The Extended Phenotype: The Long Reach of the Gene (Popular Science) (6 page)

Xenophobia is controversial, so consider a behaviour pattern that nobody would fear to regard as a Darwinian adaptation. Pit-digging in antlions is obviously an adaptation to catch prey. Antlions are insects, neuropteran larvae with the general appearance and demeanour of monsters from outer space. They are ‘sit and wait’ predators who dig pits in soft sand which trap ants and other small walking insects. The pit is a nearly perfect cone, whose sides slope so steeply that prey cannot climb out once they have fallen in. The antlion sits just under the sand at the bottom of the pit, where it lunges with its horror-film jaws at anything that falls in.

Pit-digging is a complex behaviour pattern. It costs time and energy, and satisfies the most exacting criteria for recognition as an adaptation (Williams 1966; Curio 1973). It must, then, have evolved by natural selection. How might this have happened? The details don’t matter for the moral I want to draw. Probably an ancestral antlion existed which did not dig a pit but simply lurked just beneath the sand surface waiting for prey to blunder over it. Indeed some species still do this. Later, behaviour leading to the creation of a shallow depression in the sand probably was favoured by selection because the depression marginally impeded escaping prey. By gradual degrees over many generations the behaviour changed so that what was a shallow depression became deeper and wider. This not only hindered escaping prey but also increased the catchment area over which prey might stumble in the first place. Later still the digging behaviour changed again so that the resulting pit became a steep-sided cone, lined with fine, sliding sand so that prey were unable to climb out.

Nothing in the previous paragraph is contentious or controversial. It will be regarded as legitimate speculation about historical events that we cannot see directly, and it will probably be thought plausible. One reason why it will be accepted as uncontroversial historical speculation is that it makes no mention of genes. But my point is that none of that history, nor any comparable history, could possibly have been true unless there was genetic variation in the behaviour at every step of the evolutionary way. Pit-digging in antlions is only one of the thousands of examples that I could have chosen. Unless natural selection has genetic variation to act upon, it cannot give rise to evolutionary change. It follows that where you find Darwinian adaptation there must have been genetic variation in the character concerned.

Nobody has ever done a genetic study of pit-digging behaviour in antlions (J. Lucas, personal communication). There is no need to do one, if all we
want to do is satisfy ourselves of the sometime existence of genetic variation in the behaviour pattern. It is sufficient that we are convinced that it is a Darwinian adaptation (if you are not convinced that pit-digging is such an adaptation, simply substitute any example of which you are convinced).

I spoke of the
sometime
existence of genetic variation. This was because it is quite likely that, were a genetic study to be mounted of antlions today, no genetic variation would be found. It is in general to be expected that, where there is strong selection in favour of some trait, the original variation on which selection acted to guide the evolution of the trait will have become used up. This is the familiar ‘paradox’ (it is not really very paradoxical when we think about it carefully) that traits under strong selection tend to have low heritability (Falconer 1960); ‘…evolution by natural selection destroys the genetic variance on which it feeds’ (Lewontin 1979b). Functional hypotheses frequently concern phenotypic traits, like possession of eyes, which are all but universal in the population, and therefore without contemporary genetic variation. When we speculate about, or make models of, the evolutionary production of an adaptation, we are necessarily talking about a time when there was appropriate genetic variation. We are bound, in such discussions, to postulate, implicitly or explicitly, genes ‘for’ proposed adaptations.

Some may balk at treating ‘a genetic contribution to variation in X’ as equivalent to ‘a gene or genes for X’. But this is a routine genetic practice, and one which close examination shows to be almost inevitable. Other than at the molecular level, where one gene is seen directly to produce one protein chain, geneticists never deal with units of phenotype as such. Rather, they always deal with
differences
. When a geneticist speaks of a gene ‘for’ red eyes in
Drosophila
, he is not speaking of the cistron which acts as template for the synthesis of the red pigment molecule. He is implicitly saying: there is variation in eye colour in the population; other things being equal, a fly with this gene is more likely to have red eyes than a fly without the gene. That is all that we ever mean by a gene ‘for’ red eyes. This happens to be a morphological rather than a behavioural example, but exactly the same applies to behaviour. A gene ‘for’ behaviour X is a gene ‘for’ whatever morphological and physiological states tend to produce that behaviour.

