The Selfish Gene (38 page)

The effect of genes on colour and shape of gape is itself indirect. And now here is the point. Only a little more indirect is the effect of the same cuckoo genes on the behaviour of the besotted host. In exactly the same sense as we may speak of cuckoo genes having (phenotypic)effects on the colour and shape of cuckoo gapes, so we may speak of cuckoo genes having (extended phenotypic) effects on host behaviour. Parasite genes can have effects on host bodies, not just when the parasite lives inside the host where it can manipulate by direct chemical means, but when the parasite is quite separate from the host and manipulates it from a distance. Indeed, as we are about to see, even chemical influences can act outside the body.

Cuckoos are remarkable and instructive creatures. But almost any wonder among the vertebrates can be surpassed by the insects. They have the advantage that there are just so many of them; my colleague Robert May has aptly observed that 'to a good approximation, all species are insects.' Insect 'cuckoos' defy listing; they are so numerous and their habit has been reinvented so often. Some examples that we'll look at have gone beyond familiar cuckooism to fulfil the wildest fantasies that The Extended Phenotype might have inspired.

A bird cuckoo deposits her egg and disappears. Some ant cuckoo females make their presence felt in more dramatic fashion. I don't often give Latin names, but Bothriomyrmex
regicidus and B. decapitans tell a story. These two species are both parasites on other species of ants. Among all ants, of course, the young are normally fed not by parents but by workers, so it is workers that any would-be cuckoo must fool or manipulate. A useful first step is to dispose of the workers' own mother with her propensity to produce competing brood. In these two species the parasite queen, all alone, steals into the nest of another ant species. She seeks out the host queen, and rides about on her back while she quietly performs, to quote Edward Wilson's artfully macabre understatement, 'the one act for which she is uniquely specialized: slowly cutting off the head of her victim'. The murderess is then adopted by the orphaned workers, who unsuspectingly tend her eggs and larvae. Some are nurtured into workers themselves, who gradually replace the original species in the nest. Others become queens who fly out to seek pastures new and royal heads yet unsevered.

But sawing off heads is a bit of a chore. Parasites are not accustomed to exerting themselves if they can coerce a stand-in. My favourite character in Wilson's The Insect Societies is Monomorium
santschii. This species, over evolutionary time, has lost its worker caste altogether. The host workers do everything for their parasites, even the most terrible task of all. At the behest of the invading parasite queen, they actually perform the deed of murdering their own mother. The usurper doesn't need to use her jaws. She uses mind-control. How she does it is a mystery; she probably employs a chemical, for ant nervous systems-are generally highly attuned to them. If her weapon is indeed chemical, then it is as insidious a drug as any known to science. For think what it accomplishes. It floods the brain of the worker ant, grabs the reins of her muscles, woos her from deeply ingrained duties and turns her against her own mother. For ants, matricide is an act of special genetic madness and formidable indeed must be the drug that drives them to it. In the world of the extended phenotype, ask not how an animal's behaviour benefits its genes; ask instead whose genes it is benefiting.

It is hardly surprising that ants are exploited by parasites, not just other ants but an astonishing menagerie of specialist hangers-on. Worker ants sweep a rich flow of food from a wide catchment area into a central hoard which is a sitting target for freeloaders. Ants are also good agents of protection: they are well-armed and numerous. The aphids of Chapter 10 could be seen as paying out nectar to hire professional bodyguards. Several butterfly species live out their caterpillar stage inside an ants' nest Some are straightforward pillagers. Others offer something to the ants in return for protection.

