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Authors: Richard Dawkins

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The slaves are, of course, blissfully ignorant of the fact that they are unrelated to the queen and to the brood that they are tending. Unwittingly they are rearing new platoons of slave-makers. No doubt natural selection, acting on the genes of the slave species, tends to favour anti-slavery adaptations. However, these are evidently not fully effective because slavery is a wide spread phenomenon.

 

The consequence of slavery that is interesting from our present point of view is this. The queen of the slave-making species is now in a position to bend the sex ratio in the direction she 'prefers'. This is because her own true-born children, the slavers, no longer hold the practical power in the nurseries. This power is now held by the slaves. The slaves 'think' they are looking after their own siblings and they are presumably doing whatever would be appropriate in their own nests to achieve their desired 3:1 bias in favour of sisters. But the queen of the slave-making species is able to get away with countermeasures and there is no selection operating on the slaves to neutralize these counter-measures, since the slaves are totally unrelated to the brood.

 

For example, suppose that in any ant species, queens 'attempt' to disguise male eggs by making them smell like female ones. Natural selection will normally favour any tendency by workers to 'see through' the disguise. We may picture an evolutionary battle in which queens continually 'change the code', and workers 'break the code'. The war will be won by whoever manages to get more of her genes into the next generation, via the bodies of the reproductives. This will normally be the workers, as we have seen. But when the queen of a slave-making species changes the code, the slave workers cannot evolve any ability to break the code. This is because any gene in a slave worker 'for breaking the code' is not represented in the body of any reproductive individual, and so is not passed on. The reproductives all belong to the slave-making species, and are kin to the queen but not to the slaves. If the genes of the slaves find their way into any reproductives at all, it will be into the reproductives that emerge from the original nest from which they were kidnapped. The slave workers will, if anything, be busy breaking the wrong code! Therefore, queens of a slave-making species can get away with changing their code freely, without there being any danger that genes for breaking the code will be propagated into the next generation.

 

The upshot of this involved argument is that we should expect in slave-making species that the ratio of investment in reproductives of the two sexes should approach 1:1 rather than 3:1. For once, the queen will have it all her own way. This is just what Trivers and Hare found, although they only looked at two slave-making species.

 

I must stress that I have told the story in an idealized way. Real life is not so neat and tidy. For instance, the most familiar social insect species of all, the honey bee, seems to do entirely the 'wrong' thing. There is a large surplus of investment in males over queens- something that does not appear to make sense from either the workers' or the mother queen's point of view. Hamilton has offered a possible solution to this puzzle. He points out that when a queen bee leaves the hive she goes with a large swarm of attendant workers, who help her to start a new colony. These workers are lost to the parent hive, and the cost of making them must be reckoned as part of the cost of reproduction: for every queen who leaves, many extra workers have to be made. Investment in these extra workers should be counted as part of the investment in reproductive females. The extra workers should be weighed in the balance against the males when the sex ratio is computed. So this was not a serious difficulty for the theory after all.

 

A more awkward spanner in the elegant works of the theory is the fact that, in some species, the young queen on her mating flight mates with several males instead of one. This means that the average relatedness among her daughters is less than 3/4, and may even approach 1/4 in extreme cases. It is tempting, though probably not very logical, to regard this as a cunning blow struck by queens against workers! Incidentally, this might seem to suggest that workers should chaperone a queen on her mating flight, to prevent her from mating more than once. But this would in no way help the workers' own genes-only the genes of the coming generation of workers. There is no trade-union spirit among the workers as a class. All that each one of them 'cares' about is her own genes. A worker might have 'liked' to have chaperoned her own mother, but she lacked the opportunity, not having been conceived in those days. A young queen on her mating flight is the sister of the present generation of workers, not the mother. Therefore they are on her side rather than on the side of the next generation of workers, who are merely their nieces. My head is now spinning, and it is high time to bring this topic to a close.

