The Extended Phenotype: The Long Reach of the Gene (Popular Science) (30 page)

A similar argument can be made for X chromosomes. Hamilton (1972, p. 201) pointed out that in normal diploid species a gene on an X chromosome in the homogametic sex has three-quarters of a chance of being identical by descent with a gene in a sibling of the homogametic sex. Thus the ‘X-chromosome relatedness’ of human sisters is as high as the overall relatedness of hymenopteran sisters, and higher than the overall relatedness of human sisters. Hamilton went so far as to wonder whether an X-chromosome effect
might account for the fact that helpers at the nest in birds seem, usually, to be elder brothers, rather than sisters, of the nestlings (the male sex is homogametic in birds). He noted that the X chromosome in birds accounts for some 10 per cent of the whole genome, and that it is therefore not too improbable that the genetic basis for brotherly care might lie on the X chromosome. If so, brotherly care might be favoured by the same kind of selection pressure as Hamilton had earlier suggested for sisterly care in Hymenoptera. Perhaps significantly, Syren and Luyckx (1977) point out that in some termites, the only non-haplodiploid group to have achieved full eusociality, ‘approximately half the genome is maintained as a linkage group with the sex chromosome’ (Lacy 1980).

Wickler (1977), commenting on Whitney’s (1976) rediscovery of Hamilton’s X-chromosome idea, suggests that Y-chromosome effects are potentially even more powerful than X-chromosome effects, but Y chromosomes as a rule don’t make up such a high proportion of the genome. In any case ‘sex-linked altruism’ must be
discriminating:
individuals acting under the influence of their sex chromosomes should tend to show favouritism towards close relatives of the same sex rather than of the opposite sex. Genes for sex-blind sibling care would not be outlaws.

The value of the outlawed sex-chromosome thought experiment does not lie in its plausibility—which, like Hamilton, I do not rate highly—but in the fact that it focuses our attention on the importance of this discrimination. The sex of another individual is used as a
label
to identify it as a member of a class of individuals about whose genetics something is known. In the ordinary theory of kin selection, relatedness (or rather some proximate correlate of relatedness such as presence in one’s own nest) is used as a label indicating higher than average probability of sharing a gene. From the point of view of a gene on a Y chromosome, the sex of a sibling is a label which signifies the difference between certainty of sharing the gene and certainty of not sharing it.

Note, by the way, the ineptness of notions of individual fitness, or even inclusive fitness as ordinarily understood, at dealing with situations like this. The normal calculation of inclusive fitness makes use of a coefficient of relationship which is some measure of the probability that a pair of relatives will share a particular gene, identical by descent. This is a good approximation provided the genes concerned have no better way of ‘recognizing’ copies of themselves in other individuals. If a gene is on a sex chromosome and can use the sex of relatives as a label, however, its best ‘estimate’ of the probability that a relative shares a copy of itself will be a better estimate than that provided by the coefficient of relationship. In its most general form, the principle of genes appearing to ‘recognize’ copies of themselves in other individuals has been dubbed the ‘green-beard effect’ (Dawkins 1976a, p. 96, following Hamilton 1964b, p. 25). Green-beard or
‘recognition alleles’ have been described in the literature as outlaws (Alexander & Borgia 1978; Alexander 1980), and they should therefore be discussed in this chapter, even though, as we shall see, their status as outlaws needs careful examination (Ridley & Grafen 1981).

The green-beard effect reduces the principle of ‘gene self-recognition’ to its bare essentials in an unrealistically hypothetical, but nevertheless instructive, way. A gene is postulated which has two pleiotropic effects. One effect is to confer a conspicuous label, the ‘green beard’. The other effect is to confer a tendency to behave altruistically towards bearers of the label. Such a gene, if it ever arose, could easily be favoured by natural selection, although it would be vulnerable to a mutant arising which conferred the label without the altruism.

