Reproduction: the almost forgotten currency of fitness

When an animal behaves in a manner that reduces its Darwinian fitness and increases the fitness of another individual, it is said to behave altruistically. The existence of such altruism in nature is paradoxical because natural selection would normally be expected to eliminate individuals who lower their own fitness. Much theoretical and empirical work is therefore devoted to unravelling the mechanism/s by which altruism may be favoured by natural selection. Social insects such as ants, bees and wasps are at the forefront of this research since their colonies often consist of one or a small number of fertile queens and a large number of apparently sterile workers. The European wasp Polistes dominulus (Figure 1) has been an especially favourite model system for such studies. P. dominulus is one of the most common social wasps in Europe and having been recently introduced into the United States, it has begun to rapidly displace local social wasps there. Its commonness and wide distribution have conferred on it the distinction of being one of the best-studied social wasps, certainly the best-studied Polistes. Groups of inseminated females found new nests in the Spring and cooperatively rear brood. The female wasps in a colony organize themselves into a behavioural dominance hierarchy such that only the alpha individual (the queen) reproduces, while the rest appear to function as apparently altruistic, sterile subordinates (workers), building the nest, foraging for food and pulp, feeding and caring for the brood and generally doing all that it takes to keep the nest up and running. But wait a minute, what’s in it for the workers? Why should they sacrifice their time and energy helping to rear the queen’s brood? Why not go off, found their own nests and rear their own brood – something they are quite capable of? Surely there must be something wrong with our facts. Let us look more closely. Maybe the subordinates lay some of their own eggs after all, at least enough to compensate for the offspring they might have produced in their own nests. Looking closely is precisely what Leadbeater et al. have done in a recent study. Using nine microsatellite markers to genotype pupae from 228 natural nests of P. dominulus from Spain, they measured the direct reproductive success of 1113 foundresses. Lo and behold, subordinate foundresses were seen to produce more offspring per capita than an average solitary foundress who had indeed decided to reproduce on her own. About 32% of the reproduction of subordinates came from sneaking in eggs while the dominant was still alive and 68% came from inheriting the position of the dominant in the nest after the latter had died. Thus the obvious experiment has been done and the expected result has been obtained and, of course, there is no mysterious altruism after all. But then, what is all the fuss about? Well, I think we should make a great deal of fuss about this study. Indeed, I recommend that this paper be widely read, discussed and emulated. To see why, let us flash back to 1964. That was the year in which Hamilton proposed a radically new theory which is often referred to as kin selection or inclusive fitness theory. Hamilton argued that to deal with the apparent paradox of altruism, we must expand the scope of Darwinian fitness and add to the already existing direct component, gained through personal reproduction, an indirect component gained through aiding close genetic relatives. He dubbed the sum of the direct and indirect components as inclusive fitness. Hamilton went on to derive a rule according to which an altruistic allele will be favoured by natural selection if rb > c, where r is the relatedness between the altruist and the recipient of altruism, b is the benefit accrued to the recipient and c is the cost incurred by the altruist. Unfortunately Hamilton’s rule has not been put to as rigorous an empirical test as one might have liked – costs and benefits are hard to measure although relatedness has turned out to eminently measurable. When r, b and c have all been measured as in the Indian paper wasp, Ropalidia marginata, for example, the importance of all the three parameters has become evident and Hamilton’s rule has provided a satisfactory explanation for the evolution of altruism. However, rather than take the trouble of measuring all three parameters, it has often been implicitly or explicitly argued that if b is sufficiently greater than c, then it is r that must drive the evolution of altruism. All this has led willy-nilly to the emergence of the corollary that altruism can evolve if it is nepotistic, i.e. directed to individuals with high genetic relatedness. Although it is clear from Hamilton’s rule that what is high relatedness depends on the relative magnitudes of the costs and benefits, it has become customary not to raise your eyebrows at the evidence of altruism, as long as relatedness between