Macrocyclic Lactones Act as a Queen Pheromone in a Primitively Eusocial Sweat Bee

Summary Eusociality is characterized by the reproductive division of labor between two castes: fertile queens and largely sterile workers. Queen pheromones are known to influence worker behavior and reproductive physiology and are therefore key components in regulating complex eusocial behavior [ 1 ]. Recent studies indicate that cuticular hydrocarbons (CHCs) act as queen pheromones in various eusocial hymenopteran species [ 2 , 3 , 4 , 5 , 6 , 7 , 8 ]. However, almost all species investigated to date are highly eusocial and do not include extant transitory stages from solitary to eusocial behavior [ 9 ]. Indeed, primitively eusocial species, which largely lack morphologically distinct castes, are thought to control worker reproduction through the physical aggression of the queen rather than via pheromones [ 10 , 11 , 12 ]. Halictid or sweat bees exhibit a high variability of eusociality including solitary and facultatively eusocial species [ 9 , 13 , 14 , 15 , 16 ]. However, the mechanisms controlling worker reproduction in these transitory species are unknown. The results of a recent correlative study based on caste-specific chemical profiles in various halictid bees of different social levels have revealed an overproduction of macrocyclic lactones in queens compared with workers [ 17 ]. Using chemical analyses and behavioral experiments in which we simulated below-ground nests of the primitively eusocial sweat bee Lasioglossum malachurum, we identified a queen pheromone and found that macrocyclic lactones, not CHCs, influence worker behavior and decrease ovarian activation in this species. Our data suggest that the evolution of queen pheromones is more complex than previously inferred from highly eusocial species and shed new light on the complexity of the evolution of queen pheromones.