The Extended Phenotype: The Long Reach of the Gene (Popular Science) (16 page)

Let me stress again what a feat of mind-control the
Monomorium santschii
queen achieves. To a sterile worker ant, her mother is a kind of genetic gold-mine. For a worker ant to kill her own mother is an act of genetic madness. Why do the workers do it? I am sorry I can do no more than, once again, vaguely talk about arms races. Any nervous system is vulnerable to manipulation by a clever-enough pharmacologist. There is no difficulty in believing that natural selection acting on
M. santschii
would seek out the weak points in the host workers’ nervous system, and insert a pharmacological key in the lock. Selection on the host species would soon have plugged those weak points, whereupon selection on the parasite would improve the drug, and the arms race was under way. If
M. santschii
is sufficiently rare, it is easy to see that it might ‘win’ the arms race, even though regicide is such a disastrous act for each host colony whose workers succumb to it. The overall risk of parasitization by
M. santschii
could be very low even though the marginal cost of regicide, given that an
M. santschii
queen has entered, is disastrously high. Each individual
M. santschii
queen is descended from a line of ancestors every one of whom has succeeded in manipulating host workers into regicide. Each host worker is descended from a line of ancestors whose colonies may seldom have been within 10 miles of an
M. santschii
queen. The costs of ‘bothering’ to be equipped to
resist manipulation by an occasional
M. santschii
queen may outweigh the benefits. Reflections such as this lead me to believe that the hosts might well lose the arms race.

Other species of parasitic ants use a different system. Instead of sending out queens to implant their eggs in host nests and using host labour there, they transport host labour back to their own nests. These are the so-called slavemaking ants. Slavemaking species have workers, but these workers devote part, or in some cases all, of their energy to going on slaving expeditions. They raid nests of other species and carry off larvae and pupae. These subsequently hatch in the slavers’ nest, where they work normally, foraging and tending brood, not ‘realizing’ that they are, in effect, slaves. The advantage of the slavemaking way of life is presumably that most of the cost of feeding the workforce in the larval stage is saved. That cost is borne by the home colony from which the slave pupae were taken.

The slavemaking habit is interesting from the present point of view, because it raises an unusual arms race asymmetry. Presumably there is an arms race between slavemaking species and slave species. Adaptations to counter slavery, for instance enlarged soldier jaws for driving off slave-raiders, should be expected in species that are victims of slave raids. But surely the more obvious countermeasure the slaves could take would simply be to withhold their labour in the slavers’ nest, or to kill slavemaker brood instead of feeding them? It
seems
the obvious countermeasure, but there are formidable obstacles to its evolution. Consider an adaptation to ‘go on strike’, to refuse to work in the slavemakers’ nest. The slave workers would of course have to have some means of recognizing that they had hatched in a foreign nest, but that should not be difficult in principle. The problem arises when we think in detail of how the adaptations would be passed on.

Since workers don’t reproduce, all worker adaptations, in any social insect species, have to be passed on by reproductive relatives of the workers. This normally presents no insuperable problems, because workers directly assist their own reproductive relatives, so genes giving rise to worker adaptations directly assist copies of themselves in reproductives. But take the example of a mutant gene causing slave workers to go on strike. It may very effectively sabotage the slavemakers’ nest, possibly wipe it out altogether. And to what effect? The area now contains one less slavemaking nest, presumably a good thing for
all
potential victim nests in the area, not just the nest from which the rebel slaves came, but nests containing non-striking genes as well. The same kind of problem arises in the general case of the spread of ‘spiteful’ behaviour (Hamilton 1970; Knowlton & Parker 1979).

The only easy way the genes for striking can be preferentially passed on is for striking to benefit, selectively, the strikers’ own home nest, the nest they left behind and in which their own reproductive relatives are being reared. This could happen if slavemakers habitually returned to make repeat raids
on the same nest, but otherwise we must conclude that anti-slavery adaptations must be confined to the period
before
the slave pupae have left their home nest. Once the slaves have arrived in the slavemakers’ nest they effectively drop out of the arms race since they no longer have any power to influence the success of their reproductive relatives. The slavemakers can develop manipulative adaptations of any degree of sophistication, physical or chemical, pheromones or powerful drugs, and the slaves cannot evolve countermeasures.

