existence and central importance of adaptation, or the production of adaptation by natural selection.87 Lewontin responded to Dennetts claims about the misinterpretation of his and Goulds paper, chastening Dennett for confusing adaptation with adaptationism, stating that he and Gould scorn the former, not the latter.88 He added that, We abuse a world view that raises a phenomenon to untested universality, not the phenomenon itself, which is of undoubted importance in evolution.89 However, this qualification appears to be another rhetorical ploy as the majority of adaptationists would not regard the adaptationist programme as some extension of a world view but as a fruitful means of generating hypotheses about one of the central facts of evolution. Gould and Lewontins characterisation of the adaptationist programme is a patent caricature, so it seems that whatever Gould and Lewontin were renouncing need not be sorely missed. In this vein, whilst Spandrels advocated pluralism, as did Darwin himself, 90 Gould and Lewontins florid rhetoric has been misinterpreted as a renunciation of the adaptationist programme, rather than a caution against its improper use. Consequently, Maynard Smith wrote that their paper has had little impact on practitioners, perhaps because they were seen as hostile to the whole enterprise, and not merely to careless practise of it.91 Many critics regard their attack as levelled at a straw man. Mayr reproved their failure to distinguish the failings of the adaptationist programme and the failings of its practitioners. 92 Sometimes it is possible to investigate individual traits, such as beak type, 93 however this does not require that one regard organisms merely as summations of traits. The adaptationist programme sails an admittedly perilous course between pseudoexplanatory reductionist atomism and stultifying nonexplanatory holism.94 Gould and Lewontins approach seems to have been in danger of tending towards the latter. However, Lewens has argued that the question posed by Gould and Lewontin of What is a trait? is one of central importance to evolutionary bio logy, which points towards a genuinely non-adaptationist methodology implicit in much evolutionary developmental biology.95 Lewens writes that if our idea is to understand what kinds of variants are likely to

Wonderful life (1989) which he presented as evidence for his thesis about the contingency of the evolutionary processa conclusion which Conway Morris, in turn, forcefully challenged wrote, Again and again Gould has been seen to charge into battle, sometimes hardly visible in the struggling mass. Strangely immune to seemingly lethal lunges he finally re-emerges. Eventually the dust and confusion die down. Gould announces to awestruck onlookers that our present understanding of evolutionary processes is dangerously deficient and the theory is perhaps in its death throes. We look beyond the exponent of doom, and there standing in the sunlight is the edifice of evolutionary theory, little changed (1998, p.10). 87 Gould 1997. 88 Lewontin 1983, p.368. 89 Ibid (my emphasis). 90 Gould (1993, p.312) did admit, however, that Darwins theory is basically functionalist, but that he did allow an important scope for pluralism. 91 Maynard Smith 1985, p.121. 92 Mayr 1983, p.325. 93 Grant 1986 is a wonderful study of Darwins finches, which involves an analysis of the influence of selection forces on beak type. 94 Mayr 1983, p.329. 95 Lewens 2009, p.161.

13

arise and why, then direct attention to development, rather than an attempt to provide ecological rationales for the forms we encounter, provides a bona-fide, alternative focus for evolutionary inquiry.96 Lewens admits that there is no radical new mechanism posited for evolution, rather what is proposed is a shift from an externalist to an internalist mode of investigation which would not threaten to displace the adaptationist programme but may speak to the appropriateness of implementing the programme in a given case. 97

3.

Natural theology continued

According to Maynard Smith, The main task of any theory of evolution is to explain adaptive complexity, i.e. to explain the same set of facts which Paley used as evidence of a Creator.98 Dawkins refers to himself as a neo -Paleyist, sharing the archdeacons belief that adaptive complexity demands a very special kind of explanation. 99 Godfrey-Smith takes Dawkins to be a paradigmatic explanatory adaptationist, 100 but one who rejects empirical adaptationism. Dawkins writes that large quantities of evolutionary change may be non-adaptive, but refers to these as the boring parts of evolution. 101 When Dawkins writes that adaptations awake such a powerful hunger that they have traditionally provided one of the main motivations for belief in a supernatural Creator,102 it seems that his justification for explanatory adaptationism is ultimately extra-scientific. Godfrey-Smith argues that the justification for explanatory adaptationism rests upon a fact about our psychology.103 Dawkins, however, does add the qualification that even if most evolutionary change is not adaptive, what is undeniable is that enough of evolutionary change is adaptive to demand some kind of special explanation, adding that It is the part of evolutionary change that is adaptive that Darwin so neatly explained.104 Dawkins recognises that not all evolution is adaptive, although he evidently believes that that small portion which is merits explanatory primacy. Godfrey-Smith criticises explanatory adaptationism for accepting the terms of debate favoured by theological views of the world; it is the tradition of natural theology continued.105 It is important to note that the problem of design and adaptedness is itself a product of a theological view of the world. 106 What was Darwins problem may not now be our problem. 107 Godfrey-Smiths conclusion is that the problem of design is important,

96 97

Lewens 2009, p.181. See 1.2.3. 98 Maynard Smith, quoted in Dawkins 1983, p.404. 99 Dawkins 1983, p.404. 100 Dawkins (2003, p.79) makes this apparent when he writes that, The feature of living matter that most demands explanation is that it is almost unimaginably complicated in directions that convey a powerful illusion of deliberate design. 101 Dawkins 1986, p.303. 102 Dawkins 2003, p.81. 103 Godfrey-Smith 1999, p.188. 104 Dawkins 2003, p.81. 105 Ibid., p.190 (emphasis in original). 106 Ibid. 107 See Appendix C: Darwin and adaptation.