Genes are not conscious little devils, able to recognize copies of themselves in other individuals and to act accordingly. The only way for the green-beard effect to arise is by incidental pleiotropy. A mutation must arise which just happens to have two complementary effects: the label or ‘green beard’, and the tendency to behave altruistically towards labelled individuals. I have always thought such a fortuitous conjunction of pleiotropic effects too good to be true. Hamilton also noted the idea’s inherent implausibility, but he went on ‘… exactly the same
a priori
objections might be made to the evolution of assortative mating which manifestly has evolved, probably many times independently and despite its obscure advantages’ (Hamilton 1964b, p. 25). It is worth briefly examining this comparison with assortative mating, which for present purposes I shall take to mean the tendency of individuals to prefer to mate with individuals that genetically resemble them.

Why is it that the green-beard effect seems so much more far-fetched than assortative mating? It is not just that assortative mating is positively known to occur. I suggest another reason. This is that when we think of assortative mating we implicitly assume
self-inspection
as a means of facilitating the effect. If black individuals prefer to mate with black individuals, and white with white, we do not find this hard to believe because we tacitly assume that individuals perceive their
own
colour. Each individual, whatever his colour, is assumed to be obeying the
same
rule: inspect yourself (or members of your own family) and choose a mate of the same colour. This principle does not stretch our credulity by demanding that two specific effects—colour and behavioural preference—are controlled pleiotropically by the same gene. If there is a general advantage in mating with similar partners, natural selection will favour the self-inspection rule regardless of the exact nature of the recognition character used. It does not have to be skin colour. Any conspicuous and variable character would work with the identical behavioural rule. No far-fetched pleiotropism need be postulated.

Well then, will the same kind of mechanism work for the green-beard effect? Might animals obey a behavioural rule of the form: ‘Inspect yourself
and behave altruistically towards other individuals that resemble you’? The answer is that they might, but this would not be a true example of the green-beard effect. Instead, I call it the ‘armpit effect’. In the paradigm hypothetical example, the animal is supposed to smell its own armpits, and behave altruistically towards other individuals with a similar smell. (The reason for choosing an olfactory name is that police dog trials have shown that dogs presented with handkerchiefs held under human armpits can distinguish the sweats of any two individual humans except identical twins (Kalmus 1955). This suggests that there is an enormously variable richness of genetic labelling in molecules of sweat. In the light of the result with identical twins, one feels inclined to bet that police dogs could be trained to sniff out the coefficient of relationship between pairs of humans and that, for instance, they could be trained to track down a criminal if given a sniff of his brother. Be that as it may, ‘armpit effect’ is here being used as a general name for any case of an animal inspecting himself, or a known close relative, and discriminating in favour of other individuals with a similar smell or with some other perceived similarity.)

The essential difference between the green-beard effect and the armpit self-inspection effect is as follows. The armpit self-inspection behavioural rule will lead to the detection of other individuals that are similar in some respect, perhaps in many respects, but it will not specifically lead to the detection of individuals that possess copies of the gene mediating the behavioural rule itself. The armpit rule might provide an admirable means of detecting true kin from non-kin, or of detecting whether a brother was a full brother or only a half brother. This could be very important, and it might provide the basis for selection in favour of self-inspecting behaviour, but the selection would be conventional, familiar kin selection. The self-inspection rule would be functioning simply as a kin-recognition device, analogous to a rule like: ‘Behave altruistically towards individuals that grew up in your own nest.’

The green-beard effect is quite different. Here the important thing is that a gene (or close linkage group) programs the recognition specifically of copies of
itself
. The green-beard effect is not a mechanism for the recognition of kin. Rather, kin recognition and ‘green-beard’ recognition are alternative ways in which genes could behave as if discriminating in favour of copies of themselves.

To return to Hamilton’s comparison with assortative mating, we can see that it does not really provide good grounds for optimism over the plausibility of the green-beard effect. Assortative mating is much more likely to involve self-inspection. If, for whatever reason, it is an advantage in general for like to mate with like, selection would favour an armpit type of behavioural rule: Inspect yourself, and choose a mate that resembles you. This will achieve the desired result—an optimal balance between outbreeding
and inbreeding (Bateson 1983) or whatever the advantage may be—regardless of the exact nature of the characteristics by which individuals differ.

