The Extended Phenotype: The Long Reach of the Gene (Popular Science) (15 page)

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 will 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.

We only have to accept the general plausibility of such asymmetries in order to answer the question raised by our discussion of manipulation. We agreed that if one organism could get away with manipulating the nervous system of another, and exploiting its muscle power, selection would favour such manipulation. But we were brought up short by the reflection that selection would also favour resistance to being manipulated. Should we, then, really expect to see effective manipulation in nature? The life/dinner principle, and other such principles as the rare-enemy effect, provide us with an answer. If the individual manipulator has more to lose by failing to manipulate than the individual victim has to lose by failing to resist manipulation, we should expect to see successful manipulation in nature. We should expect to see animals working in the interests of other animals’ genes.

Brood parasitism provides what may be the most striking example. A parent bird such as a reed warbler sweeps a copious flow of food from a large catchment area into the narrow funnel of its nest. There is a living to be made by any creature that evolves the necessary adaptations to insert itself in the funnel and intercept the flow. That is what cuckoos and other brood parasites have done. But the reed warbler is not an uncomplaining
cornucopia of free food. It is an active, complex machine, with sense organs, muscles and a brain. The brood parasite must not only have its body inserted in the host’s nest. It must also infiltrate the defences of the host’s nervous system, and its ports of entry are the host’s sense organs. The cuckoo uses key stimuli to unlock the host’s machinery of parental care and subvert it.

The advantages of the brood-parasite way of life are so manifest that today we are taken aback to find Hamilton and Orians needing, in 1965, to defend the proposition that it has been favoured by natural selection, against theories of ‘degenerative breakdown’ of normal breeding behaviour. Hamilton and Orians went on to provide a satisfying discussion of the probable evolutionary origins of brood parasitism, the preadaptations which preceded its evolution, and the adaptations which have accompanied its evolution.

One of these adaptations is egg mimicry. The perfection of egg mimicry, in at least some ‘gentes’ of cuckoo, shows that foster parents are potentially capable of keen-eyed discrimination against interlopers. This only underlines the mystery of why cuckoo hosts seem to be so poor at discriminating against cuckoo nestlings. Hamilton and Orians (1965) express the problem vividly: ‘Young brown-headed cowbirds and European Cuckoos, as they reach their maximum dimension, dwarf their foster parents. Consider the ludicrous sight of a tiny Garden Warbler … [Latin name leaves exact species intended unclear] standing atop a cuckoo to reach the mouth of the gaping parasite. Why does not the Garden Warbler take the adaptive measure of abandoning the nestling prematurely, especially when to the human observer it is so clearly identifiable?’ When a parent is a small fraction of the size of the nestling it is feeding, the most rudimentary eyesight should suffice to show that something has gone seriously wrong with the normal parental process. Yet, at the same time, the existence of egg mimicry shows that hosts are capable of fastidious discrimination, making use of keen eyesight. How are we to explain this paradox (see also Zahavi 1979)?

One fact that helps to reduce the mystery is that there must be stronger selection pressure on hosts to discriminate against cuckoos at the egg stage than against cuckoos at the nestling stage, simply because eggs occur earlier. The benefit of detecting a cuckoo egg is the potential gaining of an entire breeding cycle in the future. The benefit of detecting a nearly fledged cuckoo is the saving of only a few days, at a time when it may be too late to breed again anyway. Another mitigating circumstance in the case of
Cuculus canorus
(Lack 1968) is that the host’s own young is usually not there for simultaneous comparison, having been tipped out by the baby cuckoo. It is well known that discrimination is easier if there is a model actually present for comparison.

Various authors have invoked the ‘supernormal stimulus’, in one form or another. Thus Lack remarks (p. 88) that ‘the young cuckoo, with its huge
gape and loud begging call, has evidently evolved in exaggerated form the stimuli which elicit the feeding response of parent passerine birds. So much is this so that there are many records of adult passerine birds feeding a fledged young
C. canorus
raised by a different host species; this, like lipstick in the courtship of mankind, demonstrates successful exploitation by means of a “super-stimulus”.’ Wickler (1968) makes a similar point, quoting Heinroth as having referred to foster parents as behaving like ‘addicts’, and to the cuckoo nestling as a ‘vice of its foster parents’. As it stands, this kind of suggestion will strike many critics as unsatisfying, because it immediately prompts a question at least as big as the one it answers. Why doesn’t selection eliminate from the host species the tendency to be ‘addicted’ to ‘supernormal stimuli’?

This, of course, is where the arms race concept comes in again. When a human behaves in a way that is manifestly bad for him, for instance when he continually takes poison, we may explain his behaviour in at least two ways. He may not realize that the substance that he is drinking is poison, so closely does it resemble a genuinely nutritous substance. This corresponds to the host bird’s being fooled by the cuckoo’s egg mimicry. Or he may be unable to save himself because of some direct subverting influence of the poison on his nervous system. Such is the case of the heroin addict who knows the drug is killing him, but who cannot stop taking it because the drug itself controls his nervous system. We have already seen that the cuckoo nestling’s lipstick-like gape is regarded as a supernormal stimulus, and that foster parents have been described as apparently ‘addicted’ to the supernormal stimulus. Could it be that the host can no more resist the supernormal manipulative power of the cuckoo nestling than the junkie can resist his fix, or than the brainwashed prisoner can resist the orders of his captor, however much it would benefit him to do so? Perhaps cuckoos have put their adaptive emphasis on mimetic deception at the egg stage, but on positive manipulation of the host’s nervous system at the late nestling stage.

