Constraints on Perfection
In one way or another, this book is largely preoccupied with the logic of Darwinian explanations of function. Bitter experience warns that a biologist who shows a strong interest in functional explanation is likely to be accused, sometimes with a passion that startles those more accustomed to scientific than ideological debate (Lewontin 1977), of believing that all animals are perfectly optimal—accused of being an ‘adaptationist’ (Lewontin 1979a,b; Gould & Lewontin 1979). Adaptationism is defined as ‘that approach to evolutionary studies which assumes without further proof that all aspects of the morphology, physiology and behavior of organisms are adaptive optimal solutions to problems’ (Lewontin 1979b). In the first draft of this chapter I expressed doubts that anyone was truly an adaptationist in the extreme sense, but I have recently found the following quotation from, ironically enough, Lewontin himself: ‘That is the one point which I think all evolutionists are agreed upon, that it is virtually impossible to do a better job than an organism is doing in its own environment’ (Lewontin 1967). Lewontin has since, it seems, travelled his road to Damascus, so it would be unfair to use him as my adaptationist spokesman. Indeed together with Gould he has, in recent years, been one of the most articulate and forceful critics of adaptationism. As my representative adaptationist I take A. J. Cain, who has remained (Cain 1979) consistently true to the views expressed in his trenchant and elegant paper on ‘The perfection of animals’.
Writing as a taxonomist, Cain (1964) is concerned to attack the traditional dichotomy between ‘functional’ characters, which by implication are not reliable taxonomic indicators, and ‘ancestral’ characters which are. Cain argues forcefully that ancient ‘groundplan’ characters, like the pentadactyl limb of tetrapods and the aquatic phase of amphibians, are there because they are functionally useful, rather than because they are inescapable historical legacies as is often implied. If one of two groups ‘is in any way more primitive than the other, then its primitiveness must in itself be an adaptation to some less specialized mode of life which it can pursue successfully; it cannot be merely a sign of inefficiency’ (p. 57). Cain makes a similar point about so-called trivial characters, criticizing Darwin for being too ready, under the at first sight surprising influence of Richard Owen, to concede functionlessness: ‘No one will suppose that the stripes on the whelp of a lion, or the spots on the young blackbird, are of any use to these animals …’ Darwin’s remark must sound foolhardy today even to the most extreme critic of adaptationism. Indeed, history seems to be on the side of the adaptationists, in the sense that in particular instances they have confounded the scoffers again and again. Cain’s own celebrated work, with Sheppard and their school, on the selection pressures maintaining the banding polymorphism in the snail Cepaea nemoralis may have been partly provoked by the fact that ‘it had been confidently asserted that it could not matter to a snail whether it had one band on its shell or two’ (Cain, p. 48). ‘But perhaps the most remarkable functional interpretation of a “trivial” character is given by Manton’s work on the diplopod Polyxenus, in which she has shown that a character formerly described as an “ornament” (and what could sound more useless?) is almost literally the pivot of the animal’s life’ (Cain, p. 51).
Adaptationism as a working hypothesis, almost as a faith, has undoubtedly been the inspiration for some outstanding discoveries. von Frisch (1967), in defiance of the prestigious orthodoxy of von Hess, conclusively demonstrated colour vision in fish and in honeybees by controlled experiments. He was driven to undertake those experiments by his refusal to believe that, for example, the colours of flowers were there for no reason, or simply to delight men’s eyes. This is, of course, not evidence for the validity of adaptationist faith. Each question must be tackled afresh, on its merits.
Wenner (1971) performed a valuable service in questioning von Frisch’s dance language hypothesis, since he provoked J. L. Gould’s (1976) brilliant confirmation of von Frisch’s theory. If Wenner had been more of an adaptationist Gould’s research might never have been done, but Wenner would also not have allowed himself to be so blithely wrong. Any adaptationist, while perhaps conceding that Wenner had usefully exposed lacunae in von Frisch’s original experimental design, would instantly have jumped, with Lindauer (1971), on the fundamental question of why bees dance at all. Wenner never denied that they dance, nor that the dance contained all the information about the direction and distance of food that von Frisch claimed. All he denied was that other bees used the dance information. An adaptationist could not have rested happy with the idea of animals performing such a time-consuming, and above all complex and statistically improbable, activity for nothing. Adaptationism cuts both ways, however. I am now delighted that Gould did his clinching experiments, and it is entirely to my discredit that, even in the unlikely event of my having been ingenious enough to think of them, I would have been too adaptationist to have bothered. I just knew Wenner was wrong (Dawkins 1969)!
Adaptationist thinking, if not blind conviction, has been a valuable stimulator of testable hypotheses in physiology. Barlow’s (1961) recognition of the overwhelming functional need in sensory systems to reduce redundancy in input led him to a uniquely coherent understanding of a variety of facts about sensory physiology. Analogous functional reasoning can be applied to the motor system, and to hierarchical systems of organization generally (Dawkins 1976b; Hailman 1977). Adaptationist conviction cannot tell us about physiological mechanism. Only physiological experiment can do that. But cautious adaptationist reasoning can suggest which of many possible physiological hypotheses are most promising and should be tested first.
I have tried to show that adaptationism can have virtues as well as faults. But this chapter’s main purpose is to list and classify constraints on perfection, to list the main reasons why the student of adaptation should proceed with caution. Before coming to my list of six constraints on perfection, I should deal with three others that have been proposed, but which I find less persuasive. Taking, first, the modern controversy among biochemical geneticists about ‘neutral mutations’, repeatedly cited in critiques of adaptationism, it is simply irrelevant. If there are neutral mutations in the biochemists’ sense, what this means is that any change in polypeptide structure which they induce has no effect on the enzymatic activity of the protein. This means that the neutral mutation will not change the course of embryonic development, will have no phenotypic effect at all, as a whole-organism biologist would understand phenotypic effect. The biochemical controversy over neutralism is concerned with the interesting and important question of whether all gene substitutions have phenotypic effects. The adaptationism controversy is quite different. It is concerned with whether, given that we are dealing with a phenotypic effect big enough to see and ask questions about, we should assume that it is the product of natural selection. The biochemist’s ‘neutral mutations’ are more than neutral. As far as those of us who look at gross morphology, physiology and behaviour are concerned, they are not mutations at all. It was in this spirit that Maynard Smith (1976b) wrote: ‘I interpret “rate of evolution” as a rate of adaptive change. In this sense, the substitution of a neutral allele would not constitute evolution …’ If a whole-organism biologist sees a genetically determined difference among phenotypes, he already knows he cannot be dealing with neutrality in the sense of the modern controversy among biochemical geneticists
He might, nevertheless, be dealing with a neutral character in the sense of an earlier controversy (Fisher & Ford 1950; Wright 1951). A genetic difference could show itself at the phenotypic level, yet still be selectively neutral. But mathematical calculations such as those of Fisher (1930b) and Haldane (1932a) show how unreliable human subjective judgement can be on the ‘obviously trivial’ nature of some biological characters. Haldane, for example, showed that, with plausible assumptions about a typical population, a selection pressure as weak as 1 in 1000 would take only a few thousand generations to push an initially rare mutation to fixation, a small time by geological standards. It appears that, in the controversy referred to above, Wright was misunderstood (see below). Wright (1980) was embarrassed at finding the idea of evolution of nonadaptive characters by genetic drift labelled the ‘Sewall Wright effect’, ‘not only because others had previously advanced the same idea, but because I myself had strongly rejected it from the first (1929), stating that pure random drift leads “inevitably to degeneration and extinction”’. I have attributed apparent nonadaptive taxonomic differences to pleiotropy, where not merely ignorance of an adaptive significance.’ Wright was in fact showing how a subtle mixture of drift and selection can produce adaptations superior to the products of selection alone.
