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Sci Rep. 2018 Dec 13;8(1):17830. doi: 10.1038/s41598-018-36048-1.

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

Author information

1
Department of Physics of Complex Systems, Weizmann Institute of Science, Rehovot, Israel. adrialeboeuf@gmail.com.
2
Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland. adrialeboeuf@gmail.com.
3
Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland. adrialeboeuf@gmail.com.
4
Department of Evolutionary and Environmental Biology, Institute of Evolution, University of Haifa, Haifa, Israel.
5
Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
6
Arid Land Agricultural Research Center, USDA-ARS, Maricopa, United States.
7
Protein Analysis Facility, University of Lausanne, Lausanne, Switzerland.
8
Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland.

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.

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