Chemical fertility signaling in a flexibly eusocial insect
Callum Kingwell, Callum Kingwell , William Wcislo
Department of Neurobiology and Behavior, Cornell University; Smithsonian Tropical Research Institute; Department of Neurobiology and Behavior, Cornell University; Smithsonian Tropical Research Institute ; Smithsonian Tropical Research Institute
Queen pheromones (QPs) evolved independently in all highly eusocial insect lineages, and mitigate conflict over access to reproduction by inhibiting the ovarian development of workers. Despite their fundamental importance in regulating reproductive division of labor, the hallmark of eusociality, the evolutionary origins of QPs remain enigmatic. Chemical signaling of social dominance and fertility has been studied primarily in lineages with evolutionarily conserved and obligate eusociality, which are suitable for questions about current function but not evolutionary origins. We studied the cuticular and glandular chemistries of Megalopta genalis bees in Central Panamá, within a population in which eusociality is facultative and whose tribe (Augochlorini) accounts for one of two relatively recent evolutionarily origins of eusociality in the family Halictidae. Solitary and social individuals, as well as reproductive and non-reproductive individuals, are readily distinguished by their chemical profiles. Two specific chemical classes largely underpin this separation. One, methyl-alkanes, are phylogenetically widespread and linked to reproductive state in many insect taxa. The other, macrocyclic lactones, are restricted to halictid, colletid, and andrenid bees. Combined analyses of chemical production and nest social behavior shows that these chemicals reliably indicate distinct axes of reproductive potential in Megalopta, and that social selection is likely to be an important factor affecting their production. Overall, our results suggest that QPs may evolve via social selection on reliable chemical cues whose physiological links to reproductive state may show deep phylogenetic conservation, but can also be taxonomically unique. The queen pheromones of contemporary eusocial insect taxa include a mix of shared and conserved chemical elements; this may be explained by variation in the physiologies of the solitary ancestors from which modern eusocial insects evolved.