A second suggested constraint on perfection concerns allometry (Huxley 1932): ‘In cervine deer, antler size increases more than proportionately to body size … so that larger deer have more than proportionately large antlers. It is then unnecessary to give a specifically adaptive reason for the extremely large antlers of large deer’ (Lewontin 1979b). Well, Lewontin has a point here, but I would prefer to rephrase it. As it stands it suggests that the allometric constant is constant in a Godgiven immutable sense. But constants on one time scale can be variables on another. The allometric constant is a parameter of embryonic development. Like any other such parameter it may be subject to genetic variation and therefore it may change over evolutionary time (Clutton-Brock & Harvey 1979). Lewontin’s remark turns out to be analogous to the following: all primates have teeth; this is just a plain fact about primates, and it is therefore unnecessary to give a specifically adaptive reason for the presence of teeth in primates. What he probably meant to say is something like the following.
Deer have evolved a developmental mechanism such that growth of antlers relative to body size is allometric with a particular constant of allometry. Very probably the evolution of this allometric system of development occurred under the influence of selection pressures having nothing to do with the social function of antlers: probably it was conveniently compatible with pre-existing developmental processes in a way which we shall not understand until we know more about the biochemical and cellular details of embryology. Maybe ethological consequences of the extra large antlers of large deer exert a selective effect, but this selection pressure is likely to be swamped in importance by other selection pressures concerned with concealed internal embryological details.
Williams (1966, p. 16) invoked allometry in the service of a speculation about the selection pressures leading to increased brain size in man. He suggested that the prime focus of selection was on early teachability, at an elementary level, of children. ‘The resulting selection for acquiring verbal facility as early as possible might have produced, as an allometric effect on cerebral development, populations in which an occasional Leonardo might arise.’ Williams, however, did not see allometry as a weapon against the use of adaptive explanations. One feels that he was rightly less loyal to his particular theory of cerebral hypertrophy than to the general principle enunciated in his concluding rhetorical question: ‘Is it not reasonable to anticipate that our understanding of the human mind would be aided greatly by knowing the purpose for which it was designed?’
What has been said of allometry applies also to pleiotropy, the possession by one gene of more than one phenotypic effect. This is the third of the suggested constraints on perfection that I want to get out of the way before embarking on my main list. It has already been mentioned in my quotation from Wright. A possible source of confusion here is that pleiotropy has been used as a weapon by both sides in this debate, if indeed it is a real debate. Fisher (1930b) reasoned that it was unlikely that any one of a gene’s phenotypic effects was neutral, so how much more unlikely was it that all of a gene’s pleiotropic effects could be neutral. Lewontin (1979b), on the other hand, remarked that ‘many changes in characters are the result of pleiotropic gene action, rather than the direct result of selection on the character itself. The yellow color of the Malpighian tubules of an insect cannot itself be the subject of natural selection since that color can never be seen by any organism. Rather it is the pleiotropic consequence of red eye pigment metabolism, which may be adaptive.’ There is no real disagreement here. Fisher was talking of the selective effects on a genetic mutation, Lewontin of selective effects on a phenotypic character; it is the same distinction, indeed, as I was making in discussing neutrality in the biochemical geneticists’ sense.
Lewontin’s point about pleiotropy is related to another one which I shall come on to below, about the problem of defining what he calls the natural ‘suture lines’, the ‘phenotypic units’ of evolution. Sometimes the dual effects of a gene are in principle inseparable; they are different views of the same thing, just as Everest used to have two names depending on which side it was seen from. What a biochemist sees as an oxygen-carrying molecule may be seen by an ethologist as red coloration. But there is a more interesting kind of pleiotropy in which the two phenotypic effects of a mutation are separable. The phenotypic effect of any gene (versus its alleles) is not a property of the gene alone, but also of the embryological context in which it acts. This allows abundant opportunities for the phenotypic effects of one mutation to be modified by others, and is the basis of such respected ideas as Fisher’s (1930a) theory of the evolution of dominance, the Medawar (1952) and Williams (1957) theories of senescence, and Hamilton’s (1967) theory of Y-chromosome inertness. In the present connection, if a mutation has one beneficial effect and one harmful one, there is no reason why selection should not favour modifier genes that detach the two phenotypic effects, or that reduce the harmful effect while enhancing the beneficial one. As in the case of allometry, Lewontin took too static a view of gene action, treating pleiotropy as if it was a property of the gene rather than of the interaction between the gene and its (modifiable) embryological context.
This brings me to my own critique of naive adaptationism, my own list of constraints on perfection, a list which has much in common with those of Lewontin and Cain, and those of Maynard Smith (1978b), Oster and Wilson (1978), Williams (1966), Curio (1973) and others. There is, indeed, much more agreement than the polemical tone of recent critiques would suggest. I shall not be concerned with particular cases, except as examples. As Cain and Lewontin both stress, it is not of general interest to challenge our ingenuity in dreaming up possible advantages of particular strange things that animals do. Here we are interested in the more general question of what the theory of natural selection entitles us to expect. My first constraint on perfection is an obvious one, mentioned by most writers on adaptation.
Time lags
The animal we are looking at is very probably out of date, built under the influence of genes that were selected in some earlier era when conditions were different. Maynard Smith (1976b) gives a quantitative measure of this effect, the ‘lag load’. He (Maynard Smith 1978b) cites Nelson’s demonstration that gannets, who normally lay only one egg, are quite capable of successfully incubating and rearing two if an extra one is experimentally added. Obviously an awkward case for the Lack hypothesis on optimal clutch size, and Lack himself (1966) was not slow to use the ‘time-lag’ escape route. He suggested, entirely plausibly, that the gannet clutch size of one egg evolved during a time when food was less plentiful, and that there had not yet been time for them to evolve to meet the changed conditions.
Such post hoc rescuing of a hypothesis in trouble is apt to provoke accusations of the sin of unfalsifiability, but I find such accusations rather unconstructive, almost nihilistic. We are not in Parliament or a court of law, with advocates of Darwinism scoring debating points against opponents, and vice versa. With the exception of a few genuine opponents of Darwinism, who are unlikely to be reading this, we are all in this together, all Darwinians who substantially agree on how we interpret what is, after all, the only workable theory we have to explain the organized complexity of life. We should all sincerely want to know why gannets lay only one egg when they could lay two, rather than treating the fact as a debating point. Lack’s invoking of the ‘time-lag’ hypothesis may have been post hoc, but it is still thoroughly plausible, and it is testable. No doubt there are other possibilities which, with luck, may also be testable. Maynard Smith is surely right that we should leave aside the ‘defeatist’ (Tinbergen 1965) and untestable ‘natural selection has bungled again’ explanation as a last resort, as a matter of simple research strategy if nothing else. Lewontin (1978b) says much the same: ‘In a sense, then, biologists are forced to the extreme adaptationist program because the alternatives, although they are undoubtedly operative in many cases, are untestable in particular cases.’
