The Extended Phenotype: The Long Reach of the Gene (Popular Science) (50 page)

Excellent, but remember that ‘genetic background’ can include genes in other organisms as well as genes within the same organism.

The result of the close interdependence of all genes in a gene pool is tight cohesion. No gene frequency can be changed, nor any gene be added to the gene pool, without an effect on the genotype as a whole, and thus indirectly on the selective value of other genes.

Mayr himself has now subtly shifted to talking about a coadapted gene
pool
, rather than a coadapted individual genome. This is a great step in the right direction, but we must still take one further step. Mayr is here talking about interactions between all the genes in one gene-pool, regardless of the bodies they happen to be sitting in. The doctrine of the extended phenotype ultimately requires us to acknowledge the same kind of interactions among genes of different gene-pools, different phyla, different kingdoms.

Consider again the ways in which a pair of genes in the same gene-pool can interact, more specifically the ways in which the frequency of each in the
gene-pool can affect the survival prospects of the other. The first way, and the one which I suspect Mayr had mainly in mind, is through sharing the same body. The survival prospects of gene
A
are influenced by the frequency in the population of gene
B
, because
B
’s frequency influences the probability that
A
will find itself sharing a body with
B
. The interaction between the loci determining moth stripe direction and sitting direction was an example of this. So was the hypothetical lupin-mimicking caterpillar. So is a pair of genes coding for enzymes that are necessary for successive stages in a particular pathway synthesizing a useful substance. Call this type of gene interaction ‘within-body’ interaction.

The second way in which the frequency of a gene
B
in a population can affect the survival prospects of a gene
A
is ‘between-body’ interaction. The vital influence here is on the probability that any body in which
A
sits will meet another body in which
B
sits. My hypothetical cicadas provided an example of this. So does Fisher’s sex ratio theory. As I have emphasized, it has been one of my purposes in this chapter to minimize the distinction between the two kinds of gene interaction, within-body and between-body interaction.

But now consider interactions between genes in different gene-pools, different species. It will be seen that there is rather little distinction between a cross-species gene interaction and a within-species between-individual gene interaction. In neither case do the interacting genes share a body. In both cases the survival prospects of each may depend on the frequency, in its own gene-pool, of the other gene. Let me illustrate the point using the lupin thought experiment again. Suppose there is a species of beetle which is polymorphic like the cicadas. In some areas it turns out that the pink morphs of both species, cicadas and beetles, predominate, while in other areas the blue morphs of both species predominate. The two species differ in body size. They ‘cooperate’ in faking inflorescences, the smaller-bodied cicadas tending to sit near the tips of stems, where small flowers might be expected, the larger beetles tending to sit nearer the base of each fake inflorescence. A joint beetle/cicada ‘inflorescence’ fools birds more effectively than either a pure beetle or a pure cicada one.

Model 2’s frequency-dependent selection will tend to lead to the evolution of one of two evolutionarily stable states, just as before, except that two species are now involved. If historical accident leads to one local area being dominated by pink morphs (regardless of species), selection within both species will favour pink morphs over blue; and vice versa. If the beetle species was relatively recently introduced into areas already colonized by the cicada species, the direction of selection within the beetle species will depend on the colour of the locally predominant morph of cicadas. Thus there will be frequency-dependent interaction between genes in two different gene-pools, the gene-pools of two non-interbreeding species. In faking the
inflorescence of a lupin, cicadas might cooperate with spiders or snails just as effectively as with beetles or with cicadas of another species. Model 2 works across species and across phyla, as well as across individuals and within individuals.

Across kingdoms, too. Consider the interaction between flax (
Linum usitissimum
) and the rust fungus
Melampsora lini
, although this is an antagonistic rather than a cooperative interaction. ‘There is essentially a one-to-one matching in which a specific allele in the flax confers resistance to a specific allele in the rust. This “gene-for-gene” system has since been found in numerous other plant species … Models of gene-for-gene interactions are not formulated in terms of ecological parameters because of the specific nature of the genetic systems. It is one case in which the genetic interactions between species can be understood without reference to the phenotypes. A model of a gene-for-gene system would necessarily have between-species frequency dependence … (Slatkin & Maynard Smith 1979, pp. 255–256).