14

despite having been somewhat oversold, and, moreover, that this importance is probably not a kind that gives support to adaptationism as a program of scientific research. 108 I agree with Godfrey-Smith that we should not take our questions from world views that have been abandoned, any more than we should take our answers or methods,109 and that Biologists should set up their work in a way that is responsive to the best current information about which sorts of research will enable us to understand biological phenomena not in a way that complements a philo sophical campaign.110 This must certainly be true. However, this does not entail that explanatory adaptationism has no valid justification. Ruse argues that whilst there are areas apart from adaptation which engage the evolutionary biologist, particularly developmental biology, adaptation lurks in the background of most if not all evolutionary issues,111 taking the amount of variation latent within populations as an example. Whilst there is no clear means of judging the explanatory primacy of certain classes of facts, the pervasiveness of the phenomenon raises adaptation to a level of high priority. As Ruse concludes, We have good scientific reasons for taking adaptation as the fundamental issue.112

4.

Adaptationist reasoning

In this section, I intend to discuss some of the adaptationists methodological practices. Gould and Lewontin refer to the adaptationist programme as the Panglossian paradigm, claiming that it is rooted in the notion that selection is near omnipotent in forging organic design and fashioning the best among possible worlds.113 They claim that the adaptationist proceeds, first, by atomising an organism into (assumedly optimal) traits, and then, second, if it appears that a trait is not optimal invoking tradeoffs between traits, such that suboptimality of a part is explained as its contribution to the best possible design for the whole. 114 4.1 The Panglossian paradigm

Dennett argues, not uncontroversially, 115 that in approaching biological systems the adaptationist avails herself of the intentional stance, an interpretive strategy directed at intentional systems, which Dennett defines as systems whose behaviour can be (at least sometimes) explained and predicted by relying on ascriptions to the system of beliefs and desires (and hopes, fears, intentions, hunches,...).116 Systems are intentional only in relation to the strategies of someone who is trying to explain and predict its behavior. 117 According to Dennett, organisms are artefacts designed by selection in order to propagate our genes. 118
108 109

Ibid., p.191. Ibid., p.190. 110 Ibid. 111 Ruse 2003, p.280. 112 Ibid. 113 Gould and Lewontin 1979, p.584. 114 Ibid., p.585. 115 See Godfrey-Smith 1996. 116 Dennett 1971, p.87. 117 Ibid. 118 Dennett 1990, p.187. See Dawkins 1976 for an articulation of this genes-eye view of evolution.

15

By ascribing aims and desires to nature, the adaptationist may uncover the somewhat covert design rationales of the forms we discover. 119 Dennett argues that, in adopting the intentional stance towards nature, optimality must be assumed not because we think naively that evolution has made this the best of all possible worlds, but because we must be interpreters if we are to make any progress at all, and interpretation requires the invocation of optimality.120 The Panglossian does not assume that this is the best among possible worlds, but, rather, that Mother Nature does the best she can.121 The results of an optimality model may show that, given the constraints operating on an organism, a given design is the best possible in this world. Dennett admits that the Panglossian assumption involves risk, however he argues that it can be wise to take the risk since the payoff is often so high, and the task facing the more cautious and abstemious theorist is so extraordinarily difficult.122 In adopting the intentional stance towards nature, the adaptationist assumes that there is a rationale for the forms we encounter. Gould himself argued that As evolutionists, we seek answers to the question why. 123 Dennett writes that The more complex and meaningful the feature, the less likely it is that there is no sustaining rationale... The complete answer to the evolutionists question will almost always, in at least some minimal way, allude to better design.124 The adaptationist programme, as conceived by Dennett, offers a unique means of answering evolutionists why?-questions. A study of periodical cicadas (Fig. 7, overleaf) presents a wonderful case of why?-questions paying great dividends. For 17 years (13 in some species) nymphs of periodical cicadas remain underground, emerging finally for but a few weeks in which they mate, lay eggs and die. Why should this have evolved? It turns out that the synchronous life cycle, invariant in each brood, is an adaptation for predator satiation: emerging rarely in huge masses ensures that the entire brood cannot be consumed. 13- and 17-year life cycles are longer than the (typically 2-5-year) life cycles of the average predator, and, being prime numbers, cannot be tracked by predators.125 This is a truly sumptuous reason why. 126

