The Extended Phenotype: The Long Reach of the Gene (Popular Science) (43 page)

The caddis larva rides inside the stone house that it built. It therefore seems appropriate to regard the house as the outer wall of the gene vehicle, the casing of the survival machine. It is even easier to regard the shell of a snail as part of the phenotypic expression of snail genes since, although the shell is inorganic and ‘dead’, its chemical substance was directly secreted by snail cells. Variations in, say, shell thickness would be called genetic if genes in snail cells affected shell thickness. Otherwise they would be called ‘environmental’. But there are reports of snails with trematode parasites having thicker shells than unparasitized snails (Cheng 1973). From the point of view of snail genetics, this aspect of shell variation is under ‘environmental’ control—the fluke is part of the environment of the snail—but from the point of view of fluke genetics it might well be under genetic control: it might, indeed, be an evolved adaptation of the fluke. It is admittedly also possible that the thickened shell is a pathological response of the snail, a dull byproduct of infection. But let me explore the possibility that it is a fluke adaptation, because it is an interesting idea to use in further discussion.

If we consider snail shell variation as, in part, phenotypic expression of snail genes, we might recognize an optimum shell thickness in the following sense. Selection presumably penalizes snail genes that make shells too thick, as well as those that make shells too thin. Thin shells provide inadequate protection. Genes for too-thin shells therefore endanger their germ-line copies, which are thus not favoured by natural selection. Shells that are too thick presumably protect their snails (and the enclosed germ-line genes for extra thickness) superlatively, but the extra cost of making a thick shell detracts from the snail’s success in some other way. In the economy of the body, resources that are consumed in making extra-thick shells, and in carrying the extra weight around, might better have been diverted into making, say, larger gonads. Continuing with the hypothetical example, therefore, genes for extra-thick shells will tend to induce in their bodies some compensating disadvantage such as relatively small gonads, and they will therefore not be passed on to the next generation so effectively. Even if there is, in fact, no trade-off between shell thickness and gonad size, there is bound to be some kind of analogous trade-off, and a compromise will be reached at an intermediate thickness. Genes that tend to make snail shells either too thick or too thin will not prosper in the snail gene pool.

But this whole argument presupposes that the only genes that have power over variation in shell thickness are snail genes. What if some of the causal factors that are, by definition, environmental from the snail’s point of view, turn out to be genetic from some other point of view, say that of the fluke? Suppose we adopt the suggestion made above that some fluke genes are capable, through an influence on snail physiology, of exerting an effect on snail shell thickness. If shell thickness influences the replication success of such fluke genes, natural selection is bound to work on their frequencies relative to their alleles in the fluke gene-pool. Changes in snail shell thickness may be regarded, then, at least in part, as potential adaptations for the benefit of fluke genes.

Now, the optimum shell thickness from the point of view of the fluke genes is hardly likely to be the same as the optimum from the point of view of snail genes. For instance, snail genes will be selected for their beneficial effects on snail reproduction as well as snail survival, but (except under special circumstances which we shall come on to) fluke genes may value snail survival but they will not value snail reproduction at all. In the inevitable trade-off between the demands of snail survival and snail reproduction, therefore, snail genes will be selected to produce an optimal compromise, while fluke genes will be selected to devalue snail reproduction to the advantage of snail survival, and hence to thicken the shell. A thickening of the shell in parasitized snails is, it will be remembered, the observed phenomenon with which we began.

It may be objected here that, although a fluke has no direct stake in the reproduction of its own snail host, it does have a stake in there being a new generation of snails at large. This is true, but we must be very careful before we use the fact to predict that selection would favour fluke adaptations to enhance snail reproduction. The question we have to ask is this. Given that the fluke gene-pool was dominated by genes that aided snail reproduction at the expense of snail survival, would selection favour a selfish fluke gene that sacrificed the reproduction of its particular snail host, even parasitically castrated the snail, in the interest of prolonging the life of that host, and hence of promoting its own survival and reproduction? Except under special circumstances the answer is surely yes; such a rare gene would invade the fluke gene-pool, since it could exploit the free supply of new snails encouraged by the public-spirited majority of the fluke population. In other words, favouring snail reproduction at the expense of snail survival would not be a fluke ESS. Fluke genes that manage to shift the snail’s investment of resources away from reproduction and into survival will tend to be favoured in the fluke gene-pool. It is entirely plausible, therefore, that the extra thickness of shells observed in parasitized snails is a fluke adaptation.

