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

Adria C Leboeuf,Laurent Keller,Colin S Brent,Patrice Waridel,Eyal Privman,Amir B Cohanim,Richard Benton,Céline Stoffel

doi:10.1038/s41598-018-36048-1

Abstract

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.

Highlights

Coordination between cells in a multicellular organism often occurs through hormones, which bind to receptors on or in different cell types throughout the body
These results indicate that the presence of Juvenile Hormone III (JH) and JH esterase (JHE) in this social fluid is variable across social insects, implying that it is unlikely to result from a passive process such as diffusion from hemolymph
Our results reveal the evolution of a subfamily of JHE-like proteins in carpenter ants whose members have sustained many duplications, significant positive selection and shifted their location from hemolymph to the trophallactic fluid

Summary

Introduction

Coordination between cells in a multicellular organism often occurs through hormones, which bind to receptors on or in different cell types throughout the body. We recently showed that trophallactic fluid in Camponotus floridanus carpenter ants contains hormones, nestmate recognition cues, small RNAs, and a variety of proteins, many of which have been associated with growth and development[4], suggesting broader functions for this fluid in inter-individual communication. Amongst these molecules, the presence of Juvenile Hormone III (JH) was of particular interest[4] because this hormone is a key regulator of insect development[5,6] and reproduction[7,8,9] across insects, and of caste determination[5,6,7,10,11,12,13] and division of labor[14,15,16,17,18] in social insects. In addition to JH, C. floridanus trophallactic fluid contains abundant JHE-like proteins[4], raising questions about the role of these enzymes in this fluid

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Conclusion