119 120

Ibid. Ibid. 121 Dennett 1983, p.352 (his emphasis). 122 Ibid., p.352-353. 123 Gould 1977, p.99. 124 Dennett 1983, p.354. Ghiselin (1983, p.363) has argued that Panglossianism is bad because it asks the wrong question, namely, What is good?... The alternative is to reject such teleology altogether. Instead of asking, What is good? we ask, What has happened? The new question does everything we could expect the old one to do, and a lot more besides. It generates moreand betterhypotheses, and also critical tests. Dennett (1995, p.241) has responded, however, writing that There is hardly a single answer to the question What has happened (in the biosphere)? that doesnt depend crucially on assumptions about what is good, adding that you cant even avail yourself of the concept of a homology without taking on adaptationism, without taking the intentional stance. This bears on the discussion of explanatory pluralism in 2.2. 125 See Lloyd and Dybas 1996a,b. 126 Dennett (1995, p.246) notes the irony that Gould (1977) should endorse such a piece of blatant adaptationist hypothesising, although, to be fair to Gould, his article was written before he embarked upon his perceived campaign against evolutionary orthodoxy; some years later Gould (1991, p.13) wrote that sometimes he wished that all copies of Ever Since Darwin would self-destruct.

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Figure 7 Periodical cicadas

4.2

The artefact model

The artefact model is a popular heuristic which proposes that organisms can be investigated in a similar way to artefacts.127 Williams, for example, wrote, A frequently helpful but not infallible rule is to recognize adaptation in organic systems that show a clear analogy with human implements.128 Dennett has been one of the most prominent and ardent defenders of the artefact model, central to which is the project of reverse-engineering. The reverseengineer seeks to infer the problems faced in the design history of an artefact by performing an engineering analysis of the artefact. According to Dennett, the artefact is treated a s a product of reasoned design development, a series of choices among alternatives, in which the decisions reached were those deemed best by the designers.129 The reverse-engineering project relies heavily on the problem-solving conception of adaptation mentioned in 1.1. Griffiths argues that this adaptationist enterprise founders on the inability of the adaptationist to make functional generalizations130 (what Dennett refers to as forced moves131) which depends upon the robustness of evolutionary trajectories. 132 However, evolutionary convergence, the phenomenon whereby similar adaptive features arise independently in separate lineages, seems to offer ample warrant for making functional generalisations, although Griffiths denies this. 133 Conway Morris has provided a seminal study detailing the ubiquity of convergence, 134 in which he speaks of lineages repeatedly discovering solutions to particular needs.135

127 128

See Lewens 2004 for a perspicacious discussion of the artefact model. Wiilliams 1966, p.10. 129 Dennett 1995, p.230. 130 Griffiths 1996, p.521. 131 Dennett 1995, p.128-135. 132 Griffiths 1996, p.515. See 2.2. 133 Griffiths 1996, p.520-521. 134 Conway Morris 2003. 135 Ibid., p.xii. See Appendix D: Gould and Conway Morris

17

There are two serious misgivings, however, about the reverse-engineering project. The first is that the design process of artefacts is quite unlike the design process of organisms. Selection, as Lewens emphasises, is a population-level, statistical phenomenon. Intentions, on the other hand, can have influences on individual entities. 136 Adopting the intentional stance towards nature gives rise to the misconception that selection cares about building Design, when selection sees only fitness and knows nothing of Design. 137 Secondly, whilst it may be that there is in many cases quite [a] crisp anatomical isolation of functions, some traits may be highly multifunctional. 138 Although the reverse-engineer does not claim that traits exist independently, the artefact model encourages us to ignore developmental relations between traits.139 The artefact model is arguably a fruitful heuristic device, although the adaptationist should be aware of its limitations. Due to an organisms developmental organisation, some traits may not be amenable to any kind of reverse-engineering project that seeks to cast them as designed responses to sustained environmental problems. 140 Whilst many traits, such as eyes, hearts and wings, can be ascribed functions quite unequivocally, many other traits may not receive such clear ascriptions, and it may simply be a mistake to ascribe functions to other traits.141 4.3 Storytelling and hypothesising

Gould and Lewontin accuse adaptationists of telling just so stories. They write that they would not object so strongly to the adaptationist programme if its invocation, in any particular case, could lead in principle to its rejection for want of evidence. 142 Gould and Lewontins misgiving is that adaptationists, in their commitment to their re search programme, 143 may construct hypotheses which are testableas all scientific hypotheses must be144but they shall only construct adaptive hypotheses: the rejection of one adaptive story usually leads to its replacement by another, rather than to a suspicion that a different kind of explanation might be required. 145 Amundson has expressed a similar concern, that
136

Lewens 2004, p.3. Whereas selection, blind and unconscious, can only tinker with systems already available, the designer of artefacts is capable of engineering new systems from scratch (see Jacob 1977). 137 Orr 1996, p.469. 138 Lewens 2004, p.133. 139 Ibid., p.49. 140 Lewens 2004, p.137. 141 Whilst I do not think that Gould and Vrbas (1982) introduction of the term exaptation in distinction to adaptation is particularly helpful, as it seems that all adaptations are exaptations, and vice versa, it seems that the term exaptation could be used to refer to traits which have acquired functions for which there was no selection process. The point here is that application of the artefact model may result in functions being ascribed to traits as the result of a selection process, when in fact the function was not the result of a selection process and the actual function of the trait may not be realised. In this case, the trait would be an exaptation and not an adaptation because the traits function was not the result of a selection process. Failing to distinguish between adaptations and exaptations in this instance of an application of the artefact model would result in an erroneous inference about the traits design history, regarding the trait as a solution to a problem that it was never designed to solve. 142 Ibid., p.587. 143 Amundson (1990, p.578) has referred to adaptationism, as a research programme, as benignly unfaslifiable, as research programs are instruments of research generation. 144 See Popper 2002a,b. 145 Ibid.