On this hypothesis, the shell phenotype is a shared phenotype, influenced by fluke genes as well as by snail genes, just as the beaver dam is a phenotype
shared by genes in more than one individual beaver. According to the hypothesis, there are two optimum thicknesses of snail shells: a relatively thick fluke optimum, and a somewhat thinner snail optimum. The observed thickness in parasitized snails will probably be somewhere between the two optima, since snail genes and fluke genes are both in a position to exert power, and they are exerting their power in opposite directions.

As for parasite-free snails, it might be expected that their shells would have the snail-optimal thickness, since there are no fluke genes to exert power. This is too simple, however. If the population at large has a high incidence of fluke infestation, the gene-pool will probably contain genes that tend to compensate for the thickening effect of fluke genes. This would lead to uninfected snails having over-compensating phenotypes, shells that are thinner even than the snail optimum. I therefore predict that shell thicknesses in fluke-free areas should be intermediate between those of infected snails and uninfected snails in fluke-infested areas. I do not know of any evidence bearing on this prediction, but it would be interesting to look. Note that this prediction does not depend on any
ad hoc
assumption about snails ‘winning’ or flukes ‘winning’. It assumes that both snail genes and fluke genes exert
some
power over the snail phenotype. The prediction will follow regardless of the quantitative details of that power.

Flukes live inside snail shells in a sense that is not too far removed from the sense in which snails live inside snail shells, and caddis larvae live inside their stone houses. Having accepted the idea that the form and colour of a caddis house might constitute phenotypic expression of caddis genes, it is not difficult to accept the idea of the form and colour of a snail shell being phenotypic expression of genes in a fluke inside the snail. If we could fancifully imagine a fluke gene and a snail gene intelligently discussing with a caddis gene the problems of making a hard outer wall for protection, I doubt if the conversation would make any reference to the fact that the fluke was a parasite while the caddis and the snail were not. The rival merits of secreting calcium carbonate, recommended by the fluke and the snail genes, versus picking up stones, preferred by the caddis gene, would be discussed. There might be some reference to the fact that a convenient and economical way of secreting calcium carbonate involves the use of a snail. But, from the gene’s-eye viewpoint, I suspect that the concept of parasitism would be treated as irrelevant. All three genes might regard themselves as parasitic, or alternatively as using comparable levers of power to influence their respective worlds so as to survive. The living cells of the snail would be regarded by the snail gene and the fluke gene as useful objects to be manipulated in the outside world, in exactly the same sense as the stones on the bottom of the stream would be regarded by the caddis gene.

By discussing inorganic snail
shells
, I have retained continuity with the caddis houses and other non-living artefacts of the previous chapter, thereby
pursuing my policy of sustaining credulity by extending the concept of the phenotype gradually by insensible degrees. But now it is time to grasp the living snail firmly by the horns. Flukes of the genus
Leucochloridium
invade the horns of snails where they can be seen through the skin, conspicuously pulsating. This tends to make birds, who are the next host in the life cycle of the fluke, bite off the tentacles mistaking them, Wickler (1968) suggests, for insects. What is interesting here is that the flukes seem also to manipulate the
behaviour
of the snails. Whether it is because the snail’s eyes are at the ends of the horns, or whether through some more indirect physiological route, the fluke manages to change the snail’s behaviour with respect to light. The normal negative phototaxis is replaced in infected snails by positive light-seeking. This carries them up to open sites where they are presumably more likely to be eaten by birds, and this benefits the fluke.

Once again, if this is to be regarded as a parasitic adaptation, and indeed it is widely so regarded (Wickler 1968; Holmes & Bethel 1972), we are forced to postulate the sometime existence of genes in the parasite gene-pool that influenced the behaviour of hosts, since all Darwinian adaptations evolved by the selection of genes. By definition such genes were genes ‘for’ snail behaviour, and the snail behaviour has to be regarded as part of the phenotypic expression of fluke genes.

