12.4.3. Maintenance of eusociality — the police state
As we have seen, workers in social hymenopteran colonies forgo their reproduction and raise the brood of their queen, in a system that depends upon kinship — proximity of relatedness — to “justify” their sacrifice. Once non-reproductive castes have evolved (theoretically under conditions of single paternity), the requirement for high relatedness may be relaxed if workers lack any opportunity to reproduce, through mechanisms such as chemical control by the queen. Nonetheless, sporadically, and especially when the influence of the queen wanes, some workers may lay their own eggs. These “non-queen” eggs are not allowed to survive: the eggs are detected and eaten by a “police force” of other workers. This is known from honey bees, certain wasps, and some ants, and may be quite wide- spread although uncommon. For example, in a typical honey-bee hive of 30,000 workers, on average only three have functioning ovaries. Although these individuals are threatened by other workers, they can be responsible for up to 7% of the male eggs in any colony.
Because these eggs lack chemical odors produced by the queen, they can be detected and are eaten by the policing workers with such efficiency that only 0.1% of a honey-bee colony’s males derive from a worker as a mother.
Hamilton’s rule (section 12.4.1) provides an explanation for the policing behavior. The relatedness of a sister to her sister (worker to worker) is r = 0.75, which is reduced to r = 0.375 if the queen has multiply mated (as happens). An unfertilized egg of a worker, if allowed to develop, becomes a son to which his mother’s rel- atedness is r = 0.5. This kinship value is greater than to her half-sisters (0.5 > 0.375), thus providing an incentive to escape queen control. However, from the perspective of the other workers, their kinship to the son of another worker is only r = 0.125, “justifying” the killing of a half-nephew (another worker’s son), and tending the development of her sisters (r = 0.75) or half-sisters (r = 0.375) (relationships portrayed in Fig. 12.11). The evolutionary benefits to any worker derive from raising the queen’s eggs and destroying her sisters’. However, when the queen’s strength wanes or she dies, the pheromonal repression of the colony ceases, anarchy breaks out and the workers all start to lay eggs.
Outside the extreme rigidity of the honey-bee colony, a range of policing activities can be seen. In colonies of ants that lack clear division into queens and workers, a hierarchy exists with only certain individuals’ reproduction tolerated by nestmates. Although enforcement involves violence towards an offender, such regimes have some flexibility, since there is regular ousting of the reproductives. Even for honey bees, as the queen’s performance diminishes and her pheromonal control wanes, workers’ ovaries develop and rampant egg-laying takes place. Workers of some vespids discriminate between offspring of a singly-mated or a promiscuous queen, and behave according to kinship. Presumably, polygynous colonies at some stage have allowed additional queens to develop, or to return and be tolerated, providing possibilities for invasiveness by relaxed inter-nest interactions (Box 1.2). The inquilines discussed in section 12.3 and Box 1.1 evidently evade policing efforts, but the mechanisms are poorly known as yet.
In an unusual development in southern Africa, anarchistic behavior has taken hold in hives of African honey bees (Apis mellifera scutellatus) that are being invaded by a different parasitic subspecies, Cape honey bee (A. m. capensis). The invader workers, which do little work, produce diploid female eggs that are clones of themselves. These evade the regular policing of the colony, presumably by chemical mimicry of the queen pheromone. The colony is destroyed rapidly by these social parasites, which then move on to invade another hive.
(After Whitfield 2002)