The Extended Phenotype: The Long Reach of the Gene (Popular Science) (47 page)

Whichever link in the chain a geneticist chooses to regard as the ‘phenotype’ of interest, he knows that the decision was an arbitrary one. He might have chosen an earlier stage, and he might have chosen a later one. So, a student of the genetics of the Bruce Effect could assay male pheromones biochemically in order to detect the variation upon which to base his genetic study. Or he could look further back in the chain, ultimately to the immediate polypeptide products of the genes concerned. Or he could look later in the chain.

What is the next later link in the chain after the male pheromone? It is outside the male body. The chain of causation extends across a gap into the female body. It goes through a number of stages in the female body, and once again our geneticist does not have to bother himself with the details. He
chooses, for convenience, to end his conceptual chain at the point where the gene causes pregnancy blockage in females. That is the phenotypic gene-product which he finds most easy to assay, and it is the phenotype which is of direct interest to him as a student of adaptation in nature. Abortion in female mice, according to this hypothesis, is a phenotypic effect of a gene in male mice.

How, then, would the ‘extended geneticist’ visualize the evolution of the Bruce Effect? The mutant gene which, when present in males, has the phenotypic effect in female bodies of causing them to abort, is favoured by natural selection over its alleles. It is favoured because it tends to be carried in the bodies of the offspring which the female bears after blocking her previous pregnancy. But, following the habit of
Chapter 4
, we now guess that females would be unlikely to submit to such manipulation without resistance, and that a kind of arms race might develop. In the language of individual advantage, selection would favour mutant females that resisted the pheromonal manipulation of the males. How would the ‘extended geneticist’ think about this resistance? By invoking the concept of the modifier gene.

Once again, we turn first to conventional within-body genetics to remind ourselves of a principle, then carry that principle over into the realm of extended genetics. In within-body genetics we are quite used to the idea of more than one gene affecting variation in any given phenotypic character. Sometimes it is convenient to designate one locus as having the ‘major’ effect on the character, the others having ‘modifying’ effects. At other times no one locus predominates over the others sufficiently to be called major. All the genes may be thought of as modifying the effects of each other. In the chapter on ‘Outlaws and Modifiers’, we saw that two loci bearing on the same phenotypic character may be subject to conflicting selection pressures. The end result may be stalemate, compromise, or outright victory for one side or the other. The point is that conventional within-body genetics is already accustomed to thinking of the natural selection of genes at different loci bearing upon the same phenotypic character but in opposite directions.

Apply the lesson in the extended genetics domain. The phenotypic trait of interest is abortion in female mice. The genes bearing upon it no doubt include a set of genes in the female’s own body, and also another set of genes in the male’s body. In the case of the male genes the links in the chain of causation include pheromonal action at a distance, and this may make the influence of the male genes seem very indirect. But the causal links in the case of the female genes are likely to be nearly as indirect, albeit they are confined inside her body. Probably they make use of various chemical secretions flowing in her bloodstream, whereas the male genes make use, in addition, of chemical secretions flowing in the air. The point is that both sets of genes, by long and indirect causal links, bear upon the same phenotypic
character, abortion in the female, and either set of genes may be regarded as modifiers of the other set, just as some genes within each set may be regarded as modifiers of others within the same set.

Male genes influence the female phenotype. Female genes influence the female phenotype, and also modify the influence of male genes. For all we know, female genes influence the male phenotype in counter-manipulation, in which case we expect the selection of modifiers among genes in males.

This whole story could have been told in the language of
Chapter 4
, the language of individual manipulation. The language of extended genetics is not demonstrably more correct. It is a different way of saying the same thing. The Necker Cube has flipped. Readers must decide for themselves whether they like the new view better than the old. I suggest that the way the extended geneticist tells the story of the Bruce Effect is more elegant and parsimonious than the way the conventional geneticist would have told it. Both geneticists potentially have to contend with a formidably long and complex chain of causation, leading from gene to phenotype. Both admit that their choice of which link in the chain to designate as the phenotypic character of interest—earlier links being consigned to the embryologist—is arbitrary. The conventional geneticist makes the further arbitrary decision to cut off all chains at the point where they reach the outer wall of the body.

