The Extended Phenotype: The Long Reach of the Gene (Popular Science) (10 page)

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 ‘valley-crossing’, 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).

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! Just-so 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.