Returning to the time-lag effect itself, since modern man has drastically changed the environment of many animals and plants over a time-scale that is negligible by ordinary evolutionary standards, we can expect to see anachronistic adaptations rather often. The hedgehog antipredator response of rolling up into a ball is sadly inadequate against motor cars.
Lay critics frequently bring up some apparently maladaptive feature of modern human behaviour—adoption, say, or contraception—and fling down a challenge to ‘explain that if you can with your selfish genes’. Obviously, as Lewontin, Gould and others have rightly stressed, it would be possible, depending on one’s ingenuity, to pull a ‘sociobiological’ explanation out of a hat, a ‘just-so story’, but I agree with them and Cain that the answering of such challenges is a trivial exercise; indeed it is likely to be positively harmful. Adoption and contraception, like reading, mathematics, and stress-induced illness, are products of an animal that is living in an environment radically different from the one in which its genes were naturally selected. The question, about the adaptive significance of behaviour in an artificial world, should never have been put; and although a silly question may deserve a silly answer, it is wiser to give no answer at all and to explain why.
A useful analogy here is one that I heard from R. D. Alexander. Moths fly into candle flames, and this does nothing to help their inclusive fitness. In the world before candles were invented, small sources of bright light in darkness would either have been celestial bodies at optical infinity, or they might have been escape holes from caves or other enclosed spaces. The latter case immediately suggests a survival value for approaching light sources. The former case also suggests one, but in a more indirect sense (Fraenkel & Gunn 1940). Many insects use celestial bodies as compasses.
Since these are at optical infinity, rays from them are parallel, and an insect that maintains a fixed orientation of, say, 30° to them will go in a straight line. But if the rays do not come from infinity they will not be parallel, and an insect that behaves in this way will spiral in to the light source (if steering an acute-angled course) or spiral away (if steering an obtuse-angled course) or orbit the source (if steering a course of exactly 90° to the rays). Self-immolation by insects in candle flames, then, has no survival value in itself: according to this hypothesis, it is a byproduct of the useful habit of steering by means of sources of light which are ‘assumed’ to be at infinity. That assumption was once safe. It now is safe no longer, and it may be that selection is even now working to modify the insects’ behaviour. (Not necessarily, however. The overhead costs of making the necessary improvements may outweigh the benefits they might bring: moths that pay the costs of discriminating candles from stars may be less successful, on average, than moths that do not attempt the costly discrimination and accept the low risk of self-immolation)
But now we have reached a problem which is more subtle than the simple time-lag hypothesis itself. This is the problem, already mentioned, about what characteristics of animals we choose to recognize as units which require explanation. As Lewontin (1979b) puts it, ‘What are the “natural” suture lines for evolutionary dynamics? What is the topology of phenotype in evolution? What are the phenotypic units of evolution?’ The candle flame paradox arose only because of the way in which we chose to characterize the moth’s behaviour. We asked ‘Why do moths fly into candle flames?’ and were puzzled. If we had characterized the behaviour differently and asked ‘Why do moths maintain a fixed angle to light rays (a habit which incidentally causes them to spiral into the light source if the rays happen not to be parallel)?’, we should not have been so puzzled.
Consider human male homosexuality as a more serious example. On the face of it, the existence of a substantial minority of men who prefer sexual relations with their own sex rather than with the opposite sex constitutes a problem for any simple Darwinian theory. The rather discursive title of a privately circulated homosexualist pamphlet, which the author was kind enough to send me, summarizes the problem: ‘Why are there “gays” at all? Why hasn’t evolution eliminated “gayness” millions of years ago?’ The author, incidentally, thinks the problem so important that it seriously undermines the whole Darwinian view of life. Trivers (1974), Wilson (1975, 1978), and especially Weinrich (1976) have considered various versions of the possibility that homosexuals may, at some time in history, have been functionally equivalent to sterile workers, foregoing personal reproduction the better to care for other relatives. I do not find this idea particularly plausible (Ridley & Dawkins, 1981), certainly no more so than a ‘sneaky male’ hypothesis. According to this latter idea, homosexuality represents an ‘alternative male tactic’ for obtaining matings with females. In a society with harem defence by dominant males, a male who is known to be homosexual is more likely to be tolerated by a dominant male than a known heterosexual male, and an otherwise subordinate male may be able, by virtue of this, to obtain clandestine copulations with females.
But I raise the ‘sneaky male’ hypothesis not as a plausible possibility so much as a way of dramatizing how easy and inconclusive it is to dream up explanations of this kind (Lewontin, 1979b, used the same didactic trick in discussing apparent homosexuality in Drosophila). The main point I wish to make is quite different and much more important. It is again the point about how we characterize the phenotypic feature that we are trying to explain.
Homosexuality is, of course, a problem for Darwinians only if there is a genetic component to the difference between homosexual and heterosexual individuals. While the evidence is controversial (Weinrich 1976), let us assume for the sake of argument that this is the case. Now the question arises, what does it mean to say there is a genetic component to the difference, in common parlance that there is a gene (or genes) ‘for’ homosexuality? It is a fundamental truism, of logic more than of genetics, that the phenotypic ‘effect’ of a gene is a concept that has meaning only if the context of environmental influences is specified, environment being understood to include all the other genes in the genome. A gene ‘for’ A in environment X may well turn out to be a gene for B in environment Y. It is simply meaningless to speak of an absolute, context-free, phenotypic effect of a given gene.
Even if there are genes which, in today’s environment, produce a homosexual phenotype, this does not mean that in another environment, say that of our Pleistocene ancestors, they would have had the same phenotypic effect. A gene for homosexuality in our modern environment might have been a gene for something utterly different in the Pleistocene. So, we have the possibility of a special kind of ‘time-lag effect’ here. It may be that the phenotype which we are trying to explain did not even exist in some earlier environment, even though the gene did then exist. The ordinary time-lag effect which we discussed at the beginning of this section was concerned with changes in the environment as manifested in changed selection pressures. We have now added the more subtle point that changes in the environment may change the very nature of the phenotypic character we set out to explain.
Historical constraints
The jet engine superseded the propeller engine because, for most purposes, it was superior. The designers of the first jet engine started with a clean drawing board. Imagine what they would have produced if they had been constrained to ‘evolve’ the first jet engine from an existing propeller engine, changing one component at a time, nut by nut, screw by screw, rivet by rivet. A jet engine so assembled would be a weird contraption indeed. It is hard to imagine that an aeroplane designed in that evolutionary way would ever get off the ground. Yet in order to complete the biological analogy we have to add yet another constraint. Not only must the end product get off the ground; so must every intermediate along the way, and each intermediate must be superior to its predecessor. When looked at in this light, far from expecting animals to be perfect we may wonder that anything about them works at all.
