Ruling the unruly: larval passiveness enabled size inequality between ant queens and workers

Differences between reproductive and worker castes are essential to eusocial societies. The morphological chasm between castes is highly heterogeneous across the ant phylogeny. The low size dimorphism of basal ant lineages suggests that evolutionary innovations occurred during the diversification of ants, potentially enabling their major evolutionary transition from simple eusocial societies to superorganisms. We measured queen and worker body volumes of 321 ant species belonging to 124 genera and 13 subfamilies to investigate the correlation between dimorphism and a panel of traits linked to complex eusociality. Using comparative phylogenetic methods, we show that higher dimorphism is associated with large colony sizes, distinct worker subcastes, and the loss of worker ability to mate. However, these traits correlate with both dimorphism and body volume variations of female castes. In contrast, larval morphology associated with passive larval behavior correlates only with dimorphism and not body volume variations of queens and workers. We argue that creating a large size differential between totipotent larvae with identical reproductive aspirations requires firm colony control over larval caste fate, which can only be exerted if larval nutrition is regulated by workers. We suggest that the evolutionary innovation of individualized worker-to-larva feeding, for example through trophallaxis, brought about passive larvae in some major ant lineages. Our results indicate that resolution of the conflict between larval reproductive aspirations and colony priorities was a necessary step in the evolution of complex eusocial societies.