Genes affect proteins, and proteins affect X which affects Y which affects Z which … affects the phenotypic character of interest. But the conventional geneticist defines ‘phenotypic effect’ in such a way that X, Y and Z must all be confined inside one individual body wall. The extended geneticist recognizes that this cut-off is arbitrary, and he is quite happy to allow his X, Y and Z to leap the gap between one individual body and another. The conventional geneticist takes in his stride the bridging of gaps between cells within bodies. Human red blood cells, for instance, have no nuclei, and must express the phenotypes of genes in other cells. So why should we not, when the occasion warrants it, conceive of the bridging of gaps between cells in different bodies? And when will the occasion warrant it? Whenever we find it convenient, and this will tend to be in any of those cases where, in conventional language, one organism appears to be manipulating another. The extended geneticist would, in fact, be quite happy to rewrite the whole of
Chapter 4
, fixing his gaze on the new face of the Necker Cube. I shall spare the reader any such rewriting, although it would be an interesting task to undertake. I shall not pile example on example of genetic action at a distance, but instead will discuss the concept, and problems that it raises, more generally.

In the chapter on arms races and manipulation I said that an organism’s limbs might be adapted to work for the genes of another organism, and I added that this idea could not be made fully meaningful until later in the book. I meant that it could be made meaningful in terms of genetic action at
a distance. So, what does it mean to say that a female’s muscles work for a male’s genes, or that a parent’s limbs work for its offspring’s genes, or that a reed warbler’s limbs work for a cuckoo’s genes? It will be remembered that the ‘central theorem’ of the selfish organism claims that an animal’s behaviour tends to maximize its own (inclusive) fitness. We saw that to talk of an individual behaving so as to maximize its inclusive fitness is equivalent to talking of the gene or genes ‘for’ that behaviour pattern maximizing their survival. We have now also seen that, in precisely the same sense as it is ever possible to talk of a gene ‘for’ a behaviour pattern, it is possible to talk of a gene, in one organism, ‘for’ a behaviour pattern (or other phenotypic characteristic) in another organism. Putting these three things together we arrive at our own ‘central theorem’ of the extended phenotype:
An animal’s behaviour tends to maximize the survival of the genes ‘for’ that behaviour, whether or not those genes happen to be in the body of the particular animal performing it
.

And how far afield can the phenotype extend? Is there any limit to action at a distance, a sharp cut-off, an inverse square law? The farthest action at a distance I can think of is a matter of several miles, the distance separating the extreme margins of a beaver lake from the genes for whose survival it is an adaptation. If beaver lakes could fossilize, we would presumably see a trend towards increased lake size if we arranged the fossils in chronological order. The increase in size was doubtless an adaptation produced by natural selection, in which case we have to infer that the evolutionary trend came about by allele replacement. In the terms of the extended phenotype, alleles for larger lakes replaced alleles for smaller lakes. In the same terms, beavers can be said to carry within themselves genes whose phenotypic expression extends many miles away from the genes themselves.

Why not hundreds of miles, thousands of miles? Could an ectoparasite which stayed behind in England inject a swallow with a drug which affected that swallow’s behaviour on its arrival in Africa, and could the consequence in Africa be usefully regarded as the phenotypic expression of parasite genes in England? The logic of the extended phenotype might seem to favour the idea, but I think in practice it is unlikely, at least if we are talking about phenotypic expression as
adaptation
. I see a crucial practical difference from the case of the beaver dam. A gene in a beaver which, when compared with its alleles, causes a larger lake to come into existence, can directly benefit itself by means of its lake. Alleles causing smaller lakes are less likely to survive, as a direct consequence of their smaller phenotypes. It is, however, hard to see how a gene in an English ectoparasite could benefit itself, at the expense of its alleles in England, as a direct result of its African phenotypic expression. Africa is probably too far away for the consequences of the gene’s action to feed back and affect the welfare of the gene itself.