Examples of the Heath Robinson (or Rube Goldberg—Gould 1978) character of animals are harder to be confident of than the previous paragraph might lead us to expect. A favourite example, suggested to me by Professor J. D. Currey, is the recurrent laryngeal nerve. The shortest distance from the brain to the larynx in a mammal, especially a giraffe, is emphatically not via the posterior side of the aorta, yet that is the route taken by the recurrent laryngeal. Presumably there once was a time in the remote ancestry of the mammals when the straight line from origin to end organ of the nerve did run posterior to the aorta. When, in due course, the neck began to lengthen, the nerve lengthened its detour posterior to the aorta, but the marginal cost of each step in the lengthening of the detour was not great. A major mutation might have re-routed the nerve completely, but only at a cost of great upheaval in early embryonic processes. Perhaps a prophetic, God-like designer back in the Devonian could have foreseen the giraffe and designed the original embryonic routing of the nerve differently, but natural selection has no foresight. As Sydney Brenner has remarked, natural selection could not be expected to have favoured some useless mutation in the Cambrian simply because ‘it might come in handy in the Cretaceous’.
The Picasso-like face of a flatfish such as a sole, grotesquely twisted to bring both eyes round to the same side of the head, is another striking demonstration of a historical constraint on perfection. The evolutionary history of these fish is so clearly written into their anatomy, that the example is a good one to thrust down the throats of religious fundamentalists. Much the same could be said of the curious fact that the retina of the vertebrate eye appears to be installed backwards. The lightsensitive ‘photocells’ are at the back of the retina, and light has to pass through the connecting circuitry, with some inevitable attenuation, before it reaches them. Presumably it would be possible to write down a very long sequence of mutations which would eventually lead to the production of an eye whose retina was ‘the right way round’ as it is in cephalopods, and this might be, in the end, slightly more efficient. But the cost in embryological upheaval would be so great that the intermediate stages would be heavily disfavoured by natural selection in comparison with the rival, patched-up job which does, after all, work pretty well. Pittendrigh (1958) has well said of adaptive organization that it is ‘a patchwork of makeshifts pieced together, as it were, from what was available when opportunity knocked, and accepted in the hindsight, not the foresight, of natural selection’ (see also Jacob, 1977, on ‘tinkering’).
Sewall Wright’s (1932) metaphor, which has become known under the name of the ‘adaptive landscape’, conveys the same idea that selection in favour of local optima prevents evolution in the direction of ultimately superior, more global optima. His somewhat misunderstood (Wright 1980) emphasis on the role of genetic drift in allowing lineages to escape from the pull of local optima, and thereby attain a closer approximation to what a human might recognize as ‘the’ optimal solution, contrasts interestingly with Lewontin’s (1979b) invoking of drift as an ‘alternative to adaptation’. As in the case of pleiotropy, there is no paradox here. Lewontin is right that ‘the finiteness of real populations results in random changes in gene frequency so that, with a certain probability, genetic combinations with lower reproductive fitness will be fixed in a population’. But on the other hand it is also true that, to the extent that local optima constitute a limitation on the attainment of design perfection, drift will tend to provide an escape (Lande 1976). Ironically, then, a weakness in natural selection can theoretically enhance the likelihood of a lineage attaining optimal design! Because it has no foresight, unalloyed natural selection is in a sense an antiperfection mechanism, hugging, as it will, the tops of the low foot-hills of Wright’s 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. Clearly if ‘adaptationism’ is to become an issue where debating points are scored, there is scope for both sides to have it both ways!
My own feeling is that somewhere here may lie the solution to the real paradox of this section on historical constraints. The jet engine analogy suggested that animals ought to be risible monstrosities of lashed-up improvisation, top-heavy with grotesque relics of patched-over antiquity. How can we reconcile this reasonable expectation with the formidable grace of the hunting cheetah, the aerodynamic beauty of the swift, the scrupulous attention to deceptive detail of the leaf insect? Even more impressive is the detailed agreement between different convergent solutions to common problems, for instance the multiple parallels that exist between the mammal radiations of Australia, South America and the Old World. Cain (1964) remarks that, ‘Up to now it has usually been assumed, by Darwin and others, that convergence will never be so good as to mislead us’ but he goes on to give examples where competent taxonomists have been fooled. More and more groups which had hitherto been regarded as decently monophyletic, are now being suspected of polyphyletic origin.
The citation of example and counter-example is mere idle fact-dropping. What we need is constructive work on the relation between local and global optima in an evolutionary context. Our understanding of natural selection itself needs to be supplemented by a study of ‘escapes from specialization’ to use Hardy’s (1954) phrase. Hardy himself was suggesting neoteny as an escape from specialization, while in this chapter, following Wright, I have emphasized drift in this role.
Müllerian mimicry in butterflies may prove to be a useful case-study here. Turner (1977) remarks that ‘among the long-winged butterflies of the tropical American rainforests (ithomiids, heliconids, danaids, pierids, pericopids) there are six distinct warning patterns, and although all the warningly colored species belong to one of these mimicry “rings” the rings themselves coexist in the same habitats through most of the American tropics and remain very distinct… . Once the difference between two patterns is too great to be jumped by a single mutation, convergence becomes virtually impossible, and the mimicry rings will coexist indefinitely.’ This is one of the only cases where ‘historical constraints’ may be close to being understood in full genetic detail. It may provide a worthwhile opportunity also for the study of the genetic details of ‘valleycrossing’, which in the present case would consist in the detachment of a type of butterfly from the orbit of one mimicry ring, and its eventual ‘capture’ by the ‘pull’ of another mimicry ring. Though he does not invoke drift as an explanation in this case, Turner tantalizingly indicates that ‘In southern Europe Amata phegea … has … captured Zygenea ephialtes from the Müllerian mimicry ring of zygaenids, homopterans, etc. to which it still belongs outside the range of A. phegea in northern Europe …’
At a more general theoretical level, Lewontin (1978) notes that ‘there may often be several alternative stable equilibriums of genetic composition even when the force of natural selection remains the same. Which of these adaptive peaks in the space of genetic composition is eventually reached by a population depends entirely on chance events at the beginning of the selective process … For example, the Indian rhinoceros has one horn and the African rhinoceros has two. Horns are an adaptation for protection against predators but it is not true that one horn is specifically adaptive under Indian conditions as opposed to two horns on the African plains. Beginning with two somewhat different developmental systems, the two species responded to the same selective forces in slightly different ways.’ The point is basically a good one, although it is worth adding that Lewontin’s uncharacteristically ‘adaptationist’ blunder about the functional significance of rhinoceros horns is not trivial. If horns really were an adaptation against predators it would indeed be hard to imagine how a single horn could be more useful against Asian predators while two horns were of more help against African predators. However if, as seems much more likely, rhinoceros horns are an adaptation for intraspecific combat and intimidation, it could well be the case that a one-horned rhino would be at a disadvantage in one continent while a two-horned rhino would suffer in the other. Whenever the name of the game is intimidation (or sexual attraction as Fisher taught us long ago), mere conformity to the majority style, whatever that majority style may happen to be, can have advantages. The details of a threat display and its associated organs may be arbitrary, but woe betide any mutant individual that departs from established custom (Maynard Smith & Parker 1976).
