The Extended Phenotype: The Long Reach of the Gene (Popular Science) (42 page)

Presumably an individual termite working on a little corner of a big mound is in a similar position to a cell in a developing embryo, or a single soldier tirelessly obeying orders whose purpose in the larger scheme of things he does not understand. Nowhere in the single termite’s nervous system is there anything remotely equivalent to a complete image of what the finished mound will look like (Wilson 1971, p. 228). Each worker is equipped with a small toolkit of behavioural rules, and he/she is probably stimulated to choose an item of behaviour by local stimuli emanating from the work already accomplished, no matter whether he/she or other workers accomplished it—stimuli emanating from the present state of the nest in the worker’s immediate vicinity (‘stigmergie’, Grassé 1959). For my purposes it doesn’t matter exactly what the behavioural rules are, but they would be something like: ‘If you come upon a heap of mud with a certain pheromone on it, put another dollop of mud on the top.’ The important point about such rules is that they have a purely local effect. The grand design of the whole mound emerges only as the summed consequences of thousands of obeyings of micro-rules (Hansell 1984). Particular interest attaches to the local rules that are responsible for determining global properties such as the base length of the compass mound. How do the individual workers on the ground ‘know’ that they have reached the boundary of the ground plan? Perhaps in something like the same way as the cells at the boundary of a liver ‘know’ that they are not in the middle of the liver. In any case, whatever the local behavioural rules may be that determine the overall shape and size of a termite mound, they are presumably subject to genetic variation in the population at large. It is entirely plausible, indeed almost inevitable, that both the shape and size of compass termite mounds have evolved by natural selection, just like any feature of bodily morphology. This can only have come about through the selection of mutations acting at the local level on the building behaviour of individual worker termites.

Now our special problem arises, which would not arise in the ordinary embryogenesis of a multicellular body, nor in the example of mixing light and dark muds. Unlike the cells of a multicellular body, the workers are not
genetically identical. In the example of the dark and light mud, it was easy to suppose that a genetically heterogeneous work-force would simply construct a mound of mixed mud. But a work-force which was genetically heterogeneous with respect to one of the behavioural rules that affected overall mound shape might produce curious results. By analogy with our simple Mendelian model of mud selection, a colony might contain workers favouring two different rules for determining the boundary of the mound, say in the ratio three to one. It is pleasing to imagine that such a bimodal colony might produce a mound with a strange double wall and a moat between! More probably, the rules obeyed by individuals would include provision for the minority to allow themselves to be overruled by majority decisions, so that only one clean-cut wall would emerge. This could work in a similar way to the ‘democratic’ choice of a new nest site in honeybee swarms, observed by Lindauer (1961).

Scout bees leave the swarm hanging in a tree, and prospect for suitable new permanent sites such as hollow trees. Each scout returns and dances on the surface of the swarm, using the well-known von Frisch code to indicate the direction and distance of the prospective site that she has just investigated. The ‘vigour’ of the dance indicates the individual scout’s assessment of the virtues of the site. New bees are recruited to go out and examine it for themselves, and if they ‘approve’ they too dance ‘in its favour’ on returning. After some hours, then, the scouts have formed themselves into a few ‘parties’, each one ‘advocating’ a different nest site. Finally, minority ‘opinions’ become even smaller minorities, as allegiances are transferred to majority dances. When an overwhelming majority has been achieved for one site, the whole swarm takes off and flies there to set up home.

Lindauer observed this procedure for nineteen different swarms, and in only two of these cases was a consensus not soon reached. I quote his account of one of these:

In the first case two groups of messengers had got into competition; one group announced a nesting place to the northwest, the other to the northeast. Neither of the two wished to yield. The swarm then finally flew off and I could scarcely believe my eyes—it sought to divide itself. The one half wanted to fly to the northwest, the other to the northeast. Apparently each group of scouting bees wanted to abduct the swarm to the nesting place of its own choice. But that was naturally not possible, for one group was always without the queen, and there resulted a remarkable tug of war in the air, once 100 meters to the northwest, then again 150 meters to the northeast, until finally after half an hour the swarm gathered together at the old location. Immediately both groups began again with their soliciting dances,
and it was not until the next day that the northeast group finally yielded; they ended their dance and thus an agreement was reached on the nesting place in the northwest [Lindauer 1961, p. 43].