Often they bristle, literally, with equipment for manipulating their protectors. The caterpillar of a butterfly called Thisbe
irenea has a sound-producing organ in its head for summoning ants, and a pair of telescopic spouts near its rear end which exude seductive nectar. On its shoulders stands another pair of nozzles, which cast an altogether more subtle spell. Their secretion seems to be not food but a volatile potion that has a dramatic impact upon the ants' behaviour. An ant coming under the influence leaps clear into the air. Its jaws open wide and it turns aggressive, far more eager than usual to attack, bite and sting any moving object. Except, significantly, the caterpillar responsible for drugging it. Moreover, an ant under the sway of a dope-peddling caterpillar eventually enters a state called binding', in which it becomes inseparable from its caterpillar for a period of many days. Like an aphid, then, the caterpillar employs ants as bodyguards, but it goes one better. Whereas aphids rely on the ants' normal aggression against predators, the caterpillar administers an aggression-arousing drug and it seems to slip them something addictively binding as well.

I have chosen extreme examples. But, in more modest ways, nature teems with animals and plants that manipulate others of the same or of different species. In all cases in which natural selection has favoured genes for manipulation, it is legitimate to speak of those same genes as having (extended phenotypic) effects on the body of the manipulated organism. It doesn't matter in which body a gene physically sits. The target of its manipulation may be the same body or a different one. Natural selection favours those genes that manipulate the world to ensure their own propagation. This leads to what I have called the Central Theorem of the Extended Phenotype: An animals 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. I was writing in the context of animal behaviour, but the theorem could apply, of course, to colour, size, shape-to anything.

It is finally time to return to the problem with which we started, to the tension between individual organism and gene as rival candidates for the central role in natural selection. In earlier chapters I made the assumption that there was no problem, because individual reproduction was equivalent to gene survival. I assumed there that you can say either The organism works to propagate all its genes' or 'The genes work to force a succession of organisms to propagate them.' They seemed like two equivalent ways of saying the same thing, and which form of words you chose seemed a matter of taste. But somehow the tension remained.

One way of sorting this whole matter out is to use the terms 'replicator' and 'vehicle'. The fundamental units of natural selection, the basic things that survive or fail to survive, that form lineages of identical copies with occasional random mutations, are called replicators. DNA molecules are replicators. They generally, for reasons that we shall come to, gang together into large communal survival machines or 'vehicles'. The vehicles that we know best are individual bodies like our own. A body, then, is not a replicator; it is a vehicle. I must emphasize this, since the point has been misunderstood. Vehicles don't replicate themselves; they work to propagate their replicators. Replicators don't behave, don't perceive the world, don't catch prey or run away from predators; they make vehicles that do all those things. For many purposes it is convenient for biologists to focus their attention at the level of the vehicle. For other purposes it is convenient for them to focus their attention at the level of the replicator. Gene and individual organism are not rivals for the same starring role in the Darwinian drama. They are cast in different, complementary and in many respects equally important roles, the role of replicator and the role of vehicle. The replicator/vehicle terminology is helpful in various ways. For instance it clears up a tiresome controversy over the level at which natural selection acts. Superficially it might seem logical to place 'individual selection' on a sort of ladder of levels of selection, halfway between the 'gene selection' advocated in Chapter 3 and the 'group selection' criticized in Chapter 7. 'Individual selection' seems vaguely to be a middle way between two extremes, and many biologists and philosophers have been seduced into this facile path and treated it as such. But we can now see that it isn't like that at all. We can now see that the organism and the group of organisms are true rivals for the vehicle role in the story, but neither of them is even a candidate for the replicator role. The controversy between 'individual selection' and 'group selection' is a real controversy between alternative vehicles. The controversy between individual selection and gene selection isn't a controversy at all, for gene and organism are candidates for different, and complementary, roles in the story, the replicator and the vehicle.

The rivalry between individual organism and group of organisms for the vehicle role, being a real rivalry, can be settled. As it happens the outcome, in my view, is a decisive victory for the individual organism. The group is too wishy-washy an entity. A herd of deer, a pride of lions or a pack of wolves has a certain rudimentary coherence and unity of purpose. But this is paltry in comparison to the coherence and unity of purpose of the body of an individual lion, wolf, or deer. That this is true is now widely accepted, but why is it true? Extended phenotypes and parasites can again help us.