A related point is that the use of single-locus models is just a conceptual convenience, and this is true of adaptive hypotheses in exactly the same way as it is true of ordinary population genetic models. When we use single-gene language in our adaptive hypotheses, we do not intend to make a point about single-gene models as against multi-gene models. We are usually making a point about
gene
models as against non-gene models, for example as against ‘good of the species’ models. Since it is difficult enough convincing people that they ought to think in genetic terms
at all
rather than in terms of, say, the good of the species, there is no sense in making things even more
difficult by trying to handle the complexities of many loci at the outset. What Lloyd (1979) calls the OGAM (one gene analysis model) is, of course, not the last word in genetic accuracy.
Of course
we shall eventually have to face up to multi-locus complexity. But the OGAM is vastly preferable to modes of adaptive reasoning that forget about genes altogether, and this is the only point I am trying to make at present.

Similarly we may find ourselves aggressively challenged to substantiate our ‘claims’ of the existence of ‘genes for’ some adaptation in which we are interested. But this challenge, if it is a real challenge at all, should be directed at the whole of the neo-Darwinian ‘modern synthesis’ and the whole of population genetics. To phrase a functional hypothesis in terms of genes is to make no strong claims about genes at all: it is simply to make explicit an assumption which is inseparably built into the modern synthesis, albeit it is sometimes implicit rather than explicit.

A few workers have, indeed, flung just such a challenge at the whole neo-Darwinian modern synthesis, and have claimed not to be neo-Darwinians. Goodwin (1979) in a published debate with Deborah Charlesworth and others, said, ‘… neo-Darwinism has an incoherence in it … we are not given any way of generating phenotypes from genotypes in neo-Darwinism. Therefore the theory is in this respect defective.’ Goodwin is, of course, quite right that development is terribly complicated, and we don’t yet understand much about how phenotypes are generated. But
that
they are generated, and
that
genes contribute significantly to their variation are incontrovertible facts, and those facts are all we need in order to make neo-Darwinism coherent. Goodwin might just as well say that, before Hodgkin and Huxley worked out how the nerve impulse fired, we were not entitled to believe that nerve impulses controlled behaviour.
Of course
it would be nice to know how phenotypes are made but, while embryologists are busy finding out, the rest of us are entitled by the known facts of genetics to carry on being neo-Darwinians, treating embryonic development as a black box. There is no competing theory that has even a remote claim to be called coherent.

It follows from the fact that geneticists are always concerned with phenotypic
differences
that we need not be afraid of postulating genes with indefinitely complex phenotypic effects, and with phenotypic effects that show themselves only in highly complex developmental conditions. Together with Professor John Maynard Smith, I recently took part in a public debate with two radical critics of ‘sociobiology’, before an audience of students. At one time in the discussion we were trying to establish that to talk of a gene ‘for X’ is to make no outlandish claim, even where X is a complex, learned behaviour pattern. Maynard Smith reached for a hypothetical example and came up with a ‘gene for skill in tying shoelaces’. Pandemonium broke loose at this rampant genetic determinism! The air was thick with the unmistakable sound of worst suspicions being gleefully confirmed. Delightedly
sceptical cries drowned the quiet and patient explanation of just what a
modest
claim is being made whenever one postulates a gene for, say, skill in tying shoelaces. Let me explain the point with the aid of an even more radical-sounding yet truly innocuous thought experiment (Dawkins 1981).