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the a priori assumption of adaptation is not testable.146 And, furthermore, Gould and Lewontin argue that the proclivity for adaptive explanations ensures that the criteria for acceptance of a story are so loose that many pass without proper confirmation. 147 Clearly, if the adaptationist programme is to be followed, it must generate testable hypotheses which then must be tested with sufficient rigour. Mayr has noted that adaptationist hypotheses allow a falsification in most cases.148 Dennett recognises the size of the role of sheer, unfettered imagination in adaptationist thinking.149 In pursuing their programme, adaptationists must heed Williams asseveration that adaptation is a special and onerous concept that should only be used where really necessary.150 Accepted standards must be adhered to in order to ensure that Better adaptationist thinking soon drives out its rivals by normal channels...151 Adaptive explanations of traits should be sought because they offer a unique means of understanding the rationale for the forms we encounter, providing valuable answers to our why?-questions, although it may be that there are legitimate questions which remain to be answered.

5.

Conclusion

In conclusion, it is undeniable that the adaptationist programme offers a fruitful approach to the evolutionary biologist. I have attempted to show that the adaptationist programme is not as free-standing as may at first be thought and that the programme relies upon a number of assumptions, particularly about development. There does seem to be some tension between the externalism of the adaptationist programme and the internalism of developmentalist alternative programmes, although I hope to have shown that such a tension is not ineradicable. The adaptationist programme has been terrifically successful, yet it cannot be expected to satisfy all the aims evolutionary biologists may have, in which case alternative programmes must be pursued. As long as adaptationists proceeds with caution, implementing their programme scrupulously, and, especially importantly, do not simply take for granted the background assumptions upon which their programme relies, then it seems that the programme offers a powerful means of investigating one of the central factsand arguably the central factof evolution. Whilst there is much work to be done, I am sure Darwin would have been delighted with the progress that has been made.

146 147

Amundson 1994, p.557. Ibid., p.587-588. 148 Mayr 1983, p.328. 149 Ibid., p.251. 150 Williams 1966, p.4. 151 Dennett 1995, p.249.

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Appendix A
The adaptive landscape and the importance of perspective The adaptive landscape metaphor was introduced by Sewall Wright in the early 1930s. 152 The landscape (Fig. 3) was originally conceived as a genotypic space where altitude represented adaptive value. One can visualise the landscape in two dimensions, although an actual landscape would contain many thousands. Whilst the metaphor has proved controversial, 153 it can serve a useful heuristic purpose.154

Figure 1 Wright's famous two-dimensional illustration of the adaptive landscape of gene combinations. Contours represent adaptiveness; peaks (+) and valleys (-) are also marked.

Following Godfrey-Smith and Wilkins, I employ the landscape metaphor here in a simplistic, two-dimensional form with the horizontal axis containing phenotypes and the vertical axis representing fitness. 155 Godfrey-Smith and Wilkins suggest that selection for most traits is determined by interactions with other organisms it may be useful to think not of organisms moving on a fixed landscape but on something more like a wate rbed.156 Such a

152 153

Wright 1931, 1932. See Ruse 2009. 154 The following discussion draws on material from Godfrey-Smith and Wilkins 2009. 155 For a discussion of the difficulties associated with the adaptive landscape, see Godfrey-Smith and Wilkins 2009, p.201-204. 156 Godfrey-Smith and Wilkins 2009, p.203.

suggestion captures Lewontins criticism of the lock-and-key conception of adaptation;157 adaptation ensures that an organisms environment does not remain static. The reason I have introduced the landscape metaphor is that it is useful in considering some of the problems of adaptationism. Godfrey-Smith and Wilkins emphasise the importance of grain in assessments of the role of selection in evolution. 158 They argue that, depending on the grain at which one observes the evolutionary process, the role of selection shall vary. From a coarse-grained perspective (Fig. 4, overleaf) one is struck by the emptiness of the landscape, dotted here and there by entire populations. From this vantage point, the power of natural selection to produce adaptation appears quite limited.159

Populations

Figure 2 The adaptive landscape as seen from a coarse-grained perspective. Much of the landscape remains unexplored and the ruggedness of the landscape suggests that it will be difficult for a lineage to move from one peak to another

Moving from one extreme to another, seen from a fine-grained perspective (Fig. 5), the landscape appears quite different. From this view, individuals, rather than populations, litter the landscape. As in the coarse-grained perspective, from this view what is often most salient is the set of features of evolution that frustrate adaptation. 160

157 158

Lewontin 1978, p.215 Godfrey-Smith and Wilkins 2009, p.200. 159 Ibid., p.205. 160 Ibid., p.207.

