The Extended Phenotype: The Long Reach of the Gene (Popular Science) (17 page)

The mathematics confirm that Charnov’s conclusion is even more general than he suggested. In both diploid and haplodiploid species, at any population sex ratio, an individual female is theoretically indifferent whether she herself rears offspring or younger siblings. She is not, however, indifferent whether her offspring rear their own children or their siblings: she prefers them to rear their siblings (her offspring) over their offspring (her grandchildren). Therefore if there is any question of manipulation in this situation, parental manipulation of offspring is more likely than offspring manipulation of parents.

It might appear that Charnov’s, Craig’s and Grafen’s conclusions radically contradict those of Trivers and Hare on sex ratios in social Hymenoptera. The statement that, at any sex ratio, a female hymenopteran is indifferent between rearing siblings and rearing offspring, sounds tantamount to saying that she is also indifferent to what the sex ratio in her nest is. But this is not so. It is still true that, given the assumption of worker control over investment in male and female reproductives, the resulting evolutionarily stable sex ratio will not be necessarily the same as the evolutionarily stable sex ratio given queen control. In this sense a worker is not indifferent to the sex ratio: she may well work to shift the sex ratio away from what the queen is ‘trying’ to achieve.

Trivers and Hare’s analysis of the exact nature of the conflict between queen and workers over the sex ratio can be extended in ways that further illuminate the concept of manipulation (e.g. Oster & Wilson 1978). The following account is derived from Grafen (in preparation). I shall not anticipate his conclusions in detail, but wish to emphasize one principle which is explicit in his analysis as well as implicit in that of Trivers and Hare. The question is not ‘Has the “best” sex ratio been successfully achieved?’ On the contrary, we make a working assumption that natural selection has produced a result, given some constraints, and then ask what those constraints are (see
Chapter 3
). In the present case we follow Trivers and Hare in recognizing that the evolutionarily stable sex ratio depends crucially upon which parties to the arms race have practical power, but we recognize a wider range of possible dispositions of power than they did. In
effect, Trivers and Hare deduced the consequences of two alternative assumptions about practical power; firstly the assumption that the queen exerts all the power, and secondly the assumption that the workers exert all the power. But many other possible assumptions could be made, and each gives rise to a different prediction of the evolutionarily stable sex ratio. In other parts of their paper, indeed, Trivers and Hare consider some of these, for instance the assumption that workers are able to lay their own male eggs.

Grafen, like Bulmer and Taylor (in preparation), has explored the consequences of assuming that power is
divided
as follows: the queen has absolute power over the sex of the eggs that she lays; the workers have absolute power over feeding the larvae. The workers can thus determine how many of the available female eggs shall develop into queens and how many into workers. They have the power to starve the young of one sex or the other, but they have to work within the constraint of what the queen gives them in the way of eggs. Queens have the power to lay eggs in any sex ratio they choose, including withholding, totally, eggs of one sex or the other. But, once laid, those eggs are at the mercy of the workers. A queen might, for instance, play the strategy (in the game theory sense) of laying only male eggs in a given year. Reluctant as we might expect them to be, the workers have no option but to rear their brothers. The queen, in this case, can preempt certain worker strategies, such as ‘preferentially feed sisters’, simply because she ‘plays’ first. But there are other things workers can do.

Using game theory, Grafen shows that only certain queen strategies are evolutionarily stable replies to particular worker strategies, and only certain worker strategies are evolutionarily stable replies to particular queen strategies. The interesting question is, What are the evolutionarily stable combinations of worker and queen strategies? It turns out that there is more than one answer, and there can be as many as three evolutionarily stable states for a given set of parameters. Grafen’s particular conclusions are not my concern here, although I will remark that they are interestingly ‘counterintuitive’. What is my concern is that the evolutionarily stable state of the model population depends upon the assumptions we make about
power
. Trivers and Hare contrasted two possible absolute assumptions (absolute worker power versus absolute queen power). Grafen investigated one plausible
division
of power (queens have power over eggs, workers over larval feeding). But, as I have already noted, numerous other assumptions about power could be made. Each assumption generates different predictions about evolutionarily stable sex ratios, and tests of the predictions can therefore be regarded as providing evidence about the disposition of power in the nest.

For instance, we might focus our research attention on the exact moment when a queen ‘decides’ whether to fertilize a given egg or not. It is plausible to assume that, since the event takes place within the queen’s own body, that
particular decision is likely to have been selected to benefit the queen’s genes. Plausible it may be, but it is precisely this kind of assumption that the doctrine of the extended phenotype is going to call in question. For the moment, we simply note the possibility that workers might manipulate the queen’s nervous system, by pheromonal or other means, so as to subvert her behaviour in their genetic interests. Similarly, it is worker nerves and muscles that are immediately responsible for feeding the larvae, but we are not, therefore, necessarily entitled to assume that worker limbs move only in the interests of worker genes. As is well known, there is massive pheromonal traffic flow from queen to workers, and it is easy to imagine powerful manipulation of worker behaviour by queens. The point is that each assumption about power which we might make yields a testable prediction about sex ratios, and it is for this insight that we have to thank Trivers and Hare, not for the particular model whose predictions they happened to test.

