The Extended Phenotype

by Richard Dawkins

  The same question arises as before. Why does the victim of manipulation stand for it? Why does the prey fish rush literally into the jaws of death? Because it ‘thinks’ it is really rushing to get a meal itself. More formally, natural selection has acted on its ancestors, favouring tendencies to approach small wriggling objects, because small wriggling objects are usually worms. Since they are not always worms but sometimes angler fish lures, there may well be some selection on prey fish to be cautious, or to sharpen up their powers of discrimination. To the extent that lures are good mimics of worms, we may surmise that selection has acted on the angler fishes’ ancestors to improve them, in the face of improved discrimination by their prey. Some prey are caught, and angler fish do make a living, so some manipulation is going on successfully.

  It is convenient to use the metaphor of an arms race whenever we have progressive improvements in adaptations in one lineage, as an evolutionary response to progressive counter-improvements in an enemy lineage. It is important to realize who are the parties that are ‘racing’ against one another. They are not individuals but lineages. To be sure, it is individuals who attack and defend, individuals who kill or resist being killed. But the arms race takes place on the evolutionary time-scale, and individuals do not evolve. It is lineages that evolve, and lineages that exhibit progressive trends in response to the selection pressures set up by the progressive improvements in other lineages.

  One lineage will tend to evolve adaptations to manipulate the behaviour of another lineage, then the second lineage will evolve counter-adaptations. We must obviously be interested in any general rules governing whether one or the other lineage can ‘win’, or have a built-in advantage. It was just such a built-in advantage that Alexander attributed to parents over their children. Apart from his major theoretical argument which, as we have seen, is now not favoured, he also plausibly suggested various practical advantages of parents over offspring: ‘… the parent is bigger and stronger than the offspring, hence in a better position to impose its will’ (Alexander 1974). This is true, but we must not forget the lesson of the previous paragraph, that an arms race is run in evolutionary time. In any one generation the muscles of a parent are stronger than those of its offspring, and whoever controls those muscles must have the upper hand. But the question at issue is, who controls the parents’ muscles? As Trivers (1974) says, ‘An offspring cannot fling its mother to the ground at will and nurse … the offspring is expected to employ psychological rather than physical tactics.’

  Krebs and I suggested that animal signals could be thought of as employing psychological tactics in rather the same way as human advertisements. Advertisements are not there to inform, or to misinform, they are there to persuade. The advertiser uses his knowledge of human psychology, of the hopes, fears and secret motives of his targets, and he designs an advertisement which is effective in manipulating their behaviour. Packard’s (1957) exposé of the deep psychological techniques of commercial advertisers makes fascinating reading for the ethologist. A supermarket manager is quoted as saying ‘People like to see a lot of merchandise. When there are only three of four cans of an item on a shelf, they just won’t move.’ The obvious analogy with lek birds does not lose its value merely because the physiological mechanism of the effect will probably prove to be different in the two cases. Hidden cine-cameras recording the eye-blinking rate of housewives in a supermaket indicated that in some cases the effect of the multiplicity of bright-coloured packages was to induce a mild hypnoidal trance.

  K. Nelson once gave a talk at a conference, entitled ‘Is bird song music? Well, then, is it language? Well, then, what is it?’ Perhaps bird song is more akin to hypnotic persuasion, or to a form of drugging. The nightingale’s song induced in John Keats a drowsy numbness ‘… as though of hemlock I had drunk’. Might it not have an even more powerful effect on the nervous system of another nightingale? If nervous systems are susceptible to drug-like influences via the normal sense organs, should we not positively expect that natural selection would have favoured the exploitation of such possibilities, would have favoured the development of visual, olfactory, or auditory ‘drugs’?