 

I have used the analogy of farming for what hymenopteran workers do to their mothers. The farm is a gene farm. The workers use their mother as a more efficient manufacturer of copies of their own genes than they would be themselves. The genes come off the production line in packages called reproductive individuals. This farming analogy should not be confused with a quite different sense in which the social insects may be said to farm. Social insects discovered, as man did long after, that settled cultivation of food can be more efficient than hunting and gathering.

 

For example, several species of ants in the New World, and, quite independently, termites in Africa, cultivate 'fungus gardens'. The best known are the so-called parasol ants of South America. These are immensely successful. Single colonies with more than two million individuals have been found. Their nests consist of huge spreading underground complexes of passages and galleries going down to a depth of ten feet or more, made by the excavation of as much as 40 tons of soil. The underground chambers contain the fungus gardens. The ants deliberately sow fungus of a particular species in special compost beds which they prepare by chewing leaves into fragments. Instead of foraging directly for their own food, the workers forage for leaves to make compost. The 'appetite' of a colony of parasol ants for leaves is gargantuan. This makes them a major economic pest, but the leaves are not food for themselves but food for their fungi. The ants eventually harvest and eat the fungi and feed them to their brood. The fungi are more efficient at breaking down leaf material than the ants' own stomachs would be, which is how the ants benefit by the arrangement. It is possible that the fungi benefit too, even though they are cropped: the ants propagate them more efficiently than their own spore dispersal mechanism might achieve. Furthermore, the ants 'weed' the fungus gardens, keeping them clear of alien species of fungi. By removing competition, this may benefit the ants' own domestic fungi. A kind of relationship of mutual altruism could be said to exist between ants and fungi. It is remarkable that a very similar system of fungus farming has evolved independently, among the quite unrelated termites.

 

Ants have their own domestic animals as well as their crop plants. Aphids-greenfly and similar bugs-are highly specialized for sucking the juice out of plants. They pump the sap up out of the plants' veins more efficiently than they subsequently digest it. The result is that they excrete a liquid that has had only some of its nutritious value extracted. Droplets of sugar-rich 'honeydew' pass out of the back end at a great rate, in some cases more than the insect's own body-weight every hour. The honeydew normally rains down on to the ground-it may well have been the providential food known as 'manna' in the Old Testament. But ants of several species intercept it as soon as it leaves the bug. The ants 'milk' the aphids by stroking their hind-quarters with their feelers and legs. Aphids respond to this, in some cases apparently holding back their droplets until an ant strokes them, and even withdrawing a droplet if an ant is not ready to accept it. It has been suggested that some aphids have evolved a backside that looks and feels like an ant's face, the better to attract ants. What the aphids have to gain from the relationship is apparently protection from their natural enemies. Like our own dairy cattle they lead a sheltered life, and aphid species that are much cultivated by ants have lost their normal defensive mechanisms. In some cases ants care for the aphid eggs inside their own underground nests, feed the young aphids, and finally, when they are grown, gently carry them up to the protected grazing grounds.

 

A relationship of mutual benefit between members of different species is called mutualism or symbiosis. Members of different species often have much to offer each other because they can bring different 'skills' to the partnership. This kind of fundamental asymmetry can lead to evolutionarily stable strategies of mutual cooperation. Aphids have the right sort of mouthparts for pumping up plant sap, but such sucking mouthparts are no good for self-defence. Ants are no good at sucking sap from plants, but they are good at fighting. Ant genes for cultivating and protecting aphids have been favoured in ant gene-pools. Aphid genes for cooperating with the ants have been favoured in aphid gene-pools.

 

Symbiotic relationships of mutual benefit are common among animals and plants. A lichen appears superficially to be an individual plant like any other. But it is really an intimate symbiotic union between a fungus and a green alga. Neither partner could live

 

without
the other. If their union had become just a bit more intimate we would no longer have been able to tell that a lichen was a double organism at all. Perhaps then there are other double or multiple organisms which we have not recognized as such. Perhaps even we ourselves?

