The Extended Phenotype: The Long Reach of the Gene (Popular Science) (40 page)

The reader may have been bewildered and irritated at my drawn out list of five or more separate meanings of fitness. I have found this a painful chapter to write, and I am aware that it will not have been easy to read. It may be the last resort of a poor writer to blame his subject matter, but I really do believe it is the concept of fitness itself which is responsible for the agony in this case. The population geneticists’ fitness[2] aside, the concept of fitness as applied to individual organisms has become forced and contrived. Before Hamilton’s revolution, our world was peopled by individual organisms working single-mindedly to keep themselves alive and to have children. In those days it was natural to measure success in this undertaking at the level of the individual organism. Hamilton changed all that but unfortunately, instead of following his ideas through to their logical conclusion and sweeping the individual organism from its pedestal as notional agent of maximization, he exerted his genius in devising a means of rescuing the individual. He could have persisted in saying: gene survival is what matters; let us examine what a gene would have to do in order to propagate copies of itself. Instead he, in effect, said: gene survival is what matters; what is the minimum change we have to make to our old view of what individuals must do, in order that we may cling on to our idea of the individual as the unit of action? The result—inclusive fitness—was technically correct, but complicated and easy to misunderstand. I shall avoid mentioning fitness again in this book, which I trust will make for easier reading. The next three chapters develop the theory of the extended phenotype itself.

What do we really mean by the phenotypic effect of a gene? A smattering of molecular biology may suggest one kind of answer. Each gene codes for the synthesis of one protein chain. In a proximal sense that protein is its phenotypic effect. More distal effects like eye colour or behaviour are, in their turn, effects of the protein functioning as an enzyme. Such a simple account does not, however, bear much searching analysis. The ‘effect’ of any would-be cause can be given meaning only in terms of a comparison, even if only an implied comparison, with at least one alternative cause. It is strictly incomplete to speak of blue eyes as ‘the effect’ of a given gene
G1
. If we say such a thing, we really imply the potential existence of at least one alternative allele, call it
G2
, and at least one alternative phenotype, P2, in this case, say, brown eyes. Implicitly we are making a statement about a relation between a pair of genes {
G1, G2
} and a pair of distinguishable phenotypes {P1, P2}, in an environment which either is constant or varies in a non-systematic way so that its contribution randomizes out. ‘Environment’, in that last clause, is taken to include all the genes at other loci that must be present in order for P1 or P2 to be expressed. Our statement is that there is a statistical tendency for individuals with
G1
to be more likely than individuals with
G2
to show P1 (rather than P2). Of course there is no need to demand that P1 should
always
be associated with
G1
, nor that
G1
should always lead to P1: in the real world outside logic textbooks, the simple concepts of ‘necessary’ and ‘sufficient’ must usually be replaced by statistical equivalents.

Such an insistence that phenotypes are not caused by genes, but only phenotypic differences caused by gene differences (Jensen 1961; Hinde 1975) may seem to weaken the concept of genetic determination to the point where it ceases to be interesting. This is far from the case, at least if the subject of our interest is natural selection, because natural selection too is concerned with differences (
Chapter 2
). Natural selection is the process by which some alleles out-propagate their alternatives, and the instruments by which they
achieve this are their phenotypic effects. It follows that phenotypic effects can always be thought of as
relative
to alternative phenotypic effects.

It is customary to speak as if differences always mean differences between individual bodies or other discrete ‘vehicles’. The purpose of the next three chapters is to show that we can emancipate the concept of the phenotypic difference from that of the discrete vehicle altogether, and this is the meaning of the title ‘extended phenotype’. I shall show that the ordinary logic of genetic terminology leads inevitably to the conclusion that genes can be said to have
extended
phenotypic effects, effects which need not be expressed at the level of any particular vehicle. Following an earlier paper (Dawkins 1978a) I shall take a step-by-step approach to the extended phenotype, beginning with conventional examples of ‘ordinary’ phenotypic effects and gradually extending the concept of the phenotype outwards so that the continuity is easy to accept. The idea of the genetic determination of animal artefacts is a didactically useful intermediate example, and this will be the main topic of this chapter.

But first, consider a gene
A
whose immediate molecular effect is the synthesis of a black protein which directly colours the skin of an animal black. Then the gene’s only proximal effect, in the molecular biologist’s simple sense, is the synthesis of this one black protein. But is
A
a gene ‘for being black’? The point I want to make is that, as a matter of definition, that depends on how the population varies. Assume that
A
has an allele
A′
, which fails to synthesize the black pigment, so that individuals homozygous for
A′
tend to be white. In this case
A
is truly a gene ‘for’ being black, in the sense in which I wish to use the phrase. But it may alternatively be that all the variation in skin colour that actually occurs in the population is due to variation at a quite different locus,
B. B
’s immediate biochemical effect is the synthesis of a protein which is not a black pigment, but which acts as an enzyme, one of whose indirect effects (in comparison with its allele
B′
), at some distant remove, is the facilitation of the synthesis by
A
of the black pigment in skin cells.

To be sure,
A
, the gene whose protein product is the black pigment, is necessary in order for an individual to be black: so are thousands of other genes, if only because they are necessary to make the individual exist at all. But I shall not call
A
a gene for blackness unless some of the variation in the population is due to lack of
A
. If all individuals, without fail, have
A
, and the only reason individuals are not black is that they have
B′
rather than
B
, we shall say that
B
, but not
A
, is a gene for blackness. If there is variation at both loci affecting blackness, we shall refer to both
A
and
B
as genes for blackness. The point that is relevant here is that both
A
and
B
are potentially entitled to be called genes for blackness, depending on the alternatives that exist in the population. The fact that the causal chain linking
A
to the production of the black pigment molecule is short, while that for
B
is long
and tortuous, is irrelevant. Most gene effects seen by whole animal biologists, and all those seen by ethologists, are long and tortuous.