  A neurophysiologist, presented with an animal with a complex nervous system and asked to manipulate the animal’s behaviour, may insert electrodes in sensitive points of the brain and stimulate electrically, or make pinpoint lesions. An animal normally does not have direct access to the brain of another animal, although I shall mention one example, the so-called brainworm, in Chapter 12. But the eyes and ears are also entry ports to the nervous system, and there might be patterns of light or sound which, if properly deployed, could be as effective as direct electrical stimulation. Grey Walter (1953) vividly illustrates the power of flashing lights tuned to the frequency of human EEG rhythms: in one case a man felt ‘an irresistible urge to strangle the person next to him’.

  If we were asked to imagine what an ‘auditory drug’ would sound like, say for making the soundtrack of a science fiction film, what would we say? The incessant rhythm of an African drum; the eerie trilling of the tree cricket Oecanthus, of which it has been said that if moonlight could be heard that is how it would sound (quoted in Bennet-Clark 1971); or the song of the nightingale? All three strike me as worthy candidates, and I believe all three have been in some sense designed for the same purpose: the manipulation of one nervous system by another, in a way that is not in principle different from manipulation of a nervous system by a neurophysiologist’s electrodes. Of course if an animal sound powerfully affects a human nervous system this is probably incidental. The hypothesis being advanced is that selection has shaped animal sounds to manipulate some nervous system, not necessarily a human one. The snort of a pig-frog Rana grylio may affect another pig-frog as the nightingale affected Keats, or the skylark Shelley. The nightingale happened to be a better example for me to choose, because human nervous systems can be moved to deep emotion by nightingale song, whereas they are usually moved to laugh at pig-frog snorts.

  Consider that other celebrated songster, the canary, since much happens to be known about the physiology of its reproductive behaviour (Hinde & Steel 1978). If a physiologist wants to bring a female canary into reproductive condition, increase the size of her functional ovary and cause her to start nest-building and other reproductive behaviour patterns, there are various things he can do. He can inject her with gonadotropins or oestrogens. He can use electric light to increase the day-length that she experiences. Or, most interestingly from our point of view, he can play her a tape recording of male canary song. It apparently has to be canary song; budgerigar song will not do, although budgerigar song has a similar effect on female budgerigars.

  Now suppose a male canary wanted to bring a female into reproductive condition, what could he do? He does not have a syringe to inject hormones. He cannot switch on artificial lights in the female’s environment. Of course what he does is sing. The particular pattern of sounds that he makes enters the female’s head through her ears, is translated into nerve impulses, and bores insidiously into her pituitary. The male does not have to synthesize and inject gonadotropins; he makes the female’s pituitary work to synthesize them for him. He stimulates her pituitary by means of nerve impulses. They are not ‘his’ nerve impulses, in the sense that they all occur within the female’s own nerve cells. But they are his in another sense. It is his particular sounds which are subtly fashioned to make the female’s nerves work on her pituitary. Where a physiologist might pump gonadotropins into the female’s breast muscle, or electric current into her brain, the male canary pours song into her ear. And the effect is the same. Schleidt (1973) discusses other examples of such ‘tonic’ effects of signals on the physiology of the receiver.

  ‘Bores insidiously into her pituitary’ may be too much for some readers. Certainly it begs important questions. The obvious point that will be made is that the female may benefit from the transaction as much as the male, in which case ‘insidiously’ and ‘manipulation’
are inappropriate words. Alternatively, if there is any insidious manipulation it may be by the female on the male. Maybe the female ‘insists’ upon an exhausting performance of song by her mate before she will come into reproductive condition, thereby selecting only the most robust male for a mate. I think something along those lines is quite probably the explanation of the extraordinarily high rate of copulation observed in large cats (Eaton 1978). Schaller (1972) followed a sample male lion for 55 hours, during which he copulated 157 times, with an average inter-copulation interval of 21 minutes. Ovulation in cats is induced by copulation. It seems plausible that the prodigious copulation rates shown by male lions are the end product of a runaway arms race, in which females insisted on progressively more copulations before ovulating, and males were selected for ever-increased sexual stamina. Lion copulation stamina might be regarded as the behavioural equivalent of a peacock’s tail. A version of this hypothesis is compatible with that of Bertram (1978), that females have devalued the currency of copulation as a means of reducing the occurrence of disruptive male fights.

