Unexpected worker mating and colony-founding in a superorganism

Abstract

Abstract The emergence of superorganisms in ants, termites, bees, and wasps1 represents a major transition in evolution2. Pre-imaginal caste determination, leading to reproductively dominant queens, which mate, store sperm, and lay fertilized eggs, and lifetime unmatedness of worker castes are key features of these animal societies1. While workers in superorganismal species like honey bees and many ant species have consequently either lost, or retain only vestigial spermathecal structures, workers in the bumble bees, wasps and certain ant subfamilies retain complete spermathecae3,4,5. In the case of bumble bees, the retention of these structures in workers and whether they remain reproductively functional despite 25-40 million years of evolution6, is an evolutionary mystery. Here we show that bumble bee workers have retained queen-like reproductive traits. We demonstrate through artificial insemination experiments that worker spermathecae are functional, and that their gene expression post-insemination mirrors that of queens. Further, we show that inseminated workers can rear colonies and produce female offspring throughout the colony life-cycle, an act previously believed to be the sole domain of queens. Mating experiments identified that social isolation is a trigger for successful mating, with social interactions with brood, workers, or queens inhibiting mating. Subsequent semi-field experiments showed that workers can naturally mate in de-queened colonies and go on to produce queen offspring. In the wild, this may act as a back-up strategy to maintain colonies in response to the early loss of the queen. Our results demonstrate that bumble bee workers retain the ability to function as queens, resolving the paradox of why workers in certain taxa maintain intact spermatheca which never mate, and suggesting that worker lifetime unmatedness is not a pre-requisite for the evolutionary transition to superorganisms. Our finding also provides an exciting new tool to combat global declines in bumble bees through artificial insemination of workers from rare and declining species and could therefore have applications in protecting bumble bee biodiversity.