Assortative mating is not the only analogy Hamilton might have chosen. Another one is the case of cryptic moths choosing to sit on a background that matches their own colour. Kettlewell (1955) gave dark-coloured
carbonaria
and light-coloured typical morphs of the peppered moth
Biston betularia
the opportunity to sit on dark- or light-coloured backgrounds. There was a statistically significant tendency for moths to choose a background matching their own body colour. This could be due to pleiotropism (or genes for colour being closely linked to genes for background choice). If this were so, as Sargent (1969a) believes, it might, by analogy, reduce our scepticism about the inherent plausibility of the green-beard effect. Kettlewell believed, however, that the moths achieved the matching by the simpler mechanism of ‘contrast conflict’. He suggested that a moth could see a small portion of its own body, and that it moved around until the observed contrast between its own body and the background reached a minimum. It is easy to believe that natural selection might favour the genetic basis for such a contrast-minimizing behavioural rule, because it would work automatically in conjunction with any colour, including a newly mutated colour. It is of course analogous to the ‘armpit self-inspection’ effect, and is plausible for the same reason.

Sargent’s (1969a) intuition differs from Kettlewell’s. He doubts the self-inspection theory, and thinks that the two morphs of
B. betularia
differ genetically in their background preference. He has no evidence about
B. betularia
itself, but has done some ingenious experiments on other species. For example, he took members of a dark species and of a light species, and painted the circum-ocular hairs in an attempt to ‘fool’ the moths into choosing a background that matched the painted hairs. They obstinately persisted in choosing a background that matched their genetically determined colour (Sargent 1968). Unfortunately, however, this interesting result was obtained with two different species, not with dark and light morphs of one species.

In another experiment which was done with a dimorphic species,
Phigalia titea
, Sargent (1969a) simply failed to get the result Kettlewell had with
B. betularia
. The
P. titea
individuals, whether the dark or the light morph, chose to sit on light backgrounds, presumably the appropriate background for the light ancestral form of the species. What is needed is for somebody to repeat Sargent’s key experiment of painting the parts of a moth’s body that it can see, but using a dimorphic species like
B. betularia
which is known to show morph-specific background choice. Kettlewell’s theory would predict that moths painted black will select black backgrounds, and moths painted light will select light backgrounds, regardless of whether they are genetically
carbonaria
or
typica
. A purely genetic theory would predict that
carbonaria
will choose dark backgrounds and
typica
light backgrounds, regardless of how they are painted.

If the latter theory turned out to be right, would this result give aid and comfort to the green-beard theory? A little, perhaps, since it would suggest that a morphological character and behavioural recognition of something resembling that morphological character can be, or can rapidly become, closely linked genetically. It must be remembered, here, that in the moth crypsis example there is no suggestion that we are dealing with an outlaw effect. If there are two genes, one controlling colour and the other background choice behaviour, both stand to gain from the presence of the appropriate other one, and neither of the two is in any sense an outlaw. If the two genes started out distantly linked, selection would favour closer and closer linkage. It is not clear that selection would similarly favour the close linkage of a ‘green-beard gene’ and a gene for green-beard recognition. It seems that the association between the effects would have to be there by luck right from the start.

The green-beard effect is all about one selfish gene looking after copies of itself in other individuals, regardless of, indeed in spite of, the probability that those individuals will share genes in general. The green-beard gene ‘spots’ copies of itself, and it thereby seems to work against the interests of the rest of the genome. It appears to be an outlaw in the sense that it makes individuals work and pay costs, for the benefit of other individuals who are not particularly likely to share genes other than the outlaw itself. This is the reason Alexander and Borgia (1978) call it an outlaw, and it is one of the reasons for their scepticism about the existence of green-beard genes.