Socially exchanged fluids are a direct means by which an organism can influence conspecifics. It was recently shown that when workers of the carpenter ant Camponotus floridanus feed larval offspring via trophallaxis, they transfer Juvenile Hormone III (JH), a key developmental regulator, as well as paralogs of JH esterase (JHE), an enzyme that catalyzes the hydrolysis of JH. Here we combine proteomic, phylogenetic and selection analyses to investigate the evolution of this esterase subfamily. We show that Camponotus JHE-like proteins have undergone multiple duplications, experienced positive selection, and changed tissue localization to become abundantly and selectively present in trophallactic fluid. The Camponotus trophallactic esterases have maintained their catalytic triads and contain a number of positively-selected amino acid changes distributed throughout the protein, which possibly reflect an adaptation to the highly acidic trophallactic fluid of formicine ants. To determine whether these esterases might regulate larval development, we fed workers with a JHE-specific pharmacological inhibitor to introduce it into the trophallactic network. This inhibitor increased the likelihood of pupation of the larvae reared by these workers, similar to the influence of food supplementation with JH. Together, these findings suggest that JHE-like proteins have evolved a new role in the inter-individual regulation of larval development in the Camponotus genus.
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We thank Dr. George Shizuo Kamita and Prof. Dr. David Heckel for advice regarding JHEs, Dr. Jonathan Romiguier for his advice on available ant genomes, transcriptomes and methods, Dr. Christophe Dessimoz and Clément Train for early discussions on duplications and orthology, Dr. Romiguier, Dr. Kamita, Dr. David Hacker and Dr. Miriam Rosenberg for their valuable input on the manuscript. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer. This work was supported by a Swiss Friends of the Weizmann Institute of Science grant to ACL, Israel Science Foundation Grants no. 646/15, 2140/15, and 2155/15 to EP, European Research Council Advanced Grant (249375) and Swiss National Science Foundation grants to LK, and European Research Council Consolidator Grant (615094) and Swiss National Science Foundation grants to RB.
© 2018, The Author(s).
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