Available genetic variation
No matter how strong a potential selection pressure may be, no evolution will result unless there is genetic variation for it to work on. ‘Thus, although I might argue that the possession of wings in addition to arms and legs might be advantageous to some vertebrates, none has ever evolved a third pair of appendages, presumably because the genetic variation has never been available’ (Lewontin 1979b)). One could reasonably dissent from this opinion. It may be that the only reason pigs have no wings is that selection has never favoured their evolution. Certainly we must be careful before we assume, on human-centred common-sense grounds, that it would obviously be handy for any animal to have a pair of wings even if it didn’t use them very often, and that therefore the absence of wings in a given lineage must be due to lack of available mutations. Female ants can sprout wings if they happen to be nurtured as queens, but if nurtured as workers they do not express their capacity to do so. More strikingly, the queens in many species use their wings only once, for their nuptial flight, and then take the drastic step of biting or breaking them off at the roots in preparation for the rest of their life underground. Evidently wings have costs as well as benefits.
One of the most impressive demonstrations of the subtlety of Charles Darwin’s mind is given by his discussion of winglessness and the costs of having wings in the insects of oceanic islands. For present purposes, the relevant point is that winged insects may risk being blown out to sea, and Darwin (1859, p. 177) suggested that this is why many island insects have reduced wings. But he also noted that some island insects are far from wingless; they have extra large wings.
“This is quite compatible with the action of natural selection. For when a new insect first arrived on the island, the tendency of natural selection to enlarge or to reduce the wings, would depend on whether a greater number of individuals were saved by successfully battling with the winds, or by giving up the attempt and rarely or never flying. As with mariners ship-wrecked near a coast, it would have been better for the good swimmers if they had been able to swim still further, whereas it would have been better for the bad swimmers if they had not been able to swim at all and had stuck to the wreck.”
A neater piece of evolutionary reasoning would be hard to find, although one can almost hear the baying chorus of ‘Unfalsifiable! Tautological! Justso story!’
Returning to the question of whether pigs ever could develop wings, Lewontin is undoubtedly right that biologists interested in adaptation cannot afford to ignore the question of the availability of mutational variation. It is certainly true that many of us, with Maynard Smith (1978a) though without his and Lewontin’s authoritative knowledge of genetics, tend to assume ‘that genetic variance of an appropriate kind will usually exist’. Maynard Smith’s grounds are that ‘with rare exceptions, artificial selection has always proved effective, whatever the organism or the selected character’. A notorious case, fully conceded by Maynard Smith (1978b), where the genetic variation necessary to an optimality theory often seems to be lacking, is that of Fisher’s (1930a) sex ratio theory. Cattle breeders have had no trouble in breeding for high milk yield, high beef production, large size, small size, hornlessness, resistance to various diseases, and fierceness in fighting bulls. It would obviously be of immense benefit to the dairy industry if cattle could be bred with a bias towards producing heifer calves rather than bull calves. All attempts to do this have singularly failed, apparently because the necessary genetic variation does not exist. It may be the measure of how misled is my own biological intuition that I find this fact rather astonishing, indeed worrying. I would like to think that it is an exceptional case, but Lewontin is certainly right that we need to pay more attention to the problem of the limitations of available genetic variation. From this point of view, a compilation of the amenability or resistance to artificial selection of a wide variety of characters would be of great interest.
Meanwhile, there are certain common-sense things that can be said. Firstly, it may make sense to invoke lack of available mutation to explain why animals do not have some adaptation which we think reasonable, but it is harder to apply the argument the other way round. For instance, we might indeed think that pigs would be better off with wings and suggest that they lack them only because their ancestors never produced the necessary mutations. But if we see an animal with a complex organ, or a complex and time-consuming behaviour pattern, we would seem to be on strong grounds in guessing that it must have been put together by natural selection. Habits such as dancing in bees as already discussed, ‘anting’ in birds, ‘rocking’ in stick insects, and egg-shell removal in gulls are positively time-consuming, energy-consuming and complex. The working hypothesis that they must have a Darwinian survival value is overwhelmingly strong. In a few cases it has proved possible to find out what that survival value is (Tinbergen 1963).
The second common-sense point is that the hypothesis of ‘no available mutations’ loses some of its force if a related species, or the same species in other contexts, has shown itself capable of producing the necessary variation. I shall mention below a case where the known capabilities of the digger wasp Ammophila campestris were used to illuminate the lack of similar capabilities in the related species Sphex ichneumoneus. A more subtle version of the same argument can be applied within any one species. For instance, Maynard Smith (1977, see also Daly 1979) concludes a paper with an up-beat question: Why do male mammals not lactate? We need not go into the details of why he thought they ought to; he may have been wrong, his model may have been wrongly set up, and the real answer to his question may be that it would not pay male mammals to lactate. The point here is that this is a slightly different kind of question from ‘Why don’t pigs have wings?’. We know that male mammals contain the genes necessary for lactation, because all the genes in a female mammal have passed through male ancestors and may be handed on to male descendants. Genetic male mammals treated with hormones, indeed, can develop as lactating females. This all makes it less plausible that the reason male mammals don’t lactate is simply that they haven’t ‘thought of it’ mutationally speaking. (Indeed, I bet I could breed a race of spontaneously lactating males by selecting for increased sensitivity to progressively reduced dosages of injected hormone, an interesting practical application of the Baldwin/Waddington Effect.)
The third common-sense point is that if the variation that is being postulated consists in a simple quantitative extension of already existing variation it is more plausible than a radical qualitative innovation. It may be implausible to postulate a mutant pig with wing rudiments, but it is not implausible to postulate a mutant pig with a curlier tail than existing pigs. I have elaborated this point elsewhere (Dawkins 1980).
In any case, we need a more subtle approach to the question of what is the evolutionary impact of differing degrees of mutability. It is not good enough to ask, in an all or none way, whether there is or is not genetic variation available to respond to a given selection pressure. As Lewontin (1979) rightly says, ‘Not only is the qualitative possibility of adaptive evolution constrained by available genetic variation, but the relative rates of evolution of different characters are proportional to the amount of genetic variance for each.’ I think this opens up an important line of thought when combined with the notion of historical constraints treated in the previous section. The point can be illustrated with a fanciful example.
Birds fly with wings made of feathers, bats with wings consisting of flaps of skin. Why do they not both have wings made in the same way, whichever way is ‘superior’? A confirmed adaptationist might reply that birds must be better off with feathers and bats better off with skin flaps. An extreme anti-adaptationist might say that very probably feathers would actually be better than skin-flaps for both birds and bats, but bats never had the good fortune to produce the right mutations. But there is an intermediate position, one which I find more persuasive than either extreme. Let us concede to the adaptationist that, given enough time, the ancestors of bats probably could have produced the sequence of mutations necessary for them to sprout feathers. The operative phrase is ‘given enough time’. We are not making an all-or-none distinction between impossible and possible mutational variation, but simply stating the undeniable fact that some mutations are quantitatively more probable than others. In this case, ancestral mammals might have produced both mutants with rudimentary feathers and mutants with rudimentary skin flaps. But the proto-feather mutants (they might have had to go through an intermediate stage of small scales) were so slow in making their appearance in comparison with the skin-flap mutants, that skin-flap wings had long ago appeared and led to the evolution of passably efficient wings.