Individuals

Figure 3 One of the peaks viewed from a fine-grained perspective from which individuals are seen to dot the landscape. From this view adaptation appears to be frustrated by factors such as drift

However, from an intermediate grain (Fig. 6, overleaf) the view of the adaptive landscape appears quite different from at the coarse- and fine-grained perspectives. From this intermediate view, whilst the landscape is dotted by populations, these dots are not clearly distinct. It is at this level that many will hold that the salient feature of evolution is local adaptation.161 And the crucial point is that selectionist conclusions drawn at this level of analysis do not contradict non-selectionist conclusions drawn at the higher level. 162

Population

Figure 4 A region of the adaptive landscape containing a single peak as seen from an intermediate grain. From this view there appears to be a single optimal solution which the population has discovered

161 162

Ibid., p.206. Ibid.

One can thus see how it is that the importance of selection, and hence the appropriateness of working under the adaptationist programme, varies with the perspective of the evolutionary process which one adopts. From an intermediate level selection is the most prominent feature of the adaptive landscape, whilst from course- and fine-grained perspectives adaptation appears to be frustrated. Most importantly, the different conceptions of adaptiveness are not mutually exclusive, but are determined solely by the perspective from which one chooses to investigate the evolutionary process.163 Godfrey-Smith and Wilkins note two salient effects of coarsening the grain of analysis (increasing the time-span): (i) selection has opportunity to explore a greater space increasing the possibility of adaptation; and (ii) the area of space to be searched becomes greaterdecreasing the possibility of adaptation.164 The inevitable consequence of coarsening the grain is that the expansion of the search space outpaces the ability of selection and mutation to perform its search. 165 Godfrey-Smith and Wilkins remark that We are then left with a strong sense of the path-dependencies and historical constraints that have shaped the diversity of life.166 For an adaptationist such as Dawkins, trained as an ethologist, it may be that an intermediate grain is most readily appreciable, whilst for an antiadaptationist such as Gould, trained as a palaeontologist, it may be that a coarse grain is most readily appreciable; the differing conceptions of adaptation may be thus explained.

163

It should be noted, however, that adaptive landscapes do not consist of merely several dimensions. The small number of phenotypic dimensions selected by researchers to construct an adaptive landscape is far fewer than the number required for a full description of an organism, and It is likely the case that individual researchers tend to focus on those aspects of the phenotype that are most amenable to the tools with which they are most comfortable (ibid., p.212). 164 Ibid. 165 Ibid. 166 Ibid.

Appendix B
Selection and drift If selection is the only force acting on a population P, then if P occupies a peak A adjacent to a higher peak B (a state of greater adaptedness), in order to ascend B the population would first have to descend into the intervening valley to cross from A to Ba move debarred by selection, as those individuals who began to descend into the valley would be less fit than those who remained on A. This suggests that under selection alone adaptation is severely limited and that selection must be opposed if the higher adaptive climes are to be assailed by a lineage. Wright notes that there must be some trial and error mechanism on a grand scale by which the species may explore the region surrounding the small portion of the field which it occupies. To evolve, the species must not be under the strict control of selection. 167 The random sampling errors introduced by genetic drift thus become incredibly important for the discovery of higher adaptive peaks. Gould and Lewontin suggest that drift is ignored by adaptationists168 and that drift frustrates adaptation, 169 however, the landscape metaphor allows one to appreciate the importance of drift for adaptation. As Dawkins writes,
unalloyed natural selection is in a sense an anti-perfection mechanism, hugging, as it will, the tops of the low foot-hills of Wrights adaptive landscape. A mixture of strong selection interspersed with periods of relaxation of selection and drift may be the formula for crossing the valleys to the high uplands.170

Modern adaptationists second Darwins acknowledgement of a multiplicity of evolutionary forces. 171 The adaptationist programme does not deny that factors such as drift play a significant role in determining evolutionary trajectories. Selection is a necessary condition for adaptive evolution, but it is not by itself sufficient. Adaptive explanations which make no mention of non-selective factors do not deny that such factors significantly were responsible for determining a given evolutionary trajectory. In advancing an adaptive explanation, the adaptationist is not concerned with advancing an actual-sequence explanation of the trajectory, offering a detailed account of the trajectorys causal history. Instead, the adaptationist is concerned with offering a robust process account of the trajecto rys causal history, positing that trajectories in other worlds subject to the similar selective regimes would result in similar functional outcomes. 172

167 168

Wright 1932, p.359. Gould and Lewontin 1979, p.151-152. 169 Ibid., p.590-591. 170 Dawkins 1982, p.40. 171 See Darwin 1880. 172 See Sterelny 2001.

