For the last two months, I’ve been talking about things that can go wrong in the honey bee colony. Threats to social cohesion. In November, I talked about so-called “royal” subfamilies whose female larvae coerce nurse bees into feeding them royal jelly and rearing them into queens. Last month I talked about “anarchistic” workers who evade the colony’s normal checks on worker reproduction and lay eggs that successfully develop into males. Each is an example of individual selfishness at the expense of the group. Each is a ploy to win a larger slice of the Darwinian pie – more of one’s genes passed on to the next generation. A “royal” worker stands to win the biggest prize of all – the chance to be queen, inherit the brood-rearing factory of her colony, and transmit 50% of her genes with every egg she lays; and “anarchistic” workers, though not as successful as royals, still get to pass on 50% of their genes with every outlaw son they produce. Each outcome is a big improvement over the fate of a law-abiding worker who plods along, helping her mother produce sisters with whom she shares ~30% of genes in common.*1
But these selfish gains come at great cost to the integrity of the colony. Workers who switch to egg-laying invariably stop performing any work for the colony.2 Beekeepers familiar with queenless colonies can attest how quickly a colony deteriorates when its workers give up working.
Anarchistic workers are to their colonies what cancer cells are to a metazoan organism such as humans. And just as higher metazoan bodies have evolved checks on the growth of cancer cells, so the honey bee superorganism has evolved checks on selfish worker egg-laying. These checks take the form of pheromones that queens and brood produce to inhibit worker ovary development, and the workers’ practice of policing – eating each others’ eggs.
When it comes to genetic motives for eating someone’s eggs, kin selection theory offers explanations based on the degrees of relatedness existing in a colony. Figure 1 shows these relationships in a normal European colony. The bottom row, third generation, represents the progeny possibilities for “outlaw” workers – all sons. Theory predicts that a worker would rather help her mother produce more siblings with whom she shares at least 25% of genes in common than help sisters produce nephews with whom she shares only 12.5% genes in common. Although the best pay-out for a worker is to produce a son with whom she shares 50% of her genes, if everyone did this the colony would dissolve. So workers practice mutual policing, the tacit compromise being that passing along ~30% of one’s genes is better than colony collapse and zero reproduction for everybody.
Enter this month the third member of our rogues’ gallery – the Cape bee of South Africa, Apis mellifera capensis. Or more specifically, the workers of A. m. capensis. This bee is a race, or subspecies, of Apis mellifera and cross-fertile with other races. But the workers of this race are well-known for their ability to produce diploid eggs without the need for mating. These eggs are physiologically normal females, capable of being reared into workers or queens in the normal way – depending on whether the larvae are fed royal jelly. Cape workers produce these eggs by a process called parthenogenesis. The process that normally halves chromosome number during egg formation is altered, and the resulting egg not only contains a full dose of chromosomes, but those chromosomes are identical to the mother’s. In other words, a Cape worker’s daughter is virtually a clone of her mother. This has drastic consequences on the relationships in the nest as well as the predictions of kin selection theory, as detailed in Figure 2. A Cape worker is equally related to her subsister (0.25) as to her subsister’s clone daughter (0.25). The same holds true for a supersister (0.75) and the supersister’s clone daughter (0.75). And finally, the queen is equally related to her daughters (0.5) as to her daughters’ daughters (0.5). In short, the genetic incentives for policing have fallen away; with so much clonal inheritance it no longer “mattered” as much to either the queen or a worker if other workers were producing daughters. And indeed, controlled experiments performed by mixing Cape workers with workers of Apis mellifera scutellata (the parent race of the New World’s Africanized bee) show that Cape workers can and do remove eggs laid by scutellata workers, but that neither scutellata3,4 nor Cape3 workers remove eggs laid by Cape workers. In other words, Cape worker eggs are able to evade policing. The most plausible explanation for this is evolved chemical mimicry5 on the part of Cape worker eggs that makes them indistinguishable from queen-laid eggs.
But the absence of policing does not mean that there is no competition in the Cape bee nest. Far from it: the stakes are even higher, but this time kin selection theory is not as helpful because forces are in motion that favor direct, over indirect, inheritance.
Let’s think for a moment about the stakes in this drama. In the case of a European anarchist worker, she stands to pass along 50% of her genes to her son (Fig. 1). In the case of a Cape worker, she stands to pass along 100% of her genes to her clonal daughter (Fig. 2). But because of significant life fate differences, these prizes are not equivalent, even beyond the obvious difference in numbers. The European worker’s son has a realistic, albeit small, chance of mating with a new queen and contributing to the population gene pool. But if the Cape worker’s daughter becomes just another worker, she’s a virtual genetic dead-end: the only way for the Cape worker to win the jackpot is if her daughter becomes the next queen. And because of clonal inheritance, the Cape worker who produces the next queen functionally is the next queen. Thus, for a Cape worker the stakes are the highest they can possibly be: a dead-end versus the biggest prize of all.
More fundamentally however, the real possibility of direct clonal reproduction, passing along 100% of one’s genes, means that altruism – all the work done to promote …