The general point is akin to the one already made about adaptive landscapes. There we were concerned with selection preventing lineages from escaping the clutches of local optima. Here we have a lineage faced with two alternative routes of evolution, one leading to, say, feathered wings, the other to skin-flap wings. The feathered design may be not only a global optimum but the present local optimum as well. The lineage, in other words, may be sitting exactly at the foot of the slope leading to the feathered peak of the Sewall Wright landscape. If only the necessary mutations were available it would climb easily up the hill. Eventually, according to this fanciful parable, those mutations might have come, but— and this is the important point—they were too late. Skin-flap mutations had come before them, and the lineage had already climbed too far up the slopes of the skin-flap adaptive hill to turn back. As a river takes the line of least resistance downhill, thereby meandering in a route that is far from the most direct one to the sea, so a lineage will evolve according to the effects of selection on the variation available at any given moment. 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. My point is that lack of available variation does not have to be absolute in order to become a significant constraint on perfection. It need only be a quantitative brake to have dramatic qualitative effects. In spirit, then, I agree with Gould and Calloway (1980) when they say, citing Vermeij’s (1973) stimulating paper on the mathematics of morphological versatility that, ‘Some morphologies can be twisted, bent and altered in a variety of ways, and others cannot.’ But I would prefer to soften ‘cannot’, to make it a quantitative constraint, not an absolute barrier.
McCleery (1978), in an agreeably comprehensible introduction to the McFarland school of ethological optimality theory, mentions H. A. Simon’s concept of ‘satisficing’ as an alternative to optimizing. If optimizing systems are concerned with maximizing something, satisficing systems get away with doing just enough. In this case, doing enough means doing enough to stay alive. McCleery contents himself with complaining that such ‘adequacy’ concepts have not generated much experimental work. I think evolutionary theory entitles us to be a bit more negative a priori. Living things are not selected for their capacity simply to stay alive; they are staying alive in competition with other such living things. The trouble with satisficing as a concept is that it completely leaves out the competitive element which is fundamental to all life. In Gore Vidal’s words: ‘It is not enough to succeed. Others must fail.’
On the other hand ‘optimizing’ is also an unfortunate word because it suggests the attainment of what an engineer would recognize as the best design in a global sense. It tends to overlook the constraints on perfection which are the subject of this chapter. In many ways the word ‘meliorizing’ expresses a sensible middle way between optimizing and satisficing. Where optimus means best, melior means better. The points we have been considering about historical constraints, about Wright’s adaptive landscapes and about rivers following the line of immediate least resistance, are all related to the fact that natural selection chooses the better of present available alternatives. Nature does not have the foresight to put together a sequence of mutations which, for all that they may entail temporary disadvantage, set a lineage on the road to ultimate global superiority. It cannot refrain from favouring slightly advantageous available mutations now, so as to take better advantage of superior mutations which may arrive later. Like a river, natural selection blindly meliorizes its way down successive lines of immediately available least resistance. The animal that results is not the most perfect design conceivable, nor is it merely good enough to scrape by. It is the product of a historical sequence of changes, each one of which represented, at best, the better of the alternatives that happened to be around at the time.
Constraints of costs and materials
‘If there were no constraints on what is possible, the best phenotype would live for ever, would be impregnable to predators, would lay eggs at an infinite rate, and so on’ (Maynard Smith 1978b). ‘An engineer, given carte blanche on his drawing board could design an “ideal” wing for a bird, but he would demand to know the constraints under which he must work. Is he constrained to use feathers and bones, or may he design the skeleton in titanium alloy? How much is he allowed to spend on the wings, and how much of the available economic investment must be diverted into, say, egg production?’ (Dawkins & Brockmann 1980). In practice, an engineer will normally be given a specification of minimum performance such as ‘The bridge must bear a load of ten tons … The aeroplane wing must not break until it receives a stress three times what would be expected in worst-case turbulent conditions; now go ahead and build it as cheaply as you can.’ The best design is the one that satisfies (‘satisfices’) the criterion specification at the least cost. Any design that achieves ‘better’ than the specified criterion performance is likely to be rejected, because presumably the criterion could be achieved more cheaply.
The particular criterion specification is an arbitrary working rule. There is nothing magic about a safety margin of three times the expected worstcase conditions. Military aircraft may be designed with more risky safety margins than civilian ones. In effect, the engineer’s optimization instructions amount to a monetary evaluation of human safety, speed, convenience, pollution of the atmosphere, etc. The price put on each of these is a matter of judgement, and is often a matter of controversy.
In the evolutionary design of animals and plants, judgement does not enter into it, nor does controversy except among the human spectators of the show. In some way, however, natural selection must provide the equivalent of such judgement: risks of predation must be evaluated against risks of starving and benefits of mating with an extra female. For a bird, resources spent on making breast muscles for powering wings are resources that could have been spent on making eggs. An enlarged brain would permit a finer tuning of behaviour to environmental details, past and present, but at a cost of an enlarged head, which means extra weight at the front end of the body, which in turn necessitates a larger tail for aerodynamic stability, which in turn … Winged aphids are less fecund than wingless ones of the same species (J. S. Kennedy, personal communication). That every evolutionary adaptation must cost something, costs being measured in lost opportunities to do other things, is as true as that gem of traditional economic wisdom, ‘There is no such thing as a free lunch’.
Of course the mathematics of biological currency-conversion, of evaluating the costs of wing muscle, singing time, predator-vigilance time, etc., in some common currency such as ‘gonad equivalents’, are likely to be very complex. Whereas the engineer is allowed to simplify his mathematics by working to an arbitrarily chosen minimum threshold of performance, the biologist is granted no such luxury. Our sympathy and admiration must go out to those few biologists who have attempted to grapple with these problems in detail (e.g. Oster & Wilson 1978; McFarland & Houston 1981).
On the other hand, although the mathematics may be formidable, we don’t need mathematics to deduce the most important point, which is that any view of biological optimization that denies the existence of costs and trade-offs is doomed. An adaptationist who looks at one aspect of an animal’s body or behaviour, say the aerodynamic performance of its wings, while forgetting that efficiency in the wings can only be bought at a cost which will be felt somewhere else in the animal’s economy, would deserve all the criticism he gets. It has to be admitted that too many of us, while never actually denying the importance of costs, forget to mention them, perhaps even forget to think about them, when we discuss biological function. This has probably provoked some of the criticism that has come our way. In an earlier section I quoted Pittendrigh’s remark that adaptive organization was a ‘patchwork of makeshifts’. We must also not forget that it is a tangle of compromises (Tinbergen 1965).
In principle, it would seem a valuable heuristic procedure to assume that an animal is optimizing something under a given set of constraints, and to try to work out what those constraints are. This is a restricted version of what McFarland and his colleagues call the ‘reverse optimality’ approach (e.g. McCleery 1978). As a case study I shall take some work with which I happen to be familiar.
Dawkins and Brockmann (1980) found that the digger wasps (Sphex ichneumoneus) studied by Brockmann behaved in a way that a naive human economist might have criticized as maladaptive. Individual wasps appeared to commit the ‘Concorde Fallacy’ of valuing a resource according to how much they had already spent on it, rather than according to how much they could get out of it in the future. Very briefly, the evidence is as follows. Solitary females provision burrows with stung and paralysed katydids which are to serve as food for their larvae (see Chapter 7). Occasionally two females find themselves provisioning the same burrow, and they usually end up fighting over it. Each fight goes on until one wasp, thereby defined as the loser, flees from the area, leaving the winner in control of the burrow and all the katydids caught by both wasps. We measured the ‘real value’ of a burrow as the number of katydids which it contained. The ‘prior investment’ by each wasp in the burrow was measured as the number of katydids which she, as an individual, had put into it. The evidence suggested that each wasp fought for a time proportional to her own investment, rather than proportional to the ‘true value’ of the burrow.