Reading is a learned skill of prodigious complexity, but this provides no reason in itself for scepticism about the possible existence of a gene for reading. All we would need in order to establish the existence of a gene for reading is to discover a gene for not reading, say a gene which induced a brain lesion causing specific dyslexia. Such a dyslexic person might be normal and intelligent in all respects except that he could not read. No geneticist would be particularly surprised if this type of dyslexia turned out to breed true in some Mendelian fashion. Obviously, in this event, the gene would only exhibit its effect in an environment which included normal education. In a prehistoric environment it might have had no detectable effect, or it might have had some different effect and have been known to cave-dwelling geneticists as, say, a gene for inability to read animal footprints. In our educated environment it would properly be called a gene ‘for’ dyslexia, since dyslexia would be its most salient consequence. Similarly, a gene which caused total blindness would also prevent reading, but it would not usefully be regarded as a gene for not reading. This is simply because preventing reading would not be its most obvious or debilitating phenotypic effect.

Returning to our gene for specific dyslexia, it follows from the ordinary conventions of genetic terminology that the wild-type gene at the same locus, the gene that the rest of the population has in double dose, would properly be called a gene ‘for reading’. If you object to that, you must also object to our speaking of a gene for tallness in Mendel’s peas, because the logic of the terminology is identical in the two cases. In both cases the character of interest is a
difference
, and in both cases the difference only shows itself in some specified environment. The reason why something so simple as a one gene difference can have such a complex effect as to determine whether or not a person can learn to read, or how good he is at tying shoelaces, is basically as follows. However complex a given state of the world may be, the
difference
between that state of the world and some alternative state of the world may be caused by something extremely simple.

The point I made using antlions is a general one. I could have used any real or purported Darwinian adaptation whatsoever. For further emphasis I shall use one more example. Tinbergen
et al
. (1962) investigated the adaptive significance of a particular behaviour pattern in black-headed gulls (
Larus ridibundus
), eggshell removal. Shortly after a chick hatches, the parent bird grasps the empty eggshell in the bill and removes it from the vicinity of the nest. Tinbergen and his colleagues considered a number of
possible hypotheses about the survival value of this behaviour pattern. For instance they suggested that the empty eggshells might serve as breeding grounds for harmful bacteria, or the sharp edges might cut the chicks. But the hypothesis for which they ended up finding evidence was that the empty eggshell serves as a conspicuous visual beacon summoning crows and other predators of chicks or eggs to the nest. They did ingenious experiments, laying out artificial nests with and without empty eggshells, and showed that eggs accompanied by empty eggshells were, indeed, more likely to be attacked by crows than eggs without empty eggshells by their side. They concluded that natural selection had favoured eggshell removal behaviour of adult gulls, because past adults who did not do it reared fewer children.

As in the case of antlion digging, nobody has ever done a genetic study of eggshell removal behaviour in black-headed gulls. There is no direct evidence that variation in tendency to remove empty eggshells breeds true. Yet clearly the assumption that it does, or once did, is essential for the Tinbergen hypothesis. The Tinbergen hypothesis, as normally phrased in gene-free language, is not particularly controversial. Yet it, like all the rival functional hypotheses that Tinbergen rejected, rests fundamentally upon the assumption that once upon a time there must have been gulls with a genetic tendency to remove eggshells, and other gulls with a genetic tendency not to remove them, or to be less likely to remove them. There must have been genes for removing eggshells.

Here I must enter a note of caution. Suppose we actually did a study of the genetics of eggshell removal behaviour in modern gulls. It would be a behaviour-geneticist’s dream to find a simple Mendelian mutation which radically altered the behaviour pattern, perhaps abolished the behaviour altogether. By the argument given above, this mutant would truly be a gene ‘for’ not removing eggshells, and, by definition, its wild-type allele would have to be called a gene for eggshell removal. But now comes the note of caution. It most definitely does not follow that this particular locus ‘for’ eggshell removal was one of the ones upon which natural selection worked during the evolution of the adaptation. On the contrary, it seems much more probable that a complex behaviour pattern like eggshell removal must have been built up by selection on a large number of loci, each having a small effect in interaction with the others. Once the behaviour complex had been built up, it is easy to imagine a single major mutation arising, whose effect is to destroy it. Geneticists perforce must exploit the genetic variation available for them to study. They also believe that natural selection must have worked on similar genetic variation in wreaking evolutionary change. But there is no reason for them to believe that the loci controlling modern variation in an adaptation were the very same loci at which selection acted in building up the adaptation in the first place.