  To continue the quotation from Trivers on psychological manipulation tactics that children might use against their parents:

  Since an offspring will often have better knowledge of its real needs than will its parents, selection should favour parental attentiveness to signals from its offspring that apprize the parent of the offspring’s condition … But once such a system has evolved, the offspring can begin to employ it out of context. The offspring can cry not only when it is famished but also when it merely wants more food than the parent is selected to give … Selection will then of course favor parental ability to discriminate the two uses of the signals, but still subtler mimicry and deception by the offspring are always possible [Trivers 1974].

  We have arrived again at the main question raised by arms races. Are there any generalizations we can make about which side is likely to ‘win’ an arms race?

  First, what does it mean to speak of one side or the other ‘winning’? Does the ‘loser’ eventually go extinct? At times this may happen. A bizarre possibility is suggested by Lloyd and Dybas (1966) for periodical cicadas (Simon, 1979, gives an entertaining recent account). Periodical cicadas are three species of the genus Magicicada. All three species have two varieties, a 17-year and a 13-year variety. Each individual spends 17 (or 13) years feeding as an underground nymph, before emerging for a few weeks of adult reproductive life, after which it dies. In any particular area all life cycles are synchronized, with the result that each area experiences a cicada plague every 17 (or 13) years. The functional significance of this is presumably that would-be predators or parasites are swamped in plague years and starved in intervening years. The risk to an individual who remains synchronized is therefore less than the risk to one who breaks synchrony and emerges, say, a year early. But given the admitted advantage of synchrony, why didn’t the cicadas settle on a shorter life cycle than 17 (or 13) years, thereby reducing the unfortunate delay before reproduction? Lloyd and Dybas’s suggestion is that the long life cycle is the end result of an ‘evolutionary race through time’ with a now extinct predator (or parasitoid). ‘This hypothetical parasitoid presumably had a life cycle that was almost synchronized with, and nearly equal in length to (but always slightly less than), the ancestral protoperiodical cicada. As the theory goes, the cicadas finally outran their parasitoid pursuer and the poor specialized beast went extinct’ (Simon 1979). Ingeniously, Lloyd and Dybas go further and suggest that the arms race culminated in life cycles lasting a prime number of years (13 or 17) because otherwise a predator with a shorter life cycle might synchronize with the cicadas every second or every third time around!

  There is really no need for the ‘loser’ lineage of an arms race to go extinct, as suggested for the cicada parasitoid. It may be that the ‘winner’ is such a rare species that it constitutes a relatively negligible risk to individuals of the ‘loser’ species. The winner only wins in the sense that its adaptations against the loser are not effectively countered. This is good for individuals of the winner lineage, but it may not be very bad for individuals of the loser lineage who, after all, are running other races simultaneously against other lineages, possibly very successfully.

  This ‘rare-enemy effect’ is an important example of an asymmetry in selection pressures acting on the two sides of an arms race. Although we gave no formal models, Krebs and I considered one such asymmetry qualitatively under the catchphrase heading of the ‘life/dinner principle’, named after a fable of Aesop which was called to our attention by M. Slatkin: ‘The rabbit runs faster than the fox, because the rabbit is running for his life while the fox is only running for his dinner.’ The general point here is that for an animal on one side of the arms race the penalty of failure is more severe than for an animal on the other side of the arms race. Mutations that make foxes run more slowly than rabbits might therefore survive in the fox gene-pool longer than mutations that cause rabbits to run slowly can expect to survive in the rabbit gene-pool. A fox may reproduce after being outrun by a rabbit. No rabbit has ever reproduced after being outrun by a fox. Foxes may therefore be better able than rabbits to divert resources away from adaptations for running fast and into other adaptations; rabbits therefore appear to ‘win’ the arms race as far as running speed is concerned. The point is really one about asymmetries in strengths of selection pressure.

