The Extended Phenotype: The Long Reach of the Gene (Popular Science) (41 page)

Nobody has any trouble understanding the idea of genetic control of morphological differences. Nowadays few people have trouble understanding that there is, in principle, no difference between genetic control of morphology and genetic control of behaviour, and we are unlikely to be misled by unfortunate statements such as ‘Strictly speaking, it is the brain (rather than the behaviour) that is genetically inherited’ (Pugh in press). The point here is, of course, that if there is any sense in which the brain is inherited, behaviour may be inherited in exactly the same sense. If we object to calling behaviour inherited, as some do on tenable grounds, then we must, to be consistent, object to calling brains inherited too. And if we do decide to allow that both morphology and behaviour may be inherited, we cannot reasonably at the same time object to calling caddis house colour and spider web shape inherited. The extra step from behaviour to extended phenotype, in this case the stone house or the web, is as conceptually negligible as the step from morphology to behaviour.

From the viewpoint of this book an animal artefact, like any other phenotypic product whose variation is influenced by a gene, can be regarded as a phenotypic tool by which that gene could potentially lever itself into the next generation. A gene may so lever itself by adorning the tail of a male bird of paradise with a sexually attractive blue feather, or by causing a male bower bird to paint his bower with pigment crushed in his bill out of blue berries. The details may be different in the two cases but the effect, from the gene’s point of view, is the same. Genes that achieve sexually attractive phenotypic effects when compared with their alleles are favoured, and it is trivial whether those phenotypic effects are ‘conventional’ or ‘extended’. This is underlined by the interesting observation that bower bird species with especially splendid bowers tend to have relatively drab plumage, while those species with relatively bright plumage tend to build less elaborate and spectacular bowers (Gilliard 1963). It is as though some species have shifted
part of the burden of adaptation from bodily phenotype to extended phenotype.

So far the phenotypic effects we have been considering have extended only a few yards away from the initiating genes, but in principle there is no reason why the phenotypic levers of gene power should not reach out for miles. A beaver dam is built close to the lodge, but the effect of the dam may be to flood an area thousands of square metres in extent. As to the advantage of the pond from the beaver’s point of view, the best guess seems to be that it increases the distance the beaver can travel by water, which is safer than travelling by land, and easier for transporting wood. A beaver that lives by a stream quickly exhausts the supply of food trees lying along the stream bank within a reasonable distance. By building a dam across the stream the beaver creates a large shoreline which is available for safe and easy foraging without the beaver having to make long and difficult journeys overland. If this interpretation is right, the lake may be regarded as a huge extended phenotype, extending the foraging range of the beaver in a way which is somewhat analogous to the web of the spider. As in the case of the spider web, nobody has done a genetic study of beaver dams, but we really do not need to in order to convince ourselves of the rightness of regarding the dam, and the lake, as part of the phenotypic expression of beaver genes. It is enough that we accept that beaver dams must have evolved by Darwinian natural selection: this can only have come about if dams have varied under the control of genes (
Chapter 2
).

Just by talking about a few examples of animal artefacts, then, we have pushed the conceptual range of the gene’s phenotype out to many miles. But now we come up against a complication. A beaver dam is usually the work of more than one individual. Mated pairs routinely work together, and successive generations of a family may inherit responsibility for the upkeep and extension of a ‘traditional’ dam-complex comprising a staircase of half a dozen dams stepping downstream, and maybe several ‘canals’ as well. Now it was easy to argue that a caddis house, or a spider web, was the extended phenotype of the genes of the single individual that built it. But what are we to make of an artefact that is the joint production of a pair of animals or a family? Worse, consider the mound built by a colony of compass termites, a tombstone-shaped slab, one of a vista of similar monoliths all oriented precisely north–south, and rising to a height that dwarfs its builders as a mile-high skyscraper would dwarf a man (von Frisch 1975). It is built by perhaps a million termites, separated by time into cohorts, like medieval masons who could work a lifetime on one cathedral and never meet their colleagues that would complete it. A partisan of the individual as the unit of selection might pardonably ask exactly
whose
extended phenotype the termite mound is supposed to be.

