Evolutionary Biology

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

University of Lausanne, Switzerland
USDA-ARS, United States
Universidade Federal de Minas Gerais, Brazil
Ecole Polytechnique Fédérale de Lausanne, Switzerland
The University of Tokyo, Japan
Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil
University of Haifa, Israel
University of Cambridge, United Kingdom

Research Article Nov 29, 2016

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Cite this article as: eLife 2016;5:e20375 doi: 10.7554/eLife.20375

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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.

Article and author information

Author details

Adria C LeBoeuf

Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland

For correspondence
adria.leboeuf@gmail.com

Competing interests
The authors declare that no competing interests exist.
Patrice Waridel

Protein Analysis Facility, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Colin S Brent

Arid Land Agricultural Research Center, USDA-ARS, Maricopa, United States

Competing interests
The authors declare that no competing interests exist.
Andre N Gonçalves

Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais, Brazil

Competing interests
The authors declare that no competing interests exist.
Laure Menin

Institute of Chemical Sciences and Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Daniel Ortiz

Institute of Chemical Sciences and Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Oksana Riba-Grognuz

Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Akiko Koto

Department of Genetics, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, Japan

Competing interests
The authors declare that no competing interests exist.
Zamira G Soares

Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais, Brazil

Competing interests
The authors declare that no competing interests exist.
Eyal Privman

Department of Evolutionary and Environmental Biology, Institute of Evolution, University of Haifa, Haifa, Israel

Competing interests
The authors declare that no competing interests exist.
Eric A Miska

Gurdon Institute, University of Cambridge, Cambridge, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Richard Benton

Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland

For correspondence
Richard.Benton@unil.ch

Competing interests
The authors declare that no competing interests exist.
Laurent Keller

Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

For correspondence
laurent.keller@unil.ch

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5046-9953

Funding

European Research Council (Advanced Grant 249375)

Laurent Keller

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Richard Benton
Laurent Keller

European Research Council (Starting Independent Researcher 205202)

Richard Benton

European Research Council (Consolidator Grant 615094)

Richard Benton

Wellcome (Wellcome Trust grant 104640/Z/14/Z)

Eric A Miska

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

Zamira G Soares

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

Marcel Dicke, Wageningen University, Netherlands

Publication history

Received: August 5, 2016
Accepted: November 14, 2016
Accepted Manuscript published: November 29, 2016 (version 1)
Version of Record published: December 12, 2016 (version 2)
Version of Record updated: August 19, 2019 (version 3)

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.