The Extended Phenotype: The Long Reach of the Gene (Popular Science) (7 page)

Consider the most famous example of single gene control of complex
behaviour, the case of Rothenbuhler’s (1964) hygienic bees. The point of using this example is that it illustrates well how a highly complex behaviour difference can be due to a single gene difference. The hygienic behaviour of the Brown strain of honeybees involves the whole neuromuscular system, but the fact that they perform the behaviour whereas Van Scoy bees do not is, according to Rothenbuhler’s model, due to differences at two loci only. One locus determines the uncapping of cells containing diseased brood, the other locus determines the removing of diseased brood after uncapping. It would be possible, therefore, to imagine a natural selection in favour of uncapping behaviour and a natural selection in favour of removing behaviour, meaning selection of the two genes versus their respective alleles. But the point I am making here is that, although that could happen, it is not likely to be very interesting evolutionarily. The modern uncapping gene and the modern removing gene may very well not have been involved in the original natural selection process that steered the evolutionary putting together of the behaviour.

Rothenbuhler observed that even Van Scoy bees sometimes perform hygienic behaviour. They are just quantitatively much less likely to do so than are Brown bees. It is likely, therefore, that both Brown and Van Scoy bees have hygienic ancestors, and both have in their nervous systems the machinery of uncapping and removing behaviour: it is just that Van Scoy bees have genes that prevent them from turning the machinery on. Presumably if we went back even further in time we should find an ancestor of all modern bees which not only was not hygienic itself but had never had a hygienic ancestor. There must have been an evolutionary progression building up the uncapping and removing behaviour from nothing, and this evolutionary progression involved the selection of many genes which are now fixed in both the Brown and the Van Scoy strains. So, although the uncapping and the removing genes of the Brown strain really are rightly called genes for uncapping and removing, they are defined as such only because they happen to have alleles whose effect is to prevent the behaviour from being performed. The mode of action of these alleles could be boringly destructive. They might simply cut some vital link in the neural machinery. I am reminded of Gregory’s (1961) vivid illustration of the perils of making inferences from ablation experiments on the brain: ‘… the removal of any of several widely spaced resistors may cause a radio set to emit howls, but it does not follow that howls are immediately associated with these resistors, or indeed that the causal relation is anything but the most indirect. In particular, we should not say that the function of the resistors in the normal circuit is to inhibit howling. Neurophysiologists, when faced with a comparable situation, have postulated “suppressor regions”.’

This consideration seems to me to be a reason for caution, not a reason for rejecting the whole genetic theory of natural selection! Never mind if living
geneticists are debarred from studying the particular loci at which selection in the past gave rise to the original evolution of interesting adaptations. It is too bad if geneticists usually are forced to concentrate on loci that are convenient rather than evolutionarily important. It is
still
true that the evolutionary putting together of complex and interesting adaptation consisted in the replacement of genes by their alleles.

This argument can contribute tangentially to the resolution of a fashionable contemporary dispute, by helping to put the issue in perspective. It is now highly, indeed passionately, controversial whether there is significant genetic variation in human mental abilities. Are some of us genetically brainier than others? What we mean by ‘brainy’ is also highly contentious, and rightly so. But I suggest that, by any meaning of the term, the following propositions cannot be denied. (1) There was a time when our ancestors were less brainy than we are. (2) Therefore there has been an increase in braininess in our ancestral lineage. (3) That increase came about through evolution, probably propelled by natural selection. (4) Whether propelled by selection or not, at least part of the evolutionary change in phenotype reflected an underlying genetic change: allele replacement took place and consequently mean mental ability increased over generations. (5) By definition therefore, at least in the past, there must have been significant genetic variation in braininess within the human population. Some people were genetically clever in comparison with their contemporaries, others were genetically relatively stupid.

The last sentence may engender a
frisson
of ideological disquiet, yet none of my five propositions could be seriously doubted, nor could their logical sequence. The argument works for brain size, but it equally works for any behavioural measure of cleverness we care to dream up. It does not depend on simplistic views of human intelligence as being a one-dimensional scalar quantity. The fact that intelligence is not a simple scalar quantity, important as that fact is, is simply irrelevant. So is the difficulty of measuring intelligence in practice. The conclusion of the previous paragraph is inevitable, provided only that we are evolutionists who agree to the proposition that once upon a time our ancestors were less clever (by whatever criterion) then we are. Yet in spite of all that, it still does not follow that there is any genetic variation in mental abilities left in the human population today: the genetic variance might all have been used up by selection. On the other hand it might not, and my thought experiment shows at least the inadvisability of dogmatic and hysterical opposition to the very possibility of genetic variation in human mental abilities. My own opinion, for what it is worth, is that even if there is such genetic variation in modern human populations, to base any policy on it would be illogical and wicked.

The existence of a Darwinian adaptation, then, implies the sometime existence of genes for producing the adaptation. This is not always made
explicit. It is always possible to talk about the natural selection of a behaviour pattern in two ways. We can either talk about individuals with a tendency to perform the behaviour pattern being ‘fitter’ than individuals with a less strongly developed tendency. This is the now fashionable phraseology, within the paradigm of the ‘selfish organism’ and the ‘central theorem of sociobiology’. Alternatively, and equivalently, we can talk directly of genes for performing the behaviour pattern surviving better than their alleles. It is always legitimate to postulate genes in any discussion of Darwinian adaptation, and it will be one of my central points in this book that it is often positively beneficial to do so. Objections, such as I have heard made, to the ‘unnecessary geneticizing’ of the language of functional ethology, betray a fundamental failure to face up to the reality of what Darwinian selection is all about.