Appendix C
Darwin and adaptation In his Natural Theology173 William Paley presented the classical formulation of the argument from design, appealing to the many exquisite adaptations which pervade the living world, such as the human eye, and reasoning that these complex assemblages, formed of numerous interacting parts, could not be the result of mere chance. Chance could never satisfactorily account for states of organized complexity which demanded special explanation. Paleys artefactual interpretation of organic systems 174 led him to reason analogously that, just as artefacts require artificers, so, too, the design of the living world requires a designer. In walking across a heath and coming across a watch upon the ground , the inference, we think, is inevitable; that the watch must have had a maker; that there must have existed at some time and at some place or other, an artificer or artificers who formed it for the purpose which we find it actually to answer; who comprehended its construction, and designed its use. 175 A watch, like an eye, exhibits organized complexity, the only adequate explanation of which is divine design. Darwin was introduced to Paley during his time at Cambridge. He later wrote that Natural Theology gave him as much delight as did Euclid and that he was charmed and convinced by the long line of argumentation,176 although it is ironic that Darwin would later lay incontrovertible ruin to the Archdeacons argument. It is important to note, as Ruse does, that the argument from design is actually dipartite, consisting of (i) the argument to complexity and (ii) the argument to design. 177 Darwin accepted the argument to complexityhe was in complete agreement with Paley that organized complexity cannot be due to chance and that it requires explanation. However, Darwin rejected the argument to design, showing that the design of the living world is only apparent, or designoid, 178 and that it is the result of material processes. Darwin proceeded by breaking down the argument to design into a scientific part and a nonscientific part, giving an answer (natural selection) to the scientific part, and then saying that the nonscientific part is really not his concern as a scientist. 179 As Bowler puts it, Darwin stood Paley on his head by turning adaptation from a divinely ordained state into a natural process.180 Darwinism and natural theology both share an important first premise.181 Immersed in the tradition of British natural theology, Darwin wrote that he had always been much struck182 by adaptations. Francisco Ayala has argued that providing an explanation
173 174

Paley 1802. See Lewens 2004. 175 Paley 1802, p.4. 176 Neve and Messenger 2002, p.31. 177 Ruse 2003, p.15-17. 178 Dawkins 1996. 179 Ibid., p.112. 180 Bowler 1988, p.23. 181 Ruse 2008, p.254. 182 Neve and Messenger 2002, p.72.

for adaptation was Darwins primary concern, to which providing evidence for evolution was ancillary. 183 Such an interpretation does not compel, however. 184 Darwin wrote that by 1838 he had perceived that selection was the keystone of mans success in making useful races of animals and plants, although he failed to see how selection could be applied to organisms living in a state of nature185 Utilising principles of Malthusian economics, Darwin argued that given a struggle for existence favourable variations would tend to be preserved, and unfavourable ones to be destroyed, resulting in the formation of new species. 186 Natural selection could account for the adaptation, as well as the formation and diversification, of species. Now that he had a theory by which to work,187 Darwin was convinced of transmutationism, and in constructing his argument he repeatedly claimed that the facts of the living world became intelligible under his evolutionary hypothesis. Part of this project required that he assimilate the evidence used by the natural theologians in favour of their rival hypothesis. In the Origin,188 Darwin wrote that any theory of evolution could not be accepted until it could be shown how the innumerable species inhabiting this world have been modified, so as to acquire that perfection of structure and coadaptation which most justly excites our admiration.189 Whilst Hume had done much to undermine the design argument,190 Darwins provision of a naturalistic explanation for the existence of adaptation was responsible for its irrevocable demolition. Gould and Lewontin champion Darwin as an advocate for pluralism, as he was. Darwin affirmed the ubiquity of adaptation, writing that we see beautiful adaptations everywhere and in every part of the organic world.191 Given heritable variation and the struggle for existence, natural selection would produce adaptation. Darwin was not, however, a panadaptationist, regarding every feature as adaptive, and he acknowledged an array of evolutionary causes, the main but not exclusive192 being selection. Unlike most latenineteenth-century evolutionists, who devoted themselves to morphological studies, Darwin remained deeply fascinated by adaptation throughout the rest of his life. Towards the end of his book on orchids,193 after detailing the endless diversity of [their] beautiful adaptations, 194 Darwin wrote,
The more I study nature, the more I become impressed with ever-increasing force with the conclusion, that the contrivances and beautiful adaptations slowly acquired through each part occasionally varying in a slight degree in many ways, with the preservation or natural selection of those variations which are beneficial to the organism under the complex and evervarying conditions of life, transcend in an incomparable degree the contrivances and
183 184

Ayala 2007. Sober 2009 offers an interesting discussion of the nature of Darwins theory. 185 Neve and Messenger 2002, p.72. 186 Ibid. 187 Ibid. 188 Darwin 1859. 189 Darwin 1859, p.3. 190 Hume 1779. 191 Darwin 1859, p.61. 192 Ibid., p.6. 193 Darwin 1862. 194 Ibid., p.346.

adaptations which the most fertile imagination of the most imaginative man could suggest with unlimited time at his disposal.195