The genes in one organism’s cells, then, can have extended phenotypic influence on the living body of another organism; in this case a parasite’s genes find phenotypic expression in the behaviour of its host. The parasitology literature is full of interesting examples which are now usually interpreted as adaptive manipulation of hosts by parasites (e.g. Holmes & Bethel 1972; Love 1980). It has not, to be sure, always been fashionable among parasitologists to make such interpretations explicit. For instance, an important review of parasitic castration in Crustacea (Reinhard 1956) is packed with detailed information and speculation on the precise physiological routes by which parasites castrate their hosts, but is almost devoid of discussion on why they might have been selected to do so, or whether, instead, castration is simply a fortuitous byproduct of parasitization. It may be an interesting indication of changing scientific fashions that a more recent review (Baudoin 1975) extensively considers the functional significance of parasitic castration from the individual parasite’s point of view. Baudoin concludes: ‘The main theses of this paper are (1) that parasitic castration can be viewed as a parasite’s adaptation and (2) that advantages derived from this adaptation are a result of reduction in host reproductive effort; which in turn gives rise to increased host survivorship, increased host growth and/or increased energy available to the parasite thereby increasing the parasite’s Darwinian fitness.’ This is, of course, very much the argument I have just followed in discussing parasite-induced thickening of snail shells. Again, a belief that parasitic castration is a parasite adaptation logically
implies that there must be, or at least must have been, parasite genes ‘for’ changes in host physiology. The symptoms of parasitic castration, sex-change, increased size, or whatever they may be, are properly regarded as extended phenotypic manifestations of parasite genes.

The alternative to Baudoin’s interpretation is that changes in host physiology and behaviour are not parasite adaptations, but simply dull pathological byproducts of infection. Consider the parasitic barnacle (though in its adult stage it looks more like a fungus)
Sacculina
. It might be said that
Sacculina
does not directly benefit from the castration of its crab host, but simply sucks nutriment from all through the host’s body, and as a side-effect of its devouring the tissues of the gonads the crab shows the symptoms of castration. In support of the adaptation hypothesis, however, Baudoin points to those cases in which parasites achieve the castration by synthesis of host hormones, surely a specific adaptation rather than a boring byproduct. Even in those cases where the castration is initially caused as a byproduct of the devouring of gonadal tissue, my suspicion is that selection would subsequently act on parasites to modify the details of their physiological effects on hosts, modify them in a way favourable to the parasite’s well-being.
Sacculina
presumably has some options over which parts of the crab’s body its root system invades first. Natural selection is surely likely to favour genes in
Sacculina
that cause it to invade gonadal tissue before invading vital organs on which the crab’s survival depends. Applying this kind of argument at a more detailed level, since gonadal destruction has multiple and complex effects on crab physiology, anatomy and behaviour, it is entirely reasonable to guess that selection would act on parasites to fine-tune their castration technique so as to increase their benefit from the initially fortuitous consequences of castration. I believe many modern parasitologists would agree with this feeling (P. O. Lawrence, personal communication). All that I am adding, then, is the logical point that the common belief that parasitic castration is an adaptation implies that the modified host phenotype is part of the extended phenotype of parasite genes.

Parasites often stunt the growth of their hosts, and it is easy to see this as a boring byproduct of infection. More interest therefore attaches to those rarer cases in which parasites enhance host growth, and I have already mentioned the case of the thickened snail shells. Cheng (1973, p. 22) begins his account of such cases with a revealing sentence: ‘Although one generally considers parasites to be detrimental to their hosts and cause the loss of energy and poor health, instances are known where the occurrence of parasites actually induces enhanced growth of the host.’ But Cheng is here sounding like a medical doctor rather than like a Darwinian biologist. If ‘detriment’ is defined in terms of reproductive success rather than survival and ‘health’, it is probable that growth-enhancement is indeed detrimental to the host, for the reasons given in my discussion of snail shells. Natural selection has
presumably favoured an optimal host size, and if a parasite causes the host to deviate from this size
in either direction
it is probably harming the host’s reproductive success, even if it is at the same time promoting host survival. All the examples of growth-enhancement given by Cheng can be easily understood as parasite-induced switches of resources away from investment in host reproduction, which is of no interest to the parasite, to the growth and survival of the host’s own body, which is of great interest to the parasite (again we must beware of the group-selectionist plea that the existence of a new generation of hosts is of importance to the parasite
species
).