If this consideration seems to complicate the idea of the extended
phenotype beyond all reason, I can only point out that exactly the same problem has always arisen with ‘conventional’ phenotypes. We are thoroughly accustomed to the idea that a given phenotypic entity, an organ say, or a behaviour pattern, is influenced by a large number of genes whose effects interact in additive or more complex ways. Human height at a given age is affected by genes at many loci, interacting with each other and with dietary and other environmental effects. The height of a termite mound at a given mound-age is, no doubt, also controlled by many environmental factors and many genes, adding to or modifying each others’ effects. It is incidental that in the case of the termite mound the
proximal
theatre of within-body gene effects happens to be distributed among the cells of a large number of worker bodies.

If we are going to worry about proximal effects, the genes influencing my height act in ways that are distributed among many separate cells. My body is full of genes, which happen to be identically distributed among my many somatic cells. Each gene exerts its effects at the cellular level, only a minority of genes expressing themselves in any one cell. The summed effects of all these effects on cells, together with similar effects from the environment, may be measured as my total height. Similarly, a termite mound is full of genes. These genes, too, are distributed among the nuclei of a large number of cells. It happens that the cells are not contained in quite such a compact single unit as the cells in my body, but even here the difference is not very great. Termites move around relative to each other more than human organs do, but it is not unknown for human cells to travel rapidly about the body in pursuance of their errands, for instance phagocytes hunting down and engulfing microscopic parasites. A more important difference (in the case of a termite mound, though not in the case of a coral reef built by a clone of individuals) is that the cells in the termite mound are gathered into genetically heterogeneous packages: each individual termite is a clone of cells but a different clone from all other individuals in the nest. This, however, is only a relative complication. Fundamentally what is going on is that genes, compared with their alleles, exert quantitative, mutually interacting, mutually modifying, effects on a shared phenotype, the mound. They do this proximally by controlling the chemistry of cells in worker bodies, and hence worker behaviour. The principle is the same, whether the cells happen to be organized into one large homogeneous clone, as in the human body, or into a heterogeneous collection of clones, as in the termite mound. I postpone until later the complicating point that a termite body itself is a ‘colony’, with a substantial fraction of its genetic replicators contained in symbiotic protozoa or bacteria.

What, then, would a genetics of termite mounds look like? Suppose we were to do a population survey of compass mounds in the Australian steppe, scoring a trait such as colour, basal length/width ratio, or some internal
structural feature—for termite mounds are like bodies with a complex ‘organ’ structure. How could we do a genetic study of such group-manufactured phenotypes? We need not hope to find normal Mendelian inheritance with simple dominance. An obvious complication, as already mentioned, is that the genotypes of the individuals working on any one mound are not identical. For most of the life of an average colony, however, all the workers are full siblings, the children of the primary royal pair of alates who founded the colony. Like their parents the workers are diploid. We may presume that the king’s two sets of genes and the queen’s two sets of genes are permuted throughout the several million worker bodies. The ‘genotype’ of the aggregate of workers may therefore be regarded, in a sense, as a single
tetraploid
genotype consisting of all the genes which the original founding pair contributed. It is not quite as simple as that, for various reasons, for instance secondary reproductives often arise in older colonies and these may take on the full reproductive role if one of the original royal pair dies. This means that the workers building the later parts of a mound may not be full siblings of those that began the task, but their nephews and nieces (probably inbred and rather uniform, incidentally—Hamilton 1972; Bartz 1979). These later reproductives still draw their genes from the ‘tetraploid’ set introduced by the original royal pair, but their progeny will permute a particular subset of those original genes. One of the things a ‘mound-geneticist’ might look out for, then, is a sudden change in details of mound-building after replacement of a primary reproductive by a secondary reproductive.