There is no suggestion here that the two subgroups of bees were genetically different, though they may have been. What matters for the point I am making is that each individual follows local behavioural rules, the combined effect of which normally gives rise to coordinated swarm behaviour. These evidently include rules for resolving ‘disputes’ in favour of the majority. Disagreements over the preferred location for the outer wall of a termite mound might be just as serious for colony survival as disagreement over nesting sites among Lindauer’s bees (colony survival matters, because of its effects on the survival of the genes causing individuals to resolve disputes). As a working hypothesis we might expect that disputes resulting from genetic heterogeneity in termites would be resolved by similar rules. In this way the extended phenotype could take up a discrete and regular shape, despite being built by genetically heterogeneous workers.

The analysis of artefacts given in this chapter seems, at first sight, vulnerable to
reductio ad absurdum
. Isn’t there a sense, it may be asked, in which every effect that an animal has upon the world is an extended phenotype? What about the footprints left in the mud by an oystercatcher, the paths worn through the grass by sheep, the luxuriant tussock that marks the site of a last year’s cowpat? A pigeon’s nest is an artefact without a doubt, but in gathering the sticks the bird also changes the appearance of the ground where they had lain. If the nest is called extended phenotype, why shouldn’t we so call the bare patch of ground where the sticks used to lie?

To answer this we must recall the fundamental reason why we are interested in the phenotypic expression of genes in the first place. Of all the many possible reasons, the one which concerns us in this book is as follows. We are fundamentally interested in natural selection, therefore in the differential survival of replicating entities such as genes. Genes are favoured or disfavoured relative to their alleles as a consequence of their phenotypic effects upon the world. Some of these phenotypic effects may be incidental consequences of others, and have no bearing on the survival chances, one way or the other, of the genes concerned. A genetic mutation that changes the shape of an oystercatcher’s foot will doubtless thereby influence the oystercatcher’s success in propagating it. It may, for instance, slightly reduce the bird’s risk of sinking into mud, while at the same time it slightly slows him down when he is running on firm ground. Such effects are likely to be of direct relevance to natural selection. But the mutation will also have an effect on the shape of the footprints left behind in the mud—arguably an extended phenotypic effect. If, as is perfectly likely, this has no influence on the success of the gene concerned (Williams 1966, pp. 12–13), it is of no
interest to the student of natural selection, and there is no point in bothering to discuss it under the heading of the extended phenotype, though it would be formally correct to do so. If, on the other hand, the changed footprint did influence survival of the oystercatcher, say by making it harder for predators to track the bird, I would want to regard it as part of the extended phenotype of the gene. Phenotypic effects of genes, whether at the level of intracellular biochemistry, gross bodily morphology or extended phenotype, are potentially devices by which genes lever themselves into the next generation, or barriers to their doing so. Incidental side-effects are not always effective as tools or barriers, and we do not bother to regard them as phenotypic expressions of genes, either at the conventional or the extended phenotype level.

It is unfortunate that this chapter has had to be rather hypothetical. There have been only a few studies of the genetics of building behaviour in any animal (e.g. Dilger 1962), but there is no reason to think that ‘artefact genetics’ will be any different, in principle, from behaviour genetics generally (Hansell 1984). The idea of the extended phenotype is still sufficiently unfamiliar that it might not immediately occur to a geneticist to study termite mounds as a phenotype, even if it were practically easy to do so—and it wouldn’t be easy. Yet we must acknowledge at least the theoretical validity of such a branch of genetics if we are to countenance the Darwinian evolution of beaver dams and termite mounds. And who can doubt that, if termite mounds fossilized plentifully, we would see graded evolutionary series with trends as smooth (or as punctuated!) as any that we find in vertebrate skeletal palaeontology (Schmidt 1955; Hansell 1984)?