Such a policy has great human psychological appeal. We too tend to fight tenaciously for property which we have put great effort into acquiring. The fallacy gets its name from the fact that, at a time when sober economic judgement of future prospects counselled abandoning the developing of the Concorde airliner, one of the arguments in favour of continuing with the half completed project was retrospective: ‘We have already spent so much on it that we cannot back out now.’ A popular argument for prolonging wars gave rise to the other name for the fallacy, the ‘Our boys shall not have died in vain’ fallacy.
When Dr Brockmann and I first realized that digger wasps behaved in like manner, I was, it has to be confessed, a little disconcerted, possibly because of my own past investment of effort (Dawkins & Carlisle 1976; Dawkins 1976a) in persuading my colleagues that the psychologically appealing Concorde Fallacy was, indeed, a fallacy! But then we started to think more seriously about cost constraints. Could it be that what appeared to be maladaptive was better interpreted as an optimum, given certain constraints? The question then became: Is there a constraint such that the wasps’ Concordian behaviour is the best they can achieve under it?
In fact the question was more complicated than that, because it was necessary to substitute Maynard Smith’s (1974) concept of evolutionary stability (‘ESS’—see Chapter 7) for that of simple optimality, but the principle remains that a reverse optimality approach might be heuristically valuable. If we can show that an animal’s behaviour is what would be produced by an optimizing system working under constraint X, maybe we can use the approach to learn something of the constraints under which animals actually do work.
In the present case it seemed that the relevant constraint might be one of sensory capacity. If the wasps, for some reason, cannot count katydids in the burrow, but can metre some aspect of their own hunting efforts, there is an asymmetry of information possessed by the two combatants. Each one ‘knows’ that the burrow contains at least b katydids, where b is the number she herself has caught. She may ‘estimate’ that the true number in the burrow is larger than b, but she does not know how much larger. Under such conditions Grafen (in preparation) has shown that the expected ESS is approximately the one originally calculated by Bishop and Cannings (1978) for the so-called ‘generalized war of attrition’. The mathematical details can be left aside; for present purposes what matters is that the behaviour expected by the extended war of attrition model would look very like the Concordian behaviour actually shown by the wasps.
If we were interested in testing the general hypothesis that animals optimize, this kind of post hoc rationalization would be suspect. By post hoc modification of the details of the hypothesis, one is bound to find a version which fits the facts. Maynard Smith’s (1978b) reply to this kind of criticism is very relevant: ‘… in testing a model we are not testing the general proposition that nature optimizes, but the specific hypotheses about constraints, optimization criteria, and heredity’. In the present case we are making a general assumption that nature does optimize within constraints, and testing particular models of what those constraints might be.
The particular constraint suggested—inability of the wasp’s sensory system to assess the contents of a burrow—is in accordance with independent evidence from the same population of wasps (Brockmann, Grafen & Dawkins 1979; Brockmann & Dawkins 1979). There is no reason to regard it as an irrevocably binding limitation for all time. Probably the wasps could evolve the capacity to assess nest contents, but only at a cost. Digger wasps of the related species Ammophila campestris have long been known to make an assessment of the contents of each of their nests every day (Baerends 1941). Unlike Sphex, which provisions one burrow at a time, lays an egg, then fills the burrow in with soil and leaves the larva to eat the provision on its own, Ammophila campestris is a progressive provisioner of several burrows concurrently. A female tends two or three growing larvae, each in a separate burrow, at the same time. The ages of her various larvae are staggered, and their food needs are different. Every morning she assesses the current contents of each burrow on a special early morning ‘inspection round’. By experimentally changing the contents of burrows, Baerends showed that the female adjusts her whole day’s provisioning of each burrow according to what it contained at the time of her morning inspection. The contents of the burrow at any other time of day have no effect on her behaviour, even though she is provisioning it all day. She appears, therefore, to use her assessment faculty sparingly, switching it off for the rest of the day after the morning inspection, almost as though it was a costly, power-consuming instrument. Fanciful as that analogy may be, it surely suggests that the assessment faculty, whatever it is, may have overhead running costs, even if (G. P. Baerends, personal communication) these consist only in the time consumed.
Sphex ichneumoneus, not being a progressive provisioner, and tending only one burrow at a time, presumably has less need than Ammophila for a burrow-assessment faculty. By not attempting to count prey in the burrow, it can save itself not only the running expenditure that Ammophila seems so careful to ration; it can also save itself the initial manufacturing costs of the necessary neural and sensory apparatus. Probably it could benefit slightly from having an ability to assess burrow contents, but only on the comparatively rare occasions when it finds itself competing for a burrow with another wasp. It is easy to believe that the costs outweigh the benefits, and that selection has therefore never favoured the evolution of assessment apparatus. I think this is a more constructive and interesting hypothesis than the alternative hypothesis that the necessary mutational variation has never arisen. Of course we have to admit that the latter might be right, but I would prefer to keep it as a hypothesis of last resort.
Imperfections at one level due to selection at another level
One of the main topics to be tackled in this book is that of the level at which natural selection acts. The kind of adaptations we should see if selection acted at the level of the group would be quite different from the adaptations we should expect if selection acts at the level of the individual. It follows that a group selectionist might well see as imperfections, features which an individual selectionist would see as adaptations. This is the main reason why I regard as unfair Gould and Lewontin’s (1979) equating of modern adaptationism with the naive perfectionism that Haldane named after Voltaire’s Dr Pangloss. With reservations due to the various constraints on perfection, an adaptationist may believe that all aspects of organisms are ‘adaptive optimal solutions to problems’, or that ‘it is virtually impossible to do a better job than an organism is doing in its given environment’. Yet the same adaptationist may be extremely fussy about the kind of meaning he allows to words like ‘optimal’ and ‘better’. There are many kinds of adaptive, indeed Panglossian, explanations, for example most groupselectionist ones, which would be utterly ruled out by the modern adaptationist.
For the Panglossian the demonstration that something is ‘beneficial’ (to whom or to what is often not specified) is a sufficient explanation for its existence. The neo-Darwinian adaptationist, on the other hand, insists upon knowing the exact nature of the selective process that has led to the evolution of the putative adaptation. In particular, he insists on precise language about the level at which natural selection is supposed to have acted. The Panglossian looks at a one-to-one sex ratio and sees that it is good: does it not minimize the wastage of the population’s resources? The neo-Darwinian adaptationist considers in detail the fates of genes acting on parents to bias the sex ratio of their offspring, and calculates the evolutionarily stable state of the population (Fisher 1930a). The Panglossian is disconcerted by 1:1 sex ratios in polygynous species, in which a minority of males hold harems and the rest sit about in bachelor herds consuming almost half the population’s food resources yet contributing not at all to the population’s reproduction. The neo-Darwinian adaptationist takes this in his stride. The system may be hideously uneconomical from the population’s point of view, but, from the point of view of the genes influencing the trait concerned, there is no mutant that could do better. My point is that neo-Darwinian adaptationism is not a catch-all, blanket faith in all being for the best. It rules out of court most of the adaptive explanations that readily occur to the Panglossian.