Any nervous system can be subverted if treated in the right way. Any evolutionary adaptation of the host nervous system to resist manipulation by cuckoo nestlings lays itself open to counter-adaptation by the cuckoos. Selection acting on cuckoos will work to find whatever chinks there may be in the hosts’ newly evolved psychological armour. Host birds may be very good at resisting psychological manipulation, but cuckoos might become even better at manipulating. All we need to postulate is that, for some reason such as that suggested by the life/dinner principle or the rare-enemy effect, cuckoos have won the arms race: a cuckoo in the nest has
got
to manipulate its host successfully or it will surely die; its individual foster-parent will benefit somewhat if it resists manipulation, but it still has a good chance of future reproductive success in other years even if it fails to resist this particular cuckoo. Moreover, cuckoos might be sufficiently rare that the risk
of an individual of the foster species being parasitized is low; conversely the ‘risk’ of an individual cuckoo’s being a parasite is 100 per cent, no matter how common or rare either party to the arms race may be. The cuckoo is descended from a line of ancestors, every single one of whom has successfully fooled a host. The host is descended from a line of ancestors, many of whom may never have encountered a cuckoo in their lives, or may have reproduced successfully after being parasitized by a cuckoo. The arms race concept completes the classical supernormal stimulus explanation, by providing a functional account of the host’s maladaptive behaviour, instead of leaving it as an unexplained limitation of the nervous system.

In one respect my treatment of cuckoos as manipulators may be found unsatisfying. The cuckoo is, after all, only diverting the normal parental behaviour of its host. It has not succeeded in building into the host’s behavioural repertoire a whole new behaviour pattern that was not there, in some form, before. Some might find analogies with drugs, hypnotism and electrical stimulation of the brain more persuasive if an example of this more extreme kind of manipulation could be found. A possible case is the ‘preening invitation’ display of another brood parasite, the brown-headed cowbird
Molothrus ater
(Rothstein 1980). Allopreening, the preening of one individual by another, is not uncommon within various species of birds. It is not particularly surprising, therefore, that cowbirds should succeed in getting other birds of several species to preen them. Again, this can be seen as a simple diversion of intraspecific allopreening, with the cowbird providing a supernormal exaggeration of the normal eliciting stimuli for allopreening. What
is
rather surprising is that cowbirds manage to get themselves preened by species that never engage in intraspecific allopreening.

The drug analogy is especially apt for insect ‘cuckoos’ that use chemical means to coerce their hosts into acts that are profoundly damaging to their own inclusive fitness. Several species of ant have no workers of their own. The queens invade nests of other species, dispose of the host queen, and use the host workers to bring up their own reproductive young. The method of disposing of the host queen varies. In some species, such as the descriptively named
Bothriomyrmex regicidus
and
B. decapitans
, the parasite queen rides about on the back of the host queen and then, in Wilson’s (1971) delightful description, ‘begins the one act for which she is uniquely specialized: slowly cutting off the head of her victim’ (p. 363).

Monomorium santschii
achieves the same result by more subtle means. The host workers have weapons wielded by strong muscles, and nerves attached to the muscles; why should the parasite queen exert her own jaws if she can subvert the nervous systems controlling the numerous jaws of the host workers? It does not seem to be known how she achieves it, but she does: the host workers kill their own mother and adopt the usurper. A chemical
secreted by the parasite queen seems the likely weapon, in which case it might be labelled a pheromone, but it is probably more illuminating to think of it as a formidably powerful drug. In line with this interpretation, Wilson (1971, p. 413) writes of symphylic substances as being ‘more than just elementary nutritive substances or even analogues of the natural host pheromones. Several authors have spoken of a narcotizing effect of symphylic substances.’ Wilson also uses the word ‘intoxicant’ and quotes a case in which worker ants under the influence of such a substance became temporarily disoriented and less sure of their footing.

Those who have never been brainwashed or addicted to a drug find it hard to understand their fellow men who are driven by such compulsions. In the same naive way we cannot understand a host bird’s being compelled to feed an absurdly oversized cuckoo, or worker ants wantonly murdering the only being in the whole world that is vital to their genetic success. But such subjective feelings are misleading, even where the relatively crude achievements of human pharmacology are concerned. With natural selection working on the problem, who would be so presumptious as to guess what feats of mind control might not be achieved? Do not expect to see animals always behaving in such a way as to maximize their own inclusive fitness. Losers in an arms race may behave in some very odd ways indeed. If they appear disoriented and unsure of their footing, this may be only the beginning.