Actually, the very fact that the slaves cannot evolve countermeasures will tend to reduce the likelihood that the manipulative techniques evolved by the slavemakers will be very sophisticated: the fact that the slaves cannot retaliate, in an evolutionary sense, means that the slavemakers do not need to spend costly resources on elaborate and sophisticated manipulation adaptations, because simple and cheap ones will do. The example of slavery in ants is rather a special one, but it illustrates a particularly interesting sense in which one side in an arms race can be said to lose completely.

A case could be made for drawing an analogy here with the hybrid frog
Rana esculenta
(White 1978). This common European frog, the edible frog of French restaurants, is not a species in the normal sense of the word. Individuals of the ‘species’ are really various kinds of hybrids between two other species,
Rana ridibunda
and
R. lessonae
. There are two different diploid forms and two different triploid forms of
R. esculenta
. For simplicity I shall consider only one of the diploid forms, but the argument holds for all the varieties. These frogs coexist with
R. lessonae
. Their diploid karyotype consists of one set of
lessonae
chromosomes and one set of
ridibunda
chromosomes. At meiosis they discard the
lessonae
chromosomes and produce pure
ridibunda
gametes. They mate with
lessonae
individuals, thereby restoring the hybrid genotype in the next generation. In this race of
Rana esculenta
bodies, therefore,
ridibunda
genes are germ-line replicators,
lessonae
genes dead-end ones. Dead-end replicators can exert phenotypic effects. They can even be naturally selected. But the consequences of that natural selection are irrelevant to evolution (see
Chapter 5
). To make the next paragraph easier to follow, I shall call
R. esculenta
H (for hybrid),
R. ridibunda
G (for germ-line) and
R. lessonae
D (for dead-end, although it should be remembered that ‘D’ genes are dead-end replicators only when in H frogs; when in ‘D’ frogs they are normal germ-line replicators).

Now, consider a gene in the D gene-pool which exerts an effect on D bodies to make them refuse to mate with H. Such a gene should be favoured by natural selection over its H-tolerating allele, since the latter will tend to end up in H bodies of the next generation, and will be discarded at meiosis. G genes are not discarded at meiosis, and they will tend to be selected if they influence H bodies so that they overcome the reluctance of D individuals to mate with them. We should therefore see an arms race between G genes
acting on H bodies, and D genes acting on D bodies. In those respective bodies, both sets of genes are germ-line replicators. But what about D genes acting on H bodies? They should have just as powerful an influence over H phenotypes as G genes, since they constitute exactly half of the H genome. Naively, we might expect them to carry their arms race against G genes over into the H bodies which they share. But in H bodies, those D genes are in the same position as ants that have been taken as slaves. Any adaptation that they mediate in the H body cannot be passed on to the next generation; for the gametes produced by the H individual, regardless of how his developing phenotype, and indeed his survival, may have been influenced by D genes, are strictly G gametes. Just as would-be slave ants can be selected to resist being taken into captivity while they are still in their home nest, but cannot be selected to subvert the slavemaking nest once they are in it, so D genes can be selected to influence D bodies so that they resist being incorporated in H genomes in the first place, but once so incorporated they are no longer under selection, even though they can still have phenotypic effects. They lose the arms race because they are a dead-end. A similar argument could be made for fish of the hybrid ‘species’
Poeciliopsis monacha-occidentalis
(Maynard Smith 1978a).