Whilst nineteenth-century evolutionism was profoundly progressionist,196 Darwin saw the positioning of species on a ladder of progress as imponderable because all are excellently adapted to their conditions of life.197 Adaptations exalt every species, each branch of lifes great tree a unique wonder. Bowler writes that Darwins later scientific work had taken him away from the great issues of the day to concentrate on small-scale topics that could be illuminated by his particular approach to evolutionism. 198 Darwins chief concern was with the processes of evolution, his theory created from the study of small-scale changes in the modern world,199 whilst many of his contemporaries were concerned with phylogeny, something which Darwin (probably wisely, given the available methods) avoided. 200 The adaptationist programme is evidently in line with Darwins thought. As has been argued, and as Darwin would have affirmed, adaptation is not the whole story, although one could make a very good case that it is the most important part of it. 201

195 196

Ibid., p.351. See Bowler 1988. 197 Darwin 1862, p.333. 198 Bowler 1990, p.137. 199 Ibid., p.138. 200 Hulll 1988, p.427. 201 Gould (1993, p.311) writes that Darwins theory of natural seletion is undeniably functionalist in its basic mechanismand no prominent critic has ever denied this plain meaning. Natural selection is a theory devised to explain adaptation and committed to the hegemony of adaptation as a proper description of nature.

Appendix D
Gould and Conway Morris One of Goulds central theses, which he famously explored in his book Wonderful life,202 is the contingency of evolution. In a famous thought experiment he considered rewinding and erasing the tape of evolution and then letting the tape run again. Gould averred that any replay of the tape would lead evolution down a pathway radically different from the road actually taken.203 Whilst small-scale (microevolutionary) processes of adaptive evolution may be predictable, the large-scale (macroevolutionary) evolution of lineages is determined by contingent concatenations. For Gould, the adaptive landscape is large, the movement of lineages across the landscape is highly constrained, and it is unlikely that a lineage will be capable of ascending the higher climes because of stringent constraints on development. Gould rejected the extrapolation from microevolutionary to macroevolutionary processes, 204 arguing that selection occurs at multiple levels and chance events such as mass extinctions significantly affect the broad course of evolution. One of the most dramatic of these extinctions was that of the Cretaceous in which the dinosaurs were extirpated. According to Gould, were it not for this event, there would have been no mammalian diversification and certainly no humans: In an entirely literal sense, we owe our existence, as large and reasoning mammals, to our lucky stars. 205 Whilst such a conception of the evolutionary process would not prohibit the pursuit of an adaptationist programme, one can see how it would be of limited application, probably restricted solely to investigations of the microevolutionary transformations within lineages and could not be used to investigate largescale transformations across lineages. Conway Morris, also a palaeontologist, propounds a thesis almost antithetical to Goulds.206 For Conway Morris, the most striking feature of evolution is not contingency, but, rather, convergencethe phenomenon whereby similar adaptations arise multiple times in independent lineages. One of the most frequently cited examples of convergence is the evolution of the camera eye in vertebrates and cephalopods. Conway Morris speaks of lineages repeatedly discovering solutions to particular needs.207 For Conway Morris, the adaptive landscape is also large, however the number of pathways available to lineages is few: Isolated islands provide havens of biological possibility in an ocean of maladaptedness.208 Conway Morris is committed to Darwinian adaptationism, 209 remarking

202 203

Gould 1989. Ibid., p.51. 204 Sterelny 2007, p.84-86. 205 Gould 1989, p.318. 206 See Conway Morris 1998, 2003. 207 Conway Morris 2003, p.xii. 208 Ibid., p.19.

that life has an extraordinary propensity for its metaphorical hand to fit the glove.210 Evolution is constrained, but constraints stem not from a lineages history, but from the limited number of solutions to a particular need. Conway Morris remarks that we should expect the existence of biological spandrels, but he considers the notion to have had an entirely disproportionate influence.211 Conway Morris argues that the ubiquity of convergence confirms, as if there were ever any doubt, the reality of evolutionary adaptation.212 The repeated evolution of similar adaptations does seem to provide warrant for making adaptive generalisations. Conway Morris acknowledges the existence of constraints in lineages, however he adds that what is far more interesting is the way in which org anisms repeatedly get round these problems, which is why convergences are ubiquitous. 213 A world of convergence eloquently attests to the reality of adaptation and requires that an adaptationist programme is followed. Conway Morris seems to regard macroevolution to be microevolution writ large when he writes that adaptation is the motor of evolution. 214 Nevo argues that convergence substantiates a critical adaptationist program, which is the only viable program to explain biological evolution.215

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Darwins formulation of the mechanisms of evolution i s not only straightforward, but seemingly irrefutable. Organisms live in a real world, and evolve to fit their environment by a process of continuous adaptation. This is achieved by a constant winnowing through the operation of natural selection that scrutinizes the available variation to confer reproductive success on those that, by one yardstick or another, are fitter in the struggle for survival (ibid., p.1.) 210 Ibid., p.20. 211 Ibid., p.301. 212 Ibid., p.301-302. 213 Ibid., p.302. 214 Ibid., p.303. 215 Nevo 2001, p.6235.