Ignoring the problem introduced by secondary reproductives, let us confine our hypothetical genetic study to younger colonies whose workers consist entirely of full siblings. Some characters in which mounds vary may turn out to be largely controlled at one locus, while others will be polygenically controlled at many loci. This is no different from ordinary diploid genetics, but our new quasi-tetraploid genetics now introduces some complications. Suppose the behavioural mechanism involved in choosing the colour of the mud used in building varies genetically. (Again, colour is chosen for continuity with earlier thought experiments, although again it would be more realistic to avoid a visual trait, since termites make little use of vision. If necessary, we may suppose the choice to be made chemically, mud colour being incidentally correlated with the chemical cues. This is instructive, for it again emphasizes the fact that our way of labelling a phenotypic trait is a matter of arbitrary convenience.) For simplicity, assume that mud choice is influenced by the diploid genotype of the individual worker doing the choosing, in a simple one locus Mendelian fashion with choice of dark mud dominant over choice of light mud. Then a mound built by a colony containing some dark-preferring workers and some light preferring workers will consist of a mixture of dark and light muds and will
presumably be intermediate in overall colour. Of course such simple genetic assumptions are highly improbable. They are equivalent to the simplifying assumptions we ordinarily make when explaining elementary conventional genetics, and I make them here to explain analogously the principles of how a science of ‘extended genetics’ might work.

Using these assumptions, then, we can write down the expected extended phenotypes, considering mud colour only, resulting from crosses between the various possible founding pair genotypes. For instance, all colonies founded by a heterozygous king and a heterozygous queen will contain dark-building and light-building workers in the ratio 3:1. The resulting extended phenotype will be a mound built of three parts dark mud and one part light mud, therefore nearly, but not completely, dark in colour. If choice of mud colour is influenced by polygenes at many loci, the ‘tetraploid genotype’ of the colony may be expected to influence the extended phenotype, perhaps in an additive way. The colony’s immense size will lead to its acting as a statistical averaging device, making the mound as a whole become the extended phenotypic expression of the genes of the royal pair, manifested via the behaviour of several million workers each containing a different diploid sample of those genes.

Mud colour was an easy character for us to choose, because mud itself blends in a simple additive manner: mix dark and light mud, and you get khaki mud. It was therefore easy for us to deduce the result of assuming that each worker goes its own way, choosing mud of its own preferred colour (or chemical associated with colour), as determined by its own diploid genotype. But what can we say about a characteristic of overall mound morphology, say basal width/length ratio? In itself, this is not a character that any single worker can determine. Each single worker must be obeying behavioural rules, the result of which, summed over thousands of individuals, is the production of a mound of regular shape and stated dimensions. Once again, the difficulty is one we have met before, in the embryonic development of an ordinary diploid multicellular body. Embryologists are still wrestling with problems of this kind, and very formidable they are. There do appear to be some close analogies with termite mound development. For instance, conventional embryologists frequently appeal to the concept of the chemical gradient, while in
Macrotermes
there is evidence that the shape and size of the royal cell is determined by a pheromonal gradient around the body of the queen (Bruinsma & Leuthold 1977). Each cell in a developing embryo behaves as if it ‘knows’ where it is in the body, and it grows to have a form and physiology appropriate to that part of the body (Wolpert 1970).

Sometimes the effects of a mutation are easy to interpret at the cellular level. For instance, a mutation that affects skin pigmentation has a rather obvious local effect on each skin cell. But other mutations affect complex characters in drastic ways. Well-known examples are the ‘homeotic’ mutants of
Drosophila
, such as the one that grows a complete and well-formed leg in the socket where an antenna ought to be. For a change in one single gene to wreak such a major, yet orderly, change in the phenotype, it must make its lesion rather high in a hierarchical chain of command. By analogy, if a single infantryman goes off his head he alone runs amok; but if a general loses his reason an entire army behaves crazily on a grand scale—invades an ally instead of an enemy, say—while each individual soldier in that army is obeying orders normally and sensibly, and his individual behaviour as he puts one foot in front of the other will be indistinguishable from that of a soldier in an army with a sane general.