Pharaoh ant colonies dynamically regulate reproductive allocation based on colony demography

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 ant Monomorium pharaonis. By measuring the effects of demographic manipulation on colony productivity, we infer that caste allocation results 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 signaled by pheromone present on eggs. This strategy enables the dynamic alteration of colony demography in response to internal and external conditions, which is likely key to the ability of M. pharaonis and similar ants to thrive in disturbed habitats and to become widespread invasive species. SIGNIFICANCE STATEMENT: The 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 (multiqueen) societies. However, the mechanisms by which such societies regulate caste allocation are largely unknown. In this study, we perform a range of manipulative studies to disentangle social mechanisms of caste allocation in polygynous ant societies. Based on our results, we develop a model in which colonies manipulate their production of queens (and also males) versus workers according to the present density of eggs in the colony, 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.