How societies remain stable in the face of internal conflict is a fundamental question in the study of social evolution. In recent projects, we have explored the occurrence and resolution of social conflict within colonies of the bumble bee, Bombus terrestris.
As in many eusocial Hymenoptera (ants, bees and wasps with a worker caste), workers in B. terrestris are not completely sterile. Some can activate their ovaries and lay eggs. Because of their haplodiploid genetics (by which females arise from fertilised eggs and males from unfertilised eggs), such workers always lay unfertilised eggs yielding males. Workers' reproductive ability raises the question of why workers' selfish production of male eggs does not threaten the social stability of the colony.
A general answer to this question is worker policing, i.e. the repression of workers' reproduction by other workers. Indeed, worker policing in the eusocial Hymenoptera is already recognised as a leading example of how coercion can reduce conflict and so facilitate cooperation and social stability. Worker policing is found in the 'advanced' eusocial, polyandrous (multiply mated) honeybees, in which workers are more closely related to queen- than to worker-produced males. The same association of worker policing and relatedness differences is found, on average, across the eusocial Hymenoptera as a whole.
The occurrence of worker policing in honeybees and the eusocial Hymenoptera in general is therefore as inclusive fitness theory predicts. However, worker policing also occurs in some 'primitively' eusocial species with low mating frequencies, in which workers are more closely related to worker- than to queen-produced males. This suggests that separate factors underlie the origin and maintenance of worker policing. We tested this hypothesis by investigating conflict over male parentage in B. terrestris, in which eusociality is relatively 'primitive' and queens mate once (monandry).
Using observations, experiments, and microsatellite genotyping, we found that workers lay almost 70% of male eggs within colonies in the second half of the colony cycle, but that these eggs are nearly all eaten soon after being laid. Workers' eggs are eaten by queens, reproductive workers and non-reproductive workers. This extensive egg-eating explains the low observed frequencies of larval and adult worker-produced males (5-10%) found by ourselves in the same colonies (Zanette et al. 2012) and in colonies from our previous studies (Lopez-Vaamonde et al. 2004). Queen-laid male eggs were not eaten. We also found that queen- and worker-produced male eggs have equal viabilities, a result that demonstrates that worker-produced eggs are not policed for reasons of 'hygiene' (Zanette et al. 2012). Finally, we found that workers can discriminate between queen- and worker-produced eggs using cues on eggs and egg cells. These are almost certainly chemical cues originating from queens, and their existence provides a mechanism allowing worker policing of worker- but not queen-produced male eggs (Zanette et al. 2012).
The simultaneous occurrence in B. terrestris of these three key elements of 'classical' worker policing as found in the highly eusocial, polyandrous honeybees provides novel support for the hypothesis that worker policing can originate in the absence of relatedness differences maintaining it. In addition, the occurrence of egg-eating by both reproductive and non-reproductive workers in our study strongly suggests that worker policing arises from reproductive competition among workers, that is, as 'selfish' policing. Overall, therefore, our findings shed new light on the evolution of worker policing and on the role of coercion in resolving social conflict.
The most recent of these projects was carried out by Lorenzo Zanette, Sophie Miller and Christiana Faria in Andrew Bourke's group at UEA, with input from Edd Almond and Tim Huggins, UEA, and in collaboration with the late Bill Jordan, ZSL. The work has been funded by NERC.
Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430: 557-560.
Zanette LRS, Miller SDL, Faria CMA, Almond EJ, Huggins TJ, Jordan WC, Bourke AFG (2012) Reproductive conflict in bumblebees and the evolution of worker policing. Evolution 66: 3765-3777.