In this chapter, as in others, I have used hypothetical thought experiments to aid clear explanation. In case they are found too far-fetched, let me turn to Wickler again for an example of a real cicada which does something at least as far-fetched as anything I have invented.
Ityraea nigrocincta
, like
I. gregorii
, practises cooperative mimicry of lupin-like inflorescences, but it ‘possesses a further peculiarity in that both sexes have two morphs, a green form and a yellow form. These two morphs may squat together, and the green forms tend to sit at the top of the stem, especially on vertical stems, with the yellow forms below. The result is an extremely convincing “inflorescence”, because the true flowers of inflorescences often open progressively from base to apex, so that green buds are still present at the tip when the base is covered with open flowers’ (Wickler 1968).

These three chapters have extended the concept of phenotypic expression of genes by easy stages. We began with the recognition that even within a body there are many degrees of distance of gene control over phenotypes. For a nuclear gene to control the shape of the cell in which it sits is presumably simpler than to control the shape of some other cell, or of the whole body in which the cell sits. Yet we conventionally lump the three together and call them all genetic control of phenotype. My thesis has been that the slight further conceptual step outside the immediate body is a comparatively minor one. Nevertheless it is an unfamiliar one, and I tried to develop the idea in stages, working through inanimate artefacts to internal parasites controlling their hosts’ behaviour. From internal parasites we moved via cuckoos to action at a distance. In theory, genetic action at a distance could include almost all interactions between individuals of the same or different species. The living world can be seen as a network of interlocking fields of replicator power.

It is hard for me to imagine the kind of mathematics that the
understanding of the details will eventually demand. I have a dim vision of phenotypic characters in an evolutionary space being tugged in different directions by replicators under selection. It is of the essence of my approach that the replicators tugging on any given phenotypic feature will include some from outside the body as well as those inside it. Some will obviously be tugging harder than others, so the arrows of force will have varying magnitude as well as direction. Presumably the theory of arms races—the rare-enemy effect, the life/dinner principle, etc.—will have a prominent role to play in the assignment of these magnitudes. Sheer physical proximity will probably play a role: genes seem likely, other things being equal, to exert more power over nearby phenotypic characters than over distant ones. As an important special case of this, cells are likely to be quantitatively more heavily influenced by genes inside them than by genes inside other cells. The same will go for bodies. But these will be quantitative effects, to be weighed in the balance with other considerations from arms race theory. Sometimes, say because of the rare-enemy effect, genes in other bodies may exert more power than the body’s ‘own’ genes, over particular aspects of its phenotype. My hunch is that almost all phenotypic characters will turn out to bear the marks of compromise between internal and external replicator forces.

The idea of conflict and compromise between many selection pressures bearing on a given phenotypic character is, of course, familiar from ordinary biology. We often speak of, say, the size of a bird’s tail as a compromise between the needs of aerodynamics and the needs of sexual attractiveness. I do not know what kind of mathematics are considered suitable for describing this kind of within-body conflict and compromise, but whatever they are, they should be generalized to cope with the analogous problems of genetic action at a distance and extended phenotypes.

But I have not the wings to fly in mathematical spaces. There must be a verbal message for those that study animals in the field. What difference will the doctrine of the extended phenotype make to how we actually see animals? Most serious field biologists now subscribe to the theorem, largely due to Hamilton, that animals are expected to behave as if maximizing the survival chances of all the genes inside them. I have amended this to a new central theorem of the extended phenotype: 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 the behaviour. The two theorems would amount to the same thing if animal phenotypes were always under the unadulterated control of their own genotypes, and uninfluenced by the genes of other organisms. In advance of a mathematical theory to handle the quantitative interactions between conflicting pressures, perhaps the simplest qualitative conclusion is that the behaviour we are looking at may be, at least partly, an adaptation for the
preservation of some other animal’s or plant’s genes. It may therefore be positively maladaptive for the organism performing the behaviour.