It is even conceivable, in some Hymenoptera, that males might exert power. Brockmann (1980) is making an intensive study of mud-daubing wasps
Trypoxylon politum
. These are ‘solitary’ (as opposed to truly social) wasps, but they are not always totally alone. As in other sphecids, each female builds her own nest (in this case out of mud), provisions it with paralysed prey (spiders), lays one egg on the prey, then seals up the nest and begins the cycle again. In many Hymenoptera, the female carries a lifetime’s supply of sperm from one brief period of insemination early in life.
T. politum
females, however, copulate frequently throughout adult life. Males haunt female nests, losing no opportunity to copulate with the female on each of her returns to the nest. A male may spend hours at a time sitting passively in the nest, probably helping to guard it against parasites, and fighting with other males who attempt to enter. Unlike most male Hymenoptera then, the male
T. politum
is present at the scene of the action. Might he not, therefore, be potentially in a position to influence the sex ratio, in the same kind of way as has been postulated for worker ants?

If males did exert power, what would we expect the consequences to be? Since a male passes all his genes on to his daughters, and none to his mate’s sons, genes tending to make males favour daughters over sons would be favoured. If males exerted total power, completely determining the sex ratio of their mates’ offspring, the consequence would be odd. No males would be born in the first generation of male power. As a result, in the following year all eggs laid would be unfertilized and therefore male. The population would therefore oscillate violently and then go extinct (Hamilton 1967). If males exerted a limited amount of power, less drastic consequences would follow, the situation being formally analogous to that of the ‘driving X chromosome’ in the normal diploid genetic system (
Chapter 8
). In any case a male hymenopteran, if he found himself in a position to influence the sex ratio of his mate’s children, would be expected to try to do so in a female direction.
He might do this by trying to influence his mate’s decision whether to release sperm from her spermatheca. It is not obvious how he might actually do this, but it is known that honeybee queens take longer over laying a female egg than a male one, perhaps using the extra time to achieve fertilization. It would be interesting to try experimentally interrupting a queen in the middle of egg-laying, to see if the delay increased the chance of a female egg emerging.

Do male T.
politum
show any behaviour that we might suspect of being an attempt at such manipulation, for example do they behave as if trying to prolong egg-laying? Brockmann describes a curious behaviour pattern called ‘holding’. This is seen alternating with copulation during the final minutes before the female lays her egg. In addition to brief copulations throughout the provisioning phase of the nest, the final egg-laying and sealing up of the nest is heralded by a prolonged bout of repeated copulations, which lasts many minutes. The female goes head first into the vertical, organ pipe-shaped mud nest, and pushes her head up into the cluster of paralysed spiders lodged in the top of the nest. Her abdomen is facing the entrance at the bottom of the nest, and in this position the male copulates with her. The female then turns round so that she is head downwards facing out of the nest, and probes the spiders with the tip of her abdomen, as if about to lay an egg. The male meanwhile ‘holds’ her head in his forelegs for about half a minute, grabs her antennae and pulls her downwards away from the spiders. She then turns around and they copulate again. She again turns to probe the spiders with her abdomen, the male again holds her head and drags her down. The whole cycle repeats some half dozen times. Finally, after one especially long bout of head-holding, the female lays her egg.

Once the egg is laid, its sex is determined. We have already considered the hypothetical possibility of worker ants manipulating their mother’s nervous system, forcing her to change her fertilizing decision in their genetic interest. Brockmann’s suggestion is that male
T. politum
might attempt similar subversion, and that the head-holding and dragging behaviour may be a manifestation of their manipulation technique. When the male seizes the female’s antennae and drags her away from the spiders which she is probing with her abdomen, is he forcing a postponement of egg-laying as a means of increasing the chance of the egg’s being fertilized in the oviduct? The plausibility of this suggestion might depend on exactly where the egg is in the female’s body during the time of holding. Or is he, as Dr W. D. Hamilton has suggested to us, blackmailing the female by, in effect, threatening to bite her head off unless she postpones egg-laying until after further copulation? Perhaps he gains by repeated copulations, simply by flooding the female’s internal passages with his sperm, thereby raising the chance that the egg will encounter a sperm without one being deliberately released from the spermatheca by the female. Clearly these are just suggestions for further
research, and Brockmann, together with Grafen and others, is following them up. Preliminary indications, I understand, do not support the hypothesis that males actually succeed in exerting power over the sex ratio.

This chapter is intended to begin the process of undermining the reader’s confidence in the central theorem of the selfish organism. That theorem states that individual animals are expected to work for the good of their own inclusive fitness, for the good of copies of their own genes. The chapter has shown that 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. This is not necessarily just a temporary departure from the central theorem, a brief interlude of manipulative exploitation before counterselection on the victim lineage redresses the balance. 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; work hard, energetically, wantonly against their own genetic interests. When we see the members of a species consistently behaving in a certain way, ‘anting’ in birds or whatever it is, we are apt to scratch our heads and wonder how the behaviour benefits the animals’ inclusive fitness. How does it benefit a bird to allow ants to run all through its feathers? Is it using the ants to clean it of parasites, or what? The conclusion of this chapter is that we might instead ask
whose
inclusive fitness the behaviour is benefiting! Is it the animal’s own, or that of some manipulator lurking behind the scenes? In the case of ‘anting’ it does seem reasonable to speculate about advantages to the bird, but perhaps we should give at least a sideways glance at the possibility that it is an adaptation for the good of the ants!

In 1957, Benzer argued that ‘the gene’ could no longer continue as a single, unitary concept. He split it into three: the muton was the minimum unit of mutational change; the recon was the minimum unit of recombination; and the cistron was defined in a way that was directly applicable only to microorganisms, but it was effectively equivalent to the unit responsible for synthesizing one polypeptide chain. I have suggested adding a fourth unit, the
optimon
, the unit of natural selection (Dawkins 1978b). Independently, E. Mayr (personal communication) coined the term ‘selecton’ to serve the same purpose. The optimon (or selecton) is the ‘something’ to which we refer when we speak of an adaptation as being ‘for the good of’ something. The question is, what is that something; what is the optimon?