The yellow color of the Malpighian tubules of an insect cannot itself be the subject of natural selection since that color can never be seen by any organism. Rather it is the pleiotropic consequence of red eye pigment metabolism, which may be adaptive.’ There
The animal we are looking at is very probably out of date, built under the influence of genes that were selected in some earlier era when conditions were different.
. A gene ‘for’ A in environment X may well turn out to be a gene for B in environment Y. It is simply meaningless to speak of an absolute, context-free, phenotypic effect of a given gene.
In the world before candles were invented, small sources of bright light in darkness would either have been celestial bodies at optical infinity, or they might have been escape holes from caves or other enclosed spaces. The latter case immediately suggests a survival value for approaching light sources. The former case also suggests one, but in a more indirect sense (Fraenkel & Gunn 1940). Many insects use celestial bodies as compasses. Since these are at optical infinity, rays from them are parallel, and an insect that maintains a fixed orientation of, say, 30° to them will go in a straight line. But if the rays do not come from infinity they will not be parallel, and an insect that behaves in this way will spiral in to the light source (if steering an acute-angled course) or spiral away (if steering an obtuse-angled course) or orbit the source (if steering a course of exactly 90° to the rays). Self-immolation by insects in candle flames, then, has no survival value in itself: according to this hypothesis, it is a byproduct of the useful habit of steering by means of sources of light which are ‘assumed’ to be at infinity. That assumption was once safe. It now is safe no longer, and it may be that selection is even now working to modify the insects’ behaviour. (
useful analogy here is one that I heard from R. D. Alexander. Moths fly into candle flames, and this does nothing to help their
My own feeling is that somewhere here may lie the solution to the real paradox of this section on historical constraints. The jet engine analogy suggested that animals ought to be risible monstrosities of lashed-up improvisation, top-heavy with grotesque relics of patched-over antiquity.
Like a river, natural selection blindly meliorizes its way down successive lines of immediately available least resistance. The animal that results is not the most perfect design conceivable, nor is it merely good enough to scrape by. It is the product of a historical sequence of changes, each one of which represented, at best, the better of the alternatives that happened to be around at the time.
Birds fly with wings made of feathers, bats with wings consisting of flaps of skin. Why do they not both have wings made in the same way, whichever way is ‘superior’? A confirmed adaptationist might reply that birds must be better off with feathers and bats better off with skin flaps. An extreme anti-adaptationist might say that very probably feathers would actually be better than skin-flaps for both birds and bats, but bats never had the good fortune to produce the right mutations.
animals are quite likely to work hard and vigorously for the good of some other individual’s genes, and to the detriment of their own.
we tend to assume that manipulation only works because of the ‘time-lag’ constraint on perfection.
. I have suggested that fundamental asymmetries such as the life/dinner principle, and the rare-enemy effect, will see to it that many arms races reach a stable state in which animals on one side permanently work for the benefit of animals on the other side, and to their own detriment;
I define a replicator as anything in the universe of which copies are made. Examples are a DNA molecule, and a sheet of paper that is xeroxed. Replicators may be classified in two ways. They may be ‘active’ or ‘passive’, and, cutting across this classification, they may be ‘germ-line’ or ‘dead-end’ replicators.
An active replicator is any replicator whose nature has some influence over its probability of being copied.
The doctrine of the extended phenotype is that the phenotypic effect of a gene (genetic replicator) is best seen as an effect upon the world at large, and only incidentally upon the individual organism—or any other vehicle—in which it happens to
Now, how can two alternative ways of achieving the same end, in this case two alternative ways of acquiring a nest, coexist in one population? Surely one or the other ought to be more successful, and the less successful one should be removed from the population by natural selection?
firstly, digging and entering might be two outcomes of one ‘conditional strategy’; secondly, they might be equally successful at some critical frequency maintained by frequency-dependent selection—part of a ‘mixed ESS
If the first possibility were correct, all wasps would be programmed with the same conditional rule: ‘If X is true, dig, otherwise enter’; for instance, ‘If you happen to be a small wasp, dig, otherwise use your superior size to take over another wasp’s burrow’. We failed to find any evidence for a conditional program of this or any other kind. Instead, we convinced ourselves that the second possibility, the ‘mixed ESS’, fitted the facts.
The first extreme is a balanced polymorphism. In this case, if we want to use the initials ‘ESS’, the final S should be thought of as standing for state of the population rather than strategy of the individual. If this possibility obtained, there would be two distinct kinds of wasps, diggers and enterers, who would tend to be equally successful. If they were not equally successful, natural selection would tend to eliminate the less successful one from the population. It is too much to hope that, by sheer coincidence, the net costs and benefits of digging would exactly balance the net costs and benefits of entering. Rather, we are invoking frequency-dependent selection. We postulate a critical equilibrium proportion of diggers, p*, at which the two kinds of wasps are equally successful.
the other end of the continuum there is no polymorphism among individuals. In the stable state all wasps obey the same program, but that program is itself a mixture. Every wasp is obeying the instruction, ‘Dig with probability p, enter with probability 1 – p’; for instance, ‘Dig on 70 per cent of occasions, enter on 30 per cent of occasions’. If this is regarded as a ‘program’, we could perhaps refer to digging and entering themselves as ‘subroutines’. Every wasp is equipped with both subroutines. She is programmed to choose one or the other on each occasion with a characteristic probability,
As already explained, I call digging and entering ‘subroutines’, rather than programs, because we have already used ‘program’ for the overall lifetime choosing rules of an individual. An individual is regarded as being programmed with a rule for choosing the digging or the entering subroutine with some probability p.
digression. I have not been trying to argue that ‘subroutines’, or ‘strategies’ are really true replicators, true units of natural selection. They are not. Genes and fragments of genomes are true replicators. Subroutines and strategies can be thought of for certain purposes as if they were replicators, but when those purposes have been served we must return to reality. Natural selection really has the effect of choosing between alleles in wasp gene-pools, alleles which influence the probability that individual wasps will enter or dig.
But it is also easy to imagine cases where a gene might promote its own survival while harming the survival chances of most of the rest of the genome. Following Alexander and Borgia (1978) I shall call such genes outlaws.
Any replicator that managed to subvert the rules of meiosis so that it enjoyed more than the ordained 50 per cent chance of ending up in a gamete would, other things being equal, tend to be favoured over its alleles in natural
selection. Such genes are known to geneticists under the name of meiotic drive genes or segregation distorters.
. At the beginning of the chapter I divided outlaws into ‘allelic outlaws’ and ‘laterally spreading outlaws’. All the suggested outlaws we have so far considered have been allelic: they are favoured over their alleles at their own loci, while being opposed by modifiers at other loci. I now turn to laterally spreading outlaws. These are outlaws unruly enough to break away altogether from the discipline of allelic competition within the confines of a locus. They spread to other loci, even create new loci for themselves by increasing the size of the genome. They are conveniently discussed under the heading ‘Selfish DNA’,
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.
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.
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.
. 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
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
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.
The relationship of Sacculina gene to crab body is not in principle different from the relationship of caddis gene to stone, nor indeed different from the relationship of human gene to human skin. This is the first of the points that I intended to establish in this chapter. It has the corollary, which I have already emphasized in other terms in Chapter 4, that the behaviour of an individual may not always be interpretable as designed to maximize its own genetic welfare: it may be maximizing somebody else’s genetic welfare, in this case that of a parasite inside it.
: An animal’s behaviour tends to maximize the survival of the genes ‘for’ that behaviour, whether or not those genes happen to be in the body of the particular animal performing it.
Playing with an imaginary world, in order to increase our understanding of the actual world, is the technique of ‘thought experiment