 

Within each one of our cells there are numerous tiny bodies called mitochondria. The mitochondria are chemical factories, responsible for providing most of the energy we need. If we lost our mitochondria we would be dead within seconds. Recently it has been plausibly argued that mitochondria are, in origin, symbiotic bacteria who joined forces with our type of cell very early in evolution. Similar suggestions have been made for other small bodies within our cells. This is one of those revolutionary ideas which it takes time to get used to, but it is an idea whose time has come. I speculate that we shall come to accept the more radical idea that each one of our genes is a symbiotic unit. We are gigantic colonies of symbiotic genes. One cannot really speak of 'evidence' for this idea, but, as I tried to suggest in earlier chapters, it is really inherent in the very way we think about how genes work in sexual species. The other side of this coin is that viruses may be genes who have broken loose from 'colonies' such as ourselves. Viruses consist of pure DNA (or a related self-replicating molecule) surrounded by a protein jacket. They are all parasitic. The suggestion is that they have evolved from 'rebel' genes who escaped, and now travel from body to body directly through the air, rather than via the more conventional vehicles-sperms and eggs. If this is true, we might just as well regard ourselves as colonies of viruses! Some of them cooperate symbiotically, and travel from body to body in sperms and eggs. These are the conventional 'genes'. Others live parasitically, and travel by whatever means they can. If the parasitic DNA travels in sperms and eggs, it perhaps forms the 'paradoxical' surplus of DNA which I mentioned in Chapter 3. If it travels through the air, or by other direct means, it is called 'virus' in the usual sense.

 

But these are speculations for the future. At present we are concerned with symbiosis at the higher level of relationships between many-celled organisms, rather than within them. The word symbiosis is conventionally used for associations between members of different species. But, now that we have eschewed the 'good of the species' view of evolution, there seems no logical reason to distinguish associations between members of different species as things apart from associations between members of the same species. In general, associations of mutual benefit will evolve if each partner can get more out than he puts in. This is true whether we are speaking of members of the same hyena pack, or of widely distinct creatures such as ants and aphids, or bees and flowers. In practice it may be difficult to distinguish cases of genuine two-way mutual benefit from cases of one-sided exploitation.

 

The evolution of associations of mutual benefit is theoretically easy to imagine if the favours are given and received simultaneously, as in the case of the partners who make up a lichen. But problems arise if there is a delay between the giving of a favour and its repayment. This is because the first recipient of a favour may be tempted to cheat and refuse to pay it back when his turn comes. The resolution of this problem is interesting and is worth discussing in detail. I can do this best in terms of a hypothetical example.

 

Suppose a species of bird is parasitized by a particularly nasty kind of tick which carries a dangerous disease. It is very important that these ticks should be removed as soon as possible. Normally an individual bird can pull off its owns ticks when preening itself. There is one place, however-the top of the head-which it cannot reach with its own bill. The solution to the problem quickly occurs to any human. An individual may not be able to reach his own head, but nothing is easier than for a friend to do it for him. Later, when the friend is parasitized himself, the good deed can be paid back. Mutual grooming is in fact very common in both birds and mammals.

 

This makes immediate intuitive sense. Anybody with conscious foresight can see that it is sensible to enter into mutual back-scratching arrangements. But we have learnt to beware of what seems intuitively sensible. The gene has no foresight. Can the theory of selfish genes account for mutual back-scratching, or 'reciprocal altruism', where there is a delay between good deed and repayment? Williams briefly discussed the problem in his 1966 book, to which I have already referred. He concluded, as had Darwin, that delayed reciprocal altruism can evolve in species that are capable of recognizing and remembering each other as individuals. Trivers, in 1971, took the matter further. When he wrote, he did not have available to him Maynard Smith's concept of the evolutionarily stable strategy. If he had, my guess is that he would have made use of it, for it provides a natural way to express his ideas. His reference to the 'Prisoner's Dilemma'-a favourite puzzle in game theory- shows that he was already thinking along the same lines.

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