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Notes on figures
What is the nature and justification of an adaptationist programme in evolutionary biology? Figure 1. Image sourced from H. B. D. Kettlewell, Further selection experiments on industrial melanism in the Lepidoptera, Heredity, 10 (3): 287-301, (1956). Figure 2. Image sourced from T. Lewens, Adaptationism and engineering, Biology and Philosophy, 17: 1-31, (2002). Figure 3. Image sourced from G. Halder, P. Callaerts and W. J. Gehring, Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science, 267 (5205): 1788-1792, (1995).

Figure 4. Image sourced from S. J. Gould and R. C. Lewontin, The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme, Proceedings of the Royal Society of London B, 205 (1161): 581-598, (1979). Figure 5. Image sourced from D. M. Raup, Geometric analysis of shell coiling: coiling in ammonoids, Journal of Palaeontology, 41 (1): 43-65, (1967). Figure 6. See note for Figure 5. Figure 7. Image sourced from Ask Nature, Insects cycle nutrients: periodic cicadas, [online] available at: http://www.asknature.org/strategy/13eeb901a87ef3d51a5d52caf2e0c089, (15 June 2012), [accessed 25 February 2013]. Appendix A: The adaptive landscape and the importance of perspective Figure 1. Image sourced from S. Wright, The roles of mutation, inbreeding, crossbreeding and selection in evolution, Proceedings of the Sixth International Congress of Genetics, 1: 356-366, (1932). Figure 2. Image sourced from P. Godfrey-Smith and J. F. Wilkins, Adaptationism and the adaptive landscape, Biology & Philosophy, 24: 199-214, (2009) (with personal editions and annotations). Figure 3. See note for Figure 1 (with personal annotations). Figure 4. See note for Figure 1 (with personal annotations).

Glossary
adaptation the fit between an organism and its environment; may refer to a feature of an organism which promotes survival and reproduction; may also refer to the process whereby organisms within a population become adapted one who believes that natural selection is the primary causal mechanism of evolutionary change and that much of evolutionary change is adaptive. Adaptationists are typically also committed to the gradualness of evolution and the rather vague notion that organisms are well designed

adaptationist

adaptationism

refers to an array of views about the evolutionary process and its investigation: empirical adaptationism holds that selection is the most important causal mechanism in evolution; explanatory adaptationism holds that adaptation should be the focus of the evolutionary biologists enquiries; and methodological adaptationism holds that biological systems should be investigated from an adaptationist stance (see Godfrey-Smith 2001 and also Lewens 2009) a variant form of a gene the view that an ecological niches pre-exist organisms said to have occupied a given niche where a slight phenotypic variation does not result in a drastic variation in fitness; a requisite condition for adaptive evolution, as it allows effective movement across an adaptive landscape the ability of a genome to produce adaptive variants the belief that an explanation of the biological properties of an organism can be given in terms of factors internal to the organism; contrasted with internalism a measure of an organisms ability to survive and rep roduce a unit of heredity; the term is commonly used in two senses: a concrete sense, referring to the physical sequence of DNA nucleotide bases; and a more abstract sense, referring to any hereditary information for which there is a favourable or unfavourable selection bias equal to several or many times its rate of endogenous change (Dawkins 1982, p.25) changes in allele frequencies due to chance processes which occurs most significantly in smaller populations as there is a smaller gene pool the entire set of alleles within a population the entire set of alleles possessed by an organism the genetic basis of a phenotypic feature the belief that evolutionary change is, on the whole, gradual a characteristic, such as the vertebrate forelimb, shared by different species due to inheritance from a common ancestor

allele constructionism

continuity

evolvability externalism

fitness gene

genetic drift

gene pool genome genotype gradualism homology

internalism

the belief that an explanation of the biological properties of an organism can be given in terms of factors internal to the organism; contrasted with externalism the position of a gene on a chromosome dark pigmentation of the skin of an animal a random alteration in a genetic sequence; the source of raw variation in a population a model comprising a phenotype set, state equations, fitness measure and heritability assumption used to determine whether a phenotype is optimal the visible characteristics of an organism programmed by the genotype the evolutionary relationship between organisms the phenomenon whereby one gene may exert numerous phenotypic effects; if traits A (an advantageous trait) and B (a disadvantageous trait) are associated by pleiotropy, selection of A also results in selection of B the belief that evolution is caused by multiple mechanisms, often contrasted with adaptationism, even though all evolutionary biologists believe that evolution is the result of multiple mechanisms; pluralists typically claim that adaptationists unduly neglect non-selective mechanisms

locus melanism mutation

optimality model

phenotype phylogeny pleiotropy

pluralism

quasi-independence the possibility of one trait being shaped by selection without also significantly affecting other traits; a requisite condition for adaptive evolution reverse-engineering the attempt to infer the design process of a trait or an artefact from an analysis of the items structure saltation a macro-mutation resulting in a biological structure vastly different from the parental structure