A queen pheromone signals the benefits of cooperation in a flexibly social insect

Eusociality, a major transition in evolution, is characterized by reproductive division of labour between queens and workers. Queen pheromones (QPs) maintain this division and inhibit worker reproduction across diverse lineages. Although QPs evolved repeatedly, it is unclear whether they evolved as honest signals of queen fecundity, as manipulative agents of chemical control, or both. If they function as honest signals, QPs may facilitate colony formation by signalling the relative benefits of cooperative versus independent nesting to behaviourally flexible kin when eusociality is facultative. Here, we identify the first QP to our knowledge from a facultatively eusocial species, the sweat bee Megalopta genalis, in which solitary nesting, social nesting and worker helping are plastic traits. The QP blend induces subordinate behaviour and inhibits worker investment in reproduction when presented in a natural context. QP levels are elevated in social-nesting queens relative to solitary reproductives; they forecast oviposition rates and worker indirect fitness gains and they predict the retention of female offspring as workers. QP components derive from oogenic nutrients, potentially enforcing signal honesty. Our findings indicate that QPs can mediate cooperative behaviour even when eusociality is incipient and facultative, supporting their origin as honest signals that may stabilize the emergence and elaboration of eusociality.