A geneticist colleague has argued that there are virtually no behaviour-genetic traits, because all those so-far discovered have turned out to be ‘byproducts’ of more fundamental morphological or physiological effects. But what on earth does he think
any
genetic trait is, morphological, physiological or behavioural, if not a ‘byproduct’ of something more fundamental? If we think the matter through we find that all genetic effects are ‘byproducts’ except protein molecules.

Returning to the black skin example, it is even possible that the chain of causation linking a gene such as
B
to its black-skinned phenotype might involve a behavioural link. Suppose that
A
can synthesize black pigment only in the presence of sunlight, and suppose that
B
works by making individuals seek sunlight, in comparison with
B′
which makes them seek shade.
B
individuals will then tend to be blacker than
B′
individuals, because they spend more time in the sun.
B
is still, by existing terminological convention, a gene ‘for blackness’, no less than it would be if its causal chain involved internal biochemistry only, rather than an ‘external’ behavioural loop. Indeed, a geneticist in the pure sense of the word need not care about the detailed pathway from gene to phenotypic effect. Strictly speaking, a geneticist who concerns himself with these interesting matters is temporarily wearing the hat of an embryologist. The pure geneticist is concerned with end products, and in particular with differences between alleles in their effects on end products. Natural selection’s concerns are precisely the same, for natural selection ‘works on outcomes’ (Lehrman 1970). The interim conclusion is that we are already accustomed to phenotypic effects being attached to their genes by long and devious chains of causal connection, therefore further extensions of the concept of phenotype should not overstretch our credulity. This chapter takes the first step towards such further extension, by looking at animal artefacts as examples of the phenotypic expression of genes.

The fascinating subject of animal artefacts is reviewed by Hansell (1984). He shows that artefacts provide useful case studies for several principles of general ethological importance. This chapter uses the example of artefacts in the service of explaining another principle, that of the extended phenotype. Consider a hypothetical species of caddis-fly whose larvae build houses out of stones which they select from those available on the bottom of the stream. We might observe that the population contains two rather distinct colours of house, dark and light. By breeding experiments we establish that the characters ‘dark house’ and ‘light house’ breed true in some simple Mendelian fashion, say with dark house dominant to light house. In principle it ought to be possible to discover, by analysing recombination data, where the genes for house colour sit on the
chromosomes. This is, of course, hypothetical. I do not know of any genetic work on caddis houses, and it would be difficult to do because adults are difficult to breed in captivity (M. H. Hansell, personal communication). But my point is that, if the practical difficulties could be overcome, nobody would be very surprised if house colour did turn out to be a simple Mendelian character in accordance with my thought experiment. (Actually, colour is a slightly unfortunate example to have chosen, since caddis vision is poor and they almost certainly ignore visual cues in choosing stones. Rather than use a more realistic example like stone shape (Hansell), I stay with colour for the sake of the analogy with the black pigment discussed above.)

The interesting sequel is this. House colour is determined by the colour of the stones chosen from the stream bed by the larva, not by the biochemical synthesis of a black pigment. The genes determining house colour must work via the behavioural mechanism that chooses stones, perhaps via the eyes. So much would be agreed by any ethologist. All that this chapter adds is a logical point: once we have accepted that there are genes for building behaviour, the rules of existing terminology imply that the artefact itself should be treated as part of the phenotypic expression of genes in the animal. The stones are outside the body of the organism, yet logically such a gene is a gene ‘for’ house colour, in exactly as strong a sense as the hypothetical gene
B
was for skin colour. And
B
was indeed a gene for skin colour, even though it worked by mediating sun-seeking behaviour, in exactly as strong a sense as a gene ‘for’ albinism is called a gene for skin colour. The logic is identical in all three cases. We have taken the first step in extending the concept of a gene’s phenotypic effect outside the individual body. It was not a difficult step to take, because we had already softened up our resistance by realizing that even normal ‘internal’ phenotypic effects may lie at the end of long, ramified, and indirect, causal chains. Let us now step out a little further.

The house of a caddis is strictly not a part of its cellular body, but it does fit snugly round the body. If the body is regarded as a gene vehicle, or survival machine, it is easy to see the stone house as a kind of extra protective wall, in a functional sense the outer part of the vehicle. It just happens to be made of stone rather than chitin. Now consider a spider sitting at the centre of her web. If she is regarded as a gene vehicle, her web is not a part of that vehicle in quite the same obvious sense as a caddis house, since when she turns round the web does not turn with her. But the distinction is clearly a frivolous one. In a very real sense her web is a temporary functional extension of her body, a huge extension of the effective catchment area of her predatory organs.

Once again, I know of no genetic analysis of spider web morphology, but there is nothing difficult in principle about imagining such an analysis. It is known that individual spiders have consistent idiosyncrasies which are repeated in web after web. One female
Zygiella-x-notata
, for instance, was
seen to build more than 100 webs, all lacking a particular concentric ring (Witt, Read & Peakall 1968). Nobody familiar with the literature on behaviour genetics (e.g. Manning 1971) would be surprised if the observed idiosyncrasies of individual spiders turned out to have a genetic basis. Indeed, our belief that spiders’ webs have evolved their efficient shape through natural selection necessarily commits us to a belief that, at least in the past, web variation must have been under genetic influence (
Chapter 2
). As in the case of the caddis houses, the genes must have worked via building behaviour, before that in embryonic development perhaps via neuroanatomy, before that perhaps via cell membrane biochemistry. By whatever embryological routes the genes may work in detail, the small extra step from behaviour to web is not any more difficult to conceive of than the many causal steps which preceded the behavioural effect, and which lie buried in the labyrinth of neuroembryology.