Pharaoh ant colonies dynamically regulate colony demography by culling young queen and male-destined larvae

The success of social insect colonies is dependent upon efficient and dynamic allocation of resources to alternate queen and worker castes. The developmental and molecular mechanisms regulating the caste fate of individual larvae in response to environmental cues have been the focus of intense study. However, the mechanisms regulating colony-level resource allocation into alternate castes (i.e. caste allocation ratios) are less well studied. Here, we systematically manipulate colony demography to elucidate the social regulatory mechanisms of caste allocation in the antMonomorium pharaonis. We find that differences in caste allocation result from differences in timing and efficiency of culling of very young reproductive-destined larvae, which are always present in colonies. Based on our results, we develop a conceptual model depicting how colonies integrate numerous individual-level caste determination decisions to regulate colony-level caste allocation. We propose that adult workers make decisions about culling larvae based on the ratio of the number of workers to the number of eggs contained in colonies, likely signalled by pheromone present on eggs. This strategy is a bet-hedging strategy which enables the dynamic alteration of colony demography in response to internal and external conditions. The strategy is likely key to the ability ofM. pharaonisand similar ants to thrive in disturbed habitats and to become widespread invasive species.Significance StatementThe defining feature of social insect societies is the presence of alternate queen (reproductive) and worker (non-reproductive) castes of individuals. The fitness of social insect colonies is dependent upon efficient allocation of resources to alternate castes, particularly in the case of highly polygynous (multi-queen) societies. However, the mechanisms by which such societies regulate caste allocation are largely unknown. In this study, we show that colonies manipulate their production of queens (and also males) versus workers according to the present density of eggs in the colony, which serves as a reliable indicator of queens’ fertility. Provided egg density is high, colonies kill queen-and male-destined larvae; when egg density falls, colonies begin to rear queens and males. This flexible resource allocation strategy is key to the ability of highly polygynous species to thrive in marginal (often human-associated) habitats.