Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid

Socially exchanged fluids are a direct means for organisms to influence conspecifics. When orally feeding larval offspring via trophallaxis, Camponotus floridanus ant workers were shown to transfer Juvenile Hormone (JH), a key developmental regulator, as well as paralogs of JH esterase (JHE), an enzyme that hydrolyzes JH. We combine proteomic, phylogenetic and selection analyses to investigate the evolution of this esterase subfamily. We show that Camponotus JHE-like proteins have sustained multiple duplications, positive selection, and changed localization to become abundantly and selectively present in trophallactic fluid. To assess their potential role in larval development, we fed workers a JHE-specific inhibitor to introduce it into the trophallactic network. This increased the proportion larvae reared to metamorphosis by these workers, similar to supplementation with JH. Together these findings suggest that JHE-like proteins have evolved new roles in inter-individual regulation of larval development in Camponotus .