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

Authors: LEBOEUF, ADRIA - Weizmann Institite Of Science; COHANIM, AMIR - University Of Haifa; STOFFEL, CELINE - University Of Lausanne; Brent, Colin; WARIDEL, PATRICE - University Of Lausanne; PRIVMAN, EYAL - University Of Haifa; KELLER, LAURENT - University Of Lausanne; BENTON, RICHARD - University Of Lausanne

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/12/2018
Publication Date: 12/13/2018
Citation: Leboeuf, A., Cohanim, A., Stoffel, C., Brent, C.S., Waridel, P., Privman, E., Keller, L., Benton, R. 2018. Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid. Scientific Reports. 8:17830.

Interpretive Summary: Socially exchanged fluids, such as semen and milk, are a direct means through which an animal can influence others of its species. It was recently shown that when workers of the carpenter ant Camponotus floridanus orally feed larval offspring, they also transfer juvenile hormone (JH), a key developmental regulator, and several JH esterases (JHE), enzymes that break down JH. Most species typically express just one or two forms of JHE, which circulates in the blood. In Camponotus, there are many different versions of JHE-like proteins and these are expressed primarily in the trophallactic fluid (TF) used to feed larvae. These esterases show evidence of having been structurally changed to better survive in the highly acidic TF. To determine whether these TF-transmitted esterases might regulate larval development, workers were fed an inhibitor of JHE activty. This inhibitor increased the likelihood of ant larvae maturing, similar to their response to supplemental JH. These findings suggest that JHE-like proteins evolved new functional roles in Camponotus, providing a new tool for workers to regulate larval development.

Technical Abstract: Socially exchanged fluids, such as seminal fluid and milk, are a direct means through which an organism can influence conspecifics. When orally feeding larval offspring via trophallaxis, workers of the carpenter ant Camponotus floridanus were recently shown to transfer Juvenile Hormone III (JH), a key developmental regulator, and paralogs of JH esterase (JHE), an enzyme that catalyzes degradation of JH. Here we combine proteomic, phylogenetic and selection analyses to investigate the evolution of esterases in ants. We show that members of the Camponotus JHE-like protein family have undergone multiple duplications, experienced positive selection, and changed tissue localization to be abundantly and selectively expressed in trophallactic fluid (TF). The Camponotus trophallactic esterases have maintained their catalytic triads but contain a number of positively-selected amino acid changes throughout the protein, which possibly reflect an adaptation to the to the highly acidic TF of formicine ants. To determine whether these TF transmitted esterases might regulate larval development, workers were fed a JHE-specific pharmacological inhibitor. This inhibitor increased the likelihood of pupation in TF fed larvae, similar to the response to food supplemented with JH. Together, these findings suggest that JHE-like proteins have evolved new functional roles in the highly diverse ant genus Camponotus, facilitating the inter-individual regulation of larval development.