We saw that when the genes of a parasite work together with each other, but in opposition to the genes of the host (which all work together with each other), it is because the two sets of genes have different methods of leaving the shared vehicle, the host's body. Snail genes leave the shared vehicle via snail sperm and eggs. Because all snail genes have an equal stake in every sperm and every egg, because they all participate in the same unpartisan meiosis, they work together for the common good, and therefore tend to make the snail body a coherent, purposeful vehicle. The real reason why a fluke is recognizably separate from its host, the reason why it doesn't merge its purposes and its identity with the purposes and identity of the host, is that the fluke genes don't share the snail genes' method of leaving the shared vehicle, and don't share in the snail's meiotic lottery-they have a lottery of their own. Therefore, to that extent and that extent only, the two vehicles remain separated as a snail and a recognizably distinct fluke inside it. If fluke genes were passed on in snail eggs and sperms, the two bodies would evolve to become as one flesh. We mightn't even be able to tell that there ever had been two vehicles.

'Single' individual organisms such as ourselves are the ultimate embodiment of many such mergers. The group of organisms-the flock of birds, the pack of wolves-does not merge into a single vehicle, precisely because the genes in the flock or the pack do not share a common method of leaving the present vehicle. To be sure, packs may bud off daughter packs. But the genes in the parent pack don't pass to the daughter pack in a single vessel in which all have an equal share. The genes in a pack of wolves don't all stand to gain from the same set of events in the future. A gene can foster its own future welfare by favouring its own individual wolf, at the expense of other individual wolves. An individual wolf, therefore, is a vehicle worthy of the name. A pack of wolves is not. Genetically speaking, the reason for this is that all the cells except the sex cells in a wolf's body have the same genes, while, as for the sex cells, all the genes have an equal chance of being in each one of them. But the cells in a pack of wolves do not have the same genes, nor do they have the same chance of being in the cells of sub-packs that are budded off. They have everything to gain by struggling against rivals in other wolf bodies (although the fact that a wolf-pack is likely to be a kin group will mitigate the struggle).

The essential quality that an entity needs, if it is to become an effective gene vehicle, is this. It must have an impartial exit channel into the future, for all the genes inside it. This is true of an individual wolf. The channel is the thin stream of sperms, or eggs, which it manufactures by meiosis. It is not true of the pack of wolves. Genes have something to gain from selfishly promoting the welfare of their own individual bodies, at the expense of other genes in the wolf pack. A bee-hive, when it swarms, appears to reproduce by broad-fronted budding, like a wolf pack. But if we look more carefully we find that, as far as the genes are concerned, their destiny is largely shared. The future of the genes in the swarm is, at least to a large extent, lodged in the ovaries of one queen. This is why-it is just another way of expressing the message of earlier chapters-the bee colony looks and behaves like a truly integrated single vehicle.

Everywhere we find that life, as a matter of fact, is bundled into discrete, individually purposeful vehicles like wolves and bee-hives. But the doctrine of the extended phenotype has taught us that it needn't have been so. Fundamentally, all that we have a right to expect from our theory is a battleground of replicators, jostling, jockeying, fighting for a future in the genetic hereafter. The weapons in the fight are phenotypic effects, initially direct chemical effects in cells but eventually feathers and fangs and even more remote effects. It undeniably happens to be the case that these phenotypic effects have largely become bundled up into discrete vehicles, each with its genes disciplined and ordered by the prospect of a shared bottleneck of sperms or eggs funnelling them into the future. But this is not a fact to be taken for granted. It is a fact to be questioned and wondered at in its own right. Why did genes come together into large vehicles, each with a single genetic exit route? Why did genes choose to gang up and make large bodies for themselves to live in? In The Extended Phenotype I attempt to work out an answer to this difficult problem. Here I can sketch only a part of that answer-although, as might be expected after seven years, I can also now take it a little further.