  Probably the simplest asymmetry arises from what I have just called the rare-enemy effect, where one side in the arms race is rare enough to exert a relatively negligible influence on any given individual on the other side. This can be illustrated by the angler fish example again, and the example has the additional merit of showing that there is no necessary reason why prey (‘rabbits’) should come out ‘ahead’ of predators (‘foxes’). Assume that angler fish are rather rare, so however unpleasant it may be for an individual prey to be caught by an angler fish, the risk of this happening to a randomly designated individual is not high. Any adaptation costs something. For a small fish to discriminate angler fish lures from real worms it needs sophisticated visual processing apparatus. To make this apparatus may cost it resources which could otherwise have been put into, say gonads (see Chapter 3). Then again, using the apparatus takes time, which could have been spent on courting females or defending a territory, or indeed chasing the prey if it is judged to be a real worm. Finally, a fish that is very cautious about approaching worm-like objects may cut its risk of being eaten, but it also increases its risk of starving. This is because it may avoid many perfectly good worms because they might have been angler fish lures. It may well be that the balance of costs and benefits favours complete recklessness on the part of some prey animals. Individuals that always try to eat small wriggling objects, and damn the consequences, may, on average, do better than individuals that pay the costs of attempting to discriminate real worms from angler fish lures. William James made much the same point in 1910: ‘There are more worms unattached to hooks than impaled upon them; therefore, on the whole, says Nature to her fishy children, bite at every worm and take your chances’ (quoted by Staddon 1981).

  Now look at it from the point of view of the angler fish. It, too, needs to spend resources on apparatus to outwit its opponents in the arms race. The resources that go into making a lure could have been put into gonads. The time spent sitting motionless waiting patiently for prey could have been spent in actively searching for a mate. But the angler fish absolutely depends on the success of its lure for survival. An angler fish that is not well equipped to lure prey will starve. A prey fish that is not well equipped to avoid being lured may run only a small risk of being eaten, and may more than compensate for the risk by saving the cost of making and using the equipment.

  In this example the angler wins the arms race against its prey, simply because its side of the arms race constitutes a relatively negligible threat to any given individual of the other side, through being rare. This does not, by the way, mean that selection wil
l favour predators that take steps to be rare, or to constitute a small threat to their prey! Within the angler fish population selection will favour those individuals who are the most efficient killers and the most prolific contributors to reducing the rarity of their species. But the angler fish lineage may ‘keep ahead’ in the arms race against their prey, simply as an incidental consequence of being rare for some other reason, rare in spite of all their efforts.

  In addition, there are likely to be frequency-dependent effects for various reasons (Slatkin & Maynard Smith 1979). For instance, as individuals on one side in an arms race, say angler fish, become rarer, they will constitute a steadily weaker threat to individuals on the other side of the arms race. Therefore individuals on the other side will be selected to shift precious resources away from adaptations concerned with this particular arms race. In the present example, prey fish are selected to shift resources away from anti-angler adaptations and into other things such as gonads, possibly to the extent of total recklessness as suggested above. This will make life easier for individual anglers, who will therefore become more numerous. Anglers will then come to constitute a severer threat to the prey fish, who will then be selected to shift resources back into anti-angler adaptations. As usual in such arguments, we do not have to imagine an oscillation. There may, instead, be an evolutionarily stable endpoint to the arms race; stable, that is, until an environmental change shifts the relevant costs and benefits.

  Obviously, until we know a great deal more about costs and benefits in the field, we cannot predict the outcome of particular arms races. For present purposes this does not matter. All we need is to satisfy ourselves that in any particular arms race individuals on one side may have more to lose than individuals on the other side. The rabbit has his life to lose, the fox only has his dinner. The incompetent angler fish dies; the incompetent avoider of angler fish only runs a tiny risk of dying, and may, by saving costs, end up better off than the ‘competent’ prey fish.