Once when I tried to persuade a colleague of this—he is a staunch believer in the power of Darwinian selection, and a good field investigator of it—he thought that I was making an anti-adaptation point. He warned me that time and again people had written off some quirk of animal behaviour or morphology as functionless or maladaptive, only to discover that they had not fully understood it. He was right. But the point I am making is different. When I say here that a behaviour pattern is maladaptive, I only mean it is maladaptive for the
individual animal
performing it. I am suggesting that the individual performing the behaviour is not the entity for whose benefit the behaviour is an adaptation. Adaptations benefit the genetic replicators responsible for them, and only incidentally the individual organisms involved.

This could have been the end of the book. We have extended the phenotype out as far as it can go. The past three chapters build to a climax of a sort, and we might have been content with this as consummation. But I prefer to end on an upbeat, to begin the arousing of a tentative new curiosity. I confessed at the outset to being an advocate, and an easy way for any advocate to prepare the ground for his case is to attack the alternative. Before advocating the doctrine of the extended phenotype of an active germ-line replicator, therefore, I tried to undermine the reader’s confidence in the individual organism as the unit of adaptive benefit. But, now that we have discussed the extended phenotype itself, it is time to reopen the question of the organism’s existence and obvious importance in the hierarchy of life, and see whether we see it any clearer in the light of the extended phenotype. Given that life did not
have
to be packaged into discrete organisms, and allowing that organisms are not always totally discrete, why, nevertheless, did active germ-line replicators so conspicuously opt for the organismal way of doing things?

Having devoted most of this book to playing down the importance of the individual organism, and to building up an alternative image of a turmoil of selfish replicators, battling for their own survival at the expense of their alleles, reaching unimpeded through individual body walls as though those walls were transparent, interacting with the world and with each other without regard to organismal boundaries, we now hesitate. There really
is
something pretty impressive about individual organisms. If we actually could wear spectacles that made bodies transparent and displayed only DNA, the distribution of DNA that we would see in the world would be overwhelmingly non-random. If cell nuclei glowed like stars and all else was invisible, multicellular bodies would show up as close-packed galaxies with cavernous space between them. A million billion glowing pinpricks move in unison with each other and out of step with all the members of other such galaxies.

The organism is a physically discrete machine, usually walled off from other such machines. It has an internal organization, often of staggering complexity, and it displays to a high degree the quality that Julian Huxley (1912) labelled ‘individuality’—literally indivisibility—the quality of being sufficiently heterogeneous in form to be rendered non-functional if cut in half. Genetically speaking, too, the individual organism is usually a clearly definable unit, whose cells have the same genes as each other but different genes from the cells of other organisms. To an immunologist the individual organism has a special kind of ‘uniqueness’ (Medawar 1957), in that it will readily accept grafts from other parts of its own body, but not from other bodies. To the ethologist—and this is really an aspect of Huxley’s indivisibility—the organism is a unit of behavioural action in a much stronger sense than, say, two organisms, or a limb of an organism. The organism has one coordinated central nervous system. It takes ‘decisions’ (Dawkins & Dawkins 1973) as a unit. All its limbs conspire harmoniously together to achieve one end at a time. On those occasions when two or more organisms try to coordinate their efforts, say when a pride of lions
cooperatively stalks prey, the feats of coordination among individuals are feeble compared with the intricate orchestration, with high spatial and temporal precision, of the hundreds of muscles within each individual. Even a starfish, whose tube-feet enjoy a measure of autonomy and may tear the animal in two if the circum-oral nerve ring has been surgically cut, looks like a single entity, and in nature behaves as if it had a single purpose.