Permit me one further speculation to lead us into the next chapter. I have spoken as if the genes inside a termite mound were all enclosed in the nuclei of cells of termite bodies. The ‘embryological’ forces bearing on the extended phenotype have been assumed to originate from the genes of individual termites. Yet the chapter on arms races and manipulation should have alerted us to another way of looking at it. If all the DNA could be distilled out of a termite mound, perhaps as much as one-quarter of it would not have originated from termite nuclei at all. Some such proportion of the body weight of each individual termite is typically made up of symbiotic cellulose-digesting microorganisms in the gut—flagellates or bacteria. The symbionts are obligately dependent on the termites, and the termites on them. The proximal phenotypic power of the symbiont genes is exerted via protein synthesis in symbiont cytoplasm. But just as termite genes reach out beyond the cells that enclose them and manipulate the development of whole termite bodies and hence of the mound, is it not almost inevitable that the symbiont genes will have been selected to exert phenotypic power on their surroundings? And will this not include exerting phenotypic power on termite cells and hence bodies, on termite behaviour and even termite
mounds? Along these lines, could the evolution of eusociality in the Isoptera be explained as an adaptation of the microscopic symbionts rather than of the termites themselves?

This chapter has explored the idea of the extended phenotype, first of genes in a single individual, then of genes from different but closely related individuals, members of a kin-group. The logic of the argument now seems to compel us to contemplate the possibility of an extended phenotype’s being jointly manipulated, not necessarily cooperatively, by genes from distantly related individuals, individuals of different species, even different kingdoms. This is the direction in which our next outward step must take us.

Let us briefly take stock of where we have reached in our outward march. The phenotypic expression of a gene can extend outside the cell in which the genes exert their immediate biochemical influence, to affect gross features of a whole multicellular body. This is commonplace, and we are conventionally used to the idea of a gene’s phenotypic expression being extended this far.

In the previous chapter we took the small further step of extending the phenotype to artefacts, built by individual behaviour which is subject to genetic variation, for instance caddis houses. Next we saw that an extended phenotype can be built under the joint influence of genes in more than one individual body. Beaver dams and termite mounds are collectively built by the behavioural efforts of more than one individual. A genetic mutation in one individual beaver could show itself in phenotypic change in the shared artefact. If the phenotypic change in the artefact had an influence on the success of replication of the new gene, natural selection would act, positively or negatively, to change the probability of similar artefacts existing in the future. The gene’s extended phenotypic effect, say an increase in the height of the dam, affects its chances of survival in precisely the same sense as in the case of a gene with a normal phenotypic effect, such as an increase in the length of the tail. The fact that the dam is the shared product of the building behaviour of several beavers does not alter the principle: genes that tend to make beavers build high dams will themselves, on average, tend to reap the benefits (or costs) of high dams, even though every dam may be jointly built by several beavers. If two beavers working on the same dam have different genes for dam height, the resulting extended phenotype will reflect the interaction between the genes, in the same way as bodies reflect gene interactions. There could be extended genetic analogues of epistasis, of modifier genes, even of dominance and recessiveness.

Finally, at the end of the chapter, we saw that genes ‘sharing’ a given extended phenotypic trait might come from different species, even different
phyla and different kingdoms. This chapter will develop two further ideas. One is that phenotypes that extend outside the body do not have to be inanimate artefacts: they can themselves be built of living tissue. The other idea is that wherever there are ‘shared’ genetic influences on an extended phenotype, the shared influences may be in conflict with each other rather than cooperative. The relationships we shall be concerned with are those of parasites and their hosts. I shall show that it is logically sensible to regard parasite genes as having phenotypic expression in host bodies and behaviour.