Oral transfer of chemical cues, growth proteins and hormones in social insects

Adria C. Leboeuf, Patrice Waridel, Colin S. Brent, Andre N. Gonçalves, Laure Menin, Daniel Ortiz, Oksana Riba-Grognuz, Akiko Koto, Zamira G. Soares, Eyal Privman, Eric A. Miska, Richard Benton, Laurent Keller

Research output: Contribution to journalArticlepeer-review

Abstract

Social insects frequently engage in oral fluid exchange–trophallaxis–between adults, and between adults and larvae. Although trophallaxis is widely considered a food-sharing mechanism, we hypothesized that endogenous components of this fluid might underlie a novel means of chemical communication between colony members. Through protein and small-molecule mass spectrometry and RNA sequencing,we found that trophallactic fluid in the ant Camponotus floridanus contains a set of specific digestion-and non-digestion related proteins, as well as hydrocarbons, microRNAs, and a key developmental regulator, juvenile hormone. When C. floridanus workers’ food was supplemented with this hormone, the larvae they reared via trophallaxis were twice as likely to complete metamorphosis and became larger workers. Comparison of trophallactic fluid proteins across social insect species revealed that many are regulators of growth, development and behavioral maturation. These results suggest that trophallaxis plays previously unsuspected roles in communication and enables communal control of colony phenotypes.

Original languageEnglish
Article numbere20375
JournaleLife
Volume5
Issue numberNOVEMBER2016
DOIs
StatePublished - 29 Nov 2016

Bibliographical note

Funding Information:
We thank Robert I?Anson Price and Thomas Richardson for access to A. mellifera colonies, and Raphael Braunschweig for access to C. fellah colonies. We thank George Shizuo Kamita for advice on JHEs. We would like to thank Sylviane Moss and Kay Harnish for help with high-throughput sequencing and Alexandra Bezler, Thomas Auer, Roman Arguello, Juan Alcaniz-Sanchez, Pavan Ramdya, Lucia Prieto-Godino, Katja Hoedjes, Raphael Braunschweig and Sean McGregor for their useful comments on the manuscript. This work was funded by an ERC Advanced Grant (249375) and a Swiss NSF grant to LK, an ERC Starting Independent Researcher and Consolidator Grants (205202 and 615094) and a Swiss NSF Grant to R.B. 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. ZSG was supported by CAPES Brazil. EAM was supported by Wellcome Trust (104640/Z/14/Z).

Publisher Copyright:
© LeBoeuf et al.

ASJC Scopus subject areas

  • Neuroscience (all)
  • Immunology and Microbiology (all)
  • Biochemistry, Genetics and Molecular Biology (all)

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