Some years ago, a colleague received an application from a prospective graduate student wishing to work on adaptation, who was brought up a religious fundamentalist and did not believe in evolution. He believed in adaptations, but thought they were designed by God, designed for the benefit of … ah, but that is just the problem! It might be thought that it did not matter whether the student believed adaptations were produced by natural selection or by God. Adaptations are ‘beneficial’ whether because of natural selection or because of beneficient design, and could not a fundamentalist student be usefully employed in uncovering the detailed ways in which they were beneficial? My point is that this argument will not do, because what is beneficial to one entity in the hierarchy of life is harmful to another, and creationism gives us no grounds for supposing that one entity’s welfare will be preferred to another’s. In passing, the fundamentalist student might pause to wonder at a God who goes to great trouble to provide predators with beautiful adaptations to catch prey, while with the other hand giving prey beautiful adaptations to thwart them. Perhaps He enjoys the spectator sport. Returning to the main point, if adaptations were designed by God, He might have designed them to benefit the individual animal (its survival or—not the same thing—its inclusive fitness), the species, some other species such as mankind (the usual view of religious fundamentalists), the ‘balance of nature’, or some other inscrutable purpose known only to Him. These are frequently incompatible alternatives. It really matters for whose benefit adaptations are designed. Facts such as the sex ratio in harem-forming mammals are inexplicable on certain hypotheses and easily explicable on others. The adaptationist working within the framework of a proper understanding of the genetical theory of natural selection countenances only a very restricted set of the possible functional hypotheses which the Panglossian might admit.
One of the main messages of this book is that, for many purposes, it is better to regard the level at which selection acts as neither the organism, nor the group or any larger unit, but the gene or small genetic fragment. This difficult topic will be debated in later chapters. For the present, it is sufficient to note that selection at the level of the gene can give rise to apparent imperfections at the level of the individual. I shall discuss ‘meiotic drive’ and related phenomena in Chapter 8, but the classic example is the case of heterozygous advantage. A gene may be positively selected because of its beneficial effects when heterozygous, even though it has harmful effects when homozygous. As a consequence of this, a predictable proportion of the individual organisms in the population will have defects. The general point is this. The genome of an individual organism in a sexual population is the product of a more or less random shuffling of the genes in the population. Genes are selected over their alleles because of their phenotypic effects, averaged over all the individual bodies in which they are distributed, over the whole population, and through many generations. The effects that a given gene has will usually depend upon the other genes with which it shares a body: heterozygous advantage is just a special case of this. A certain proportion of bad bodies seems an almost inevitable consequence of selection for good genes, where good refers to the average effects of a gene on a statistical sample of bodies in which it finds itself permuted with other genes.
Inevitable, that is, as long as we accept the Mendelian shuffle as given and inescapable. Williams (1979), disappointed at finding no evidence for adaptive fine-adjustment of the sex ratio, makes the perceptive point that
“Sex is only one of many offspring characters that would seem adaptive for a parent to control. For instance, in human populations affected by sickle-cell anaemia, it would be advantageous for a heterozygous woman to have her A eggs fertilized only by a-bearing sperm, and vice versa, or even to abort all homozygous embryos. Yet if mated to another heterozygote she will reliably submit to the Mendelian lottery, even though this means markedly lowered fitness for half her children … The really fundamental questions in evolution may be answerable only by regarding each gene as ultimately in conflict with every other gene, even those at other loci in the same cell. A really valid theory of natural selection must be based ultimately on selfish replicators, genes and all other entities capable of the biased accumulation of different variant forms. Amen!”
Mistakes due to environmental unpredictability or ‘malevolence’
However well adapted an animal may be to environmental conditions, those conditions must be regarded as a statistical average. It will usually be impossible to cater for every conceivable contingency of detail, and any given animal will therefore frequently be observed to make ‘mistakes’, mistakes which can easily be fatal. This is not the same point as the timelag problem already mentioned. The time-lag problem arises because of non-stationarities in the statistical properties of the environment: average conditions now are different from the average conditions experienced by the animal’s ancestors. The present point is more inescapable. The modern animal may be living in identical average conditions to those of an ancestor, yet the detailed moment to moment occurrences facing either of them are not the same from day to day, and are too complex for precise prediction to be possible.
It is particularly in behaviour that such mistakes are seen. The more static attributes of an animal, its anatomical structure for instance, are obviously adapted only to long-term average conditions. An individual is either big or small, it cannot change size from minute to minute as the need arises. Behaviour, rapid muscular movement, is that part of an animal’s adaptive repertoire which is specifically concerned with high speed adjustment. The animal can be now here, now there, now up a tree, now underground, rapidly accommodating to environmental contingencies. The number of such possible contingencies, when defined in all their detail, is like the number of possible chess positions, virtually infinite. Just as chessplaying computers (and chess-playing people) learn to classify chess positions into a manageable number of generalized classes, so the best that an adaptationist can hope for is that an animal will have been programmed to behave in ways appropriate to a manageable number of general contingency classes. Actual contingencies will fit these general classes only approximately, and apparent mistakes are therefore bound to be made.
The animal that we see up a tree may come from a long line of treedwelling ancestors. The trees in which the ancestors underwent natural selection were, in general, much the same as the trees of today. General rules of behaviour which worked then, such as ‘Never go out on a limb that is too thin’, still work. But the details of any one tree are inevitably different from the details of another. The leaves are in slightly different places, the breaking strain of the branches is only approximately predictable from their diameter, and so on. However strongly adaptationist our beliefs may be, we can only expect animals to be average statistical optimizers, never perfect anticipators of every detail.
So far we have considered the environment as statistically complex and therefore hard to predict. We have not reckoned on its being actively malevolent from our animal’s point of view. Tree boughs surely do not deliberately snap out of spite when monkeys venture on to them. But a ‘tree bough’ may turn out to be a camouflaged python, and our monkey’s last mistake is then no accident but is, in a sense, deliberately engineered. Part of a monkey’s environment is non-living or at least indifferent to the monkey’s existence, and the monkey’s mistakes can be put down to statistical unpredictability. But other parts of the monkey’s environment consist of living things that are themselves adapted to profit at the expense of monkeys. This portion of the monkey’s environment may be called malevolent.
Malevolent environmental influences may themselves be hard to predict for the same reasons as indifferent ones, but they introduce an added hazard; an added opportunity for the victim to make ‘mistakes’. The mistake made by a robin in feeding a cuckoo in its nest is presumably in some sense a maladaptive blunder. This is not an isolated, unpredictable occurrence such as arises because of the statistical unpredictability of the non-malevolent part of the environment. It is a recurrent blunder, afflicting generation after generation of robins, even the same robin several times in its life. Examples of this kind always make us wonder at the compliance, in evolutionary time, of the organisms that are manipulated against their best interests. Why doesn’t selection simply eliminate the susceptibility of robins to the deception of cuckoos? This kind of problem is one of many which I believe will one day become the stock in trade of a new subdiscipline of biology—the study of manipulation, arms races and the extended phenotype. Manipulation and arms races form the subject of the next chapter, which in some ways can be regarded as an expansion of the theme of the final section of this chapter.