Let me illustrate this failure by another anecdote. I recently attended a research seminar given by an anthropologist. He was trying to interpret the incidence among various human tribes of a particular mating system (it happened to be polyandry) in terms of a theory of kin selection. A kin selection theorist can make models to predict the conditions under which we would expect to find polyandry. Thus, on one model applied to Tasmanian native hens (Maynard Smith & Ridpath 1972), the population sex ratio would need to be male-biased, and partners would need to be close kin, before a biologist would predict polyandry. The anthropologist sought to show that his polyandrous human tribes lived under such conditions, and, by implication, that other tribes showing the more normal patterns of monogamy or polygyny lived under different conditions.

Though fascinated by the information he presented, I tried to warn him of some difficulties in his hypothesis. I pointed out that the theory of kin selection is fundamentally a genetic theory, and that kin-selected adaptations to local conditions had to come about through the replacement of alleles by other alleles, over generations. Had his polyandrous tribes been living, I asked, under their current peculiar conditions for long enough—enough generations—for the necessary genetic replacement to have taken place? Was there, indeed, any reason to believe that variations in human mating systems are under genetic control at all?

The speaker, supported by many of his anthropological colleagues in the seminar, objected to my dragging genes into the discussion. He was not talking about genes, he said, but about a social behaviour pattern. Some of his colleagues seemed uncomfortable with the very mention of the four-letter word ‘gene’. I tried to persuade him that it was
he
who had ‘dragged genes in’ to the discussion although, to be sure, he had not mentioned the word gene in his talk. That is exactly the point I am trying to make. You cannot talk about kin selection, or any other form of Darwinian selection,
without
dragging genes in, whether you do so explicitly or not. By even speculating
about kin selection as an explanation of differences in tribal mating systems, my anthropologist friend was implicitly dragging genes into the discussion. It is a pity he did not make it
explicit
, because he would then have realized what formidable difficulties lay in the path of his kin selection hypothesis: either his polyandrous tribes had to have been living, in partial genetic isolation, under their peculiar conditions for a large number of centuries, or natural selection had to have favoured the universal occurrence of genes programming some complex ‘conditional strategy’. The irony is that, of all the participants in that seminar on polyandry, it was I who was advancing the least ‘genetically deterministic’ view of the behaviour under discussion. Yet because I insisted on making the genetic nature of the kin selection hypothesis explicit, I expect I appeared to be characteristically obsessed with genes, a ‘typical genetic determinist’. The story illustrates well the main message of this chapter, that frankly facing up to the fundamental genetic nature of Darwinian
selection
is all too easily mistaken for an unhealthy preoccupation with hereditarian interpretations of ontogenetic
development
.

The same prejudice against explicit mention of genes where one can get away with an individual-level circumlocution is common among biologists. The statement, ‘genes for performing behaviour X are favoured over genes for not performing X’ has a vaguely naive and unprofessional ring to it. What evidence is there for such genes? How dare you conjure up
ad hoc
genes simply to satisfy your hypothetical convenience! To say ‘individuals that perform X are fitter than individuals that do not perform X’ sounds much more respectable. Even if it is not known to be true, it will probably be accepted as a permissible speculation. But the two sentences are exactly equivalent in meaning. The second one says nothing that the first does not say more clearly. Yet if we recognize this equivalence and talk explicitly about genes ‘for’ adaptations, we run the risk of being accused of ‘genetic determinism’. I hope I have succeeded in showing that this risk results from nothing more than misunderstanding. A sensible and unexceptionable way of thinking about natural selection—‘gene selectionism’—is mistaken for a strong belief about development—‘genetic determinism’. Anyone who thinks clearly about the details of how adaptations come into being is almost bound to think, implicitly if not explicitly, about genes, albeit they may be hypothetical genes. As I shall show in this book, there is much to be said for making the genetic basis of Darwinian functional speculations explicit rather than implicit. It is a good way of avoiding certain tempting errors of reasoning (Lloyd 1979). In doing this we may give the impression, entirely for the wrong reason, of being obsessed with genes and all the mythic baggage that genes carry in the contemporary journalistic consciousness. But determinism, in the sense of an inflexible, tramline-following ontogeny, is, or should be, a thousand miles from our thoughts. Of course, individual sociobiologists may or may not be genetic determinists. They may be
Rastafarians, Shakers or Marxists. But their private opinions on genetic determinism, like their private opinions on religion, have nothing to do with the fact that they use the language of ‘genes for behaviour’ when talking about natural selection.

A large part of this chapter has been based on the assumption that a biologist might wish to speculate on the Darwinian ‘function’ of behaviour patterns. This is not to say that all behaviour patterns necessarily have a Darwinian function. It may be that there is a large class of behaviour patterns which are selectively neutral or deleterious to their performers, and cannot usefully be regarded as the products of natural selection. If so, the arguments of this chapter do not apply to them. But it is legitimate to say ‘I am interested in adaptation. I don’t necessarily think all behaviour patterns are adaptations, but I want to study those behaviour patterns that are adaptations.’ Similarly, to express a preference for studying vertebrates rather than invertebrates does not commit us to the belief that all animals are vertebrates. Given that our field of interest is adaptive behaviour, we cannot talk about the Darwinian evolution of the objects of interest without postulating a genetic basis for them. And to use ‘a gene for X’ as a convenient way of talking about ‘the genetic basis of X’, has been standard practice in population genetics for over half a century.

The question of how large is the class of behaviour patterns that we can consider to be adaptations is an entirely separate question. It is the subject of the next chapter.

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’.