The Extended Phenotype: The Long Reach of the Gene (Popular Science) (12 page)

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 group-selectionist
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!

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 time-lag 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 chess-playing 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 tree-dwelling 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.

One of my purposes in this book is to question the ‘central theorem’ that it is useful to expect individual organisms to behave in such a way as to maximize their own inclusive fitness, or in other words to maximize the survival of copies of the genes inside them. The end of the previous chapter suggests one way in which the central theorem might be violated. Organisms might consistently work in the interests of other organisms rather than of themselves. That is, they might be ‘manipulated’.

The fact that animals frequently cause other animals to perform some action that is against their own best interests is, of course, well known. Obviously it happens every time an angler fish catches prey, every time a cuckoo is fed by its foster mother. I shall make use of both these examples in this chapter, but I shall also emphasize two points that have not always been stressed. Firstly, it is natural to assume that even if a manipulator gets away with it temporarily, it is only a matter of evolutionary time before the lineage of manipulated organisms comes up with a counter-adaptation. In other words, we tend to assume that manipulation only works because of the ‘time-lag’ constraint on perfection. In this chapter I shall point out that, on the contrary, there are conditions under which we should expect manipulators to succeed consistently and for indefinite lengths of evolutionary time. I shall discuss this later under the catch-phrase of ‘arms races’.

Secondly, until the last decade or so, most of us have paid insufficient attention to the likelihood of intraspecific manipulation, especially exploitative manipulation within the family. I attribute this deficiency to a residuum of group-selectionist intuition which often lurks in the depths of the biologist’s mind even after group selection has been rejected at the surface level of reason. I think that a minor revolution has taken place in the way we think about social relationships. ‘Genteel’ (Lloyd 1979) ideas of vaguely benevolent mutual cooperation are replaced by an expectation of stark, ruthless, opportunistic mutual exploitation (e.g. Hamilton 1964a,b, 1970, 1971a; Williams 1966; Trivers 1972, 1974.; Ghiselin 1974a; Alexander
1974). This revolution is popularly associated with the name ‘sociobiology’, although the association is somewhat ironic since, as I have suggested before, Wilson’s (1975) great book of that name is in many respects pre-revolutionary in attitude: not the new synthesis, but the last and greatest synthesis of the old, benevolent regime (e.g. his
Chapter 5
).