Genetic determination of guarding and undertaking in honey-bee colonies

Darwin¹ considered the dramatic differences in morphology and behaviour among sterile workers, the basis of colony division of labour in the social insects, to be a greater challenge to his theory of natural selection than the occurrence of worker sterility itself. Darwin's model for the evolution of these worker traits required: (1) heritable variation among workers within colonies; (2) variation in reproductive success among colonies due to different distributions of worker traits; and (3) changes in the distribution of worker traits within colonies due to colony-level selection. The role of genetics in this evolutionary process, unknown to Darwin, has still received little attention^2,3. Calderone and Page⁴ recently demonstrated differences in the pollen-collecting behaviour of honey bees from two artificially selected strains⁵ co-fostered in wild-type colonies to be a consequence of genotypic differences between workers. These differences were caused by an artificial selection process analogous to that proposed by Darwin. Their study established a foundation for understanding genetic mechanisms underlying the evolution of division of labour but did not demonstrate a genetic basis for division of labour between related members of colonies, the essential element of the darwinian model. Here we report previously undescribed genetic differences in task specialization between related members of Apis mellifera colonies. These results, which support the first requirement of the darwinian model for the evolution of colony organisation, suggest that the genetic structure of an insect society plays a fundamental, and previously unrecognized, role in the division of labour.