By the same token, beyond a certain size of beaver lakes, it would become
hard to regard further increases in size as adaptations. The reason is that, beyond a certain size, other beavers than the builders of the dam are just as likely to benefit from each increase in size as the dam-builders themselves. A big lake benefits all the beavers in the area, whether they created it or whether they just found it and exploited it. Similarly, even if a gene in an English animal could exert some phenotypic effect on Africa which directly benefited the survival of the gene’s ‘own’ animal, other English animals of the same kind would almost certainly benefit just as much. We must not forget that natural selection is all about
relative
success.

It is admittedly possible to speak of a gene as having a particular phenotypic expression, even when its own survival is not influenced by that phenotypic expression. In this sense, then, a gene in England might indeed have phenotypic expression in a remote continent where its consequences do not feed back upon its own success in the English gene-pool. But I have already argued that in the world of the extended phenotype this is not a profitable way of speaking. I used the example of footprints in mud as phenotypic expression of genes for foot shape, and I gave my intention of using extended phenotype language only when the character concerned might conceivably influence, positively or negatively, the replication success of the gene or genes concerned.

It is not plausible, but it helps to make the point if I construct a thought experiment in which it would indeed be useful to speak of a gene as having phenotypic expression extending to another continent. Swallows return, each year, to exactly the same nest. It follows that an ectoparasite, waiting dormant in a swallow’s nest in England, can expect to see the very same swallow both before and after the swallow’s journey to Africa. If the parasite could engineer some change in the swallow’s behaviour in Africa, it might indeed reap the consequences on the swallow’s return to England. Suppose, for instance, that the parasite needs a rare trace element which is not found in England, but which occurs in the fat of a particular African fly. Swallows normally have no preference for this fly, but the parasite, by injecting a drug into the swallow before it leaves for Africa, so changes its dietary preferences as to increase the likelihood of its eating specimens of this fly. When the swallow returns to England, its body contains enough of the trace element to benefit the individual parasite (or its children) waiting in the original nest, benefit them at the expense of rivals within the parasite species. Only in circumstances such as these would I wish to speak of a gene in one continent as having phenotypic expression in another continent.

There is a risk, which I had better forestall, that such talk of adaptation on a global scale may call to the reader’s mind the fashionable image of the ecological ‘web’, of which the most extreme manifestation is the ‘Gaia’ hypothesis of Lovelock (1979). My web of interlocking extended phenotypic influences bears a superficial resemblance to the webs of mutual dependence
and symbiosis that bulk so largely in the pop-ecology literature (e.g.
The Ecologist
) and in Lovelock’s book. The comparison could hardly be more misleading. Since Lovelock’s Gaia hypothesis has been enthusiastically espoused by no less a scientist then Margulis (1981), and extravagantly praised by Mellanby (1979) as the work of a genius, it cannot be ignored, and I must digress in order categorically to disclaim any connection with the extended phenotype.

Lovelock rightly regards homeostatic self-regulation as one of the characteristic activities of living organisms, and this leads him to the daring hypothesis that the whole Earth is equivalent to a single living organism. Whereas Thomas’s (1974) likening of the world to a living cell can be accepted as a throwaway poetic line, Lovelock clearly takes his Earth/organism comparison seriously enough to devote a whole book to it. He really means it. His explanations of the nature of the atmosphere are representative of his ideas. The Earth has much more oxygen than is typical of comparable planets. It has long been widely suggested that green plants are probably almost entirely responsible for this high oxygen content. Most people would regard oxygen production as a byproduct of plant activity, and a fortunate one for those of us who need to breathe oxygen (presumably, too, we have been selected to breathe oxygen partly because there is so much of it about). Lovelock goes further, and regards oxygen production by plants as an adaptation on the part of the Earth/organism or ‘Gaia’ (named after the Greek Earth goddess): plants produce oxygen
because
it benefits life as a whole.