The inability of slaves to evolve counter-adaptations was originally invoked by Trivers and Hare (1976), in their theory of the sex-ratio arms race in social Hymenoptera. This is one of the best known of recent discussions of a particular arms race, and it is worth considering further. Elaborating on ideas of Fisher (1930a) and Hamilton (1972), Trivers and Hare reasoned that the evolutionarily stable sex ratio in ant species with one singly mated queen per nest cannot be simply predicted. If the queen is assumed to have all power over the sex of reproductive offspring (young queens and males), the stable ratio of economic investment in male and female reproductives is 1:1. If, on the other hand, non-laying workers are assumed to hold all power over investment in young, the stable ratio will be 3:1 in favour of females, ultimately because of the haplodiploid genetic system. There is, therefore, a potential conflict between queen and workers. Trivers and Hare reviewed the, admittedly imperfect, available data, and reported a good average fit to the 3:1 prediction, from which they concluded that they had found evidence for worker power winning the battle against queen power. It was a clever attempt to use real data to test a hypothesis of a kind that is often criticized as untestable, but like other innovative first attempts it is easy to find fault with it. Alexander and Sherman (1977) complained about Trivers and Hare’s handling of the data, and also suggested an alternative explanation for the female-biased sex ratio common in ants. Their explanation (‘local mate competition’), like that of Trivers and Hare, was originally derived from Hamilton, in this case his paper on extraordinary sex ratios (1967).

This controversy has had the good effect of stimulating further work.
Especially illuminating in the context of arms races and manipulation is the paper by Charnov (1978), which is concerned with the origins of eusociality, and which introduces a potentially important version of the life/dinner principle. His argument works for diploid as well as haplodiploid organisms, and I shall consider the diploid case first. Consider a mother whose elder children have still not left the nest when the next brood hatches. When the time comes for them to leave the nest and begin their own reproduction, the young have the option, instead, of staying behind and helping to rear their young siblings. As is now well known, all other things being equal such a fledgling should be genetically indifferent between rearing offspring and rearing full siblings (Hamilton 1964a,b). But suppose the old mother could exert any manipulative power over the decision of her elder children: would she ‘prefer’ that they leave and rear families of their own, or stay and rear her next brood? Obviously that they should stay and rear her next brood, since grandchildren are half as valuable to her as children. (The argument as it stands is incomplete. If she manipulated
all
her children for the whole of her life into rearing yet more non-producing child labourers, her germ-line would peter out. We must assume that she manipulates some offspring of the same genetic type into developing into reproductives and others into developing as workers.) Selection will, then, favour such manipulative tendencies in parents.

Normally, when we postulate selection in favour of manipulation we dutifully pay lip service to counter-selection on the victim to resist manipulation. The beauty of Charnov’s point is that in this case there will be no counter-selection. The ‘arms race’ is a walk-over because one side, so to speak, doesn’t even try. The offspring being manipulated are, as we have already seen, indifferent to whether they rear young siblings or offspring of their own (again assuming all other things equal). Therefore, although we may
postulate
reverse manipulation by offspring of parents, this is bound, at least in the simple example visualized by Charnov, to be outweighed by parental manipulation of offspring. This is an asymmetry to be added to the list of parental advantages offered by Alexander (1974), but I find it more generally convincing than any others on the list.

At first sight it might appear that Charnov’s argument does not apply to haplodiploid animals, and that would be a pity since most social insects are haplodiploid. But this view is mistaken. Charnov himself shows this for the special assumption that the population has an unbiased sex ratio, in which case even in haplodiploid species females are indifferent between rearing siblings (
r
= the average of ¾ and ¼) and rearing offspring (
r
= ½). But Craig (1980) and Grafen (in preparation) independently show that Charnov did not even need to assume an unbiased sex ratio. The potential worker is
still
indifferent between rearing siblings and rearing offspring at any conceivable population sex ratio. Thus suppose the population sex ratio is female-biased,
even suppose it conforms to Trivers and Hare’s predicted 3:1. Since the worker is more closely related to her sister than to her brother or her offspring of either sex, it might seem that she would ‘prefer’ to rear siblings over offspring given such a female-biased sex ratio: is she not gaining mostly valuable sisters (plus only a few relatively worthless brothers) when she opts for siblings? But this reasoning neglects the relatively great reproductive value of males in such a population as a consequence of their rarity. The worker may not be closely related to each of her brothers, but if males are rare in the population as a whole each one of those brothers is correspondingly highly likely to be an ancestor of future generations.