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

  1. Adria C LeBoeuf  Is a corresponding author
  2. Patrice Waridel
  3. Colin S Brent
  4. Andre N Gonçalves
  5. Laure Menin
  6. Daniel Ortiz
  7. Oksana Riba-Grognuz
  8. Akiko Koto
  9. Zamira G Soares
  10. Eyal Privman
  11. Eric A Miska
  12. Richard Benton  Is a corresponding author
  13. Laurent Keller  Is a corresponding author
  1. University of Lausanne, Switzerland
  2. USDA-ARS, United States
  3. Universidade Federal de Minas Gerais, Brazil
  4. Ecole Polytechnique Fédérale de Lausanne, Switzerland
  5. The University of Tokyo, Japan
  6. Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil
  7. University of Haifa, Israel
  8. University of Cambridge, United Kingdom
Research Article
  • Cited 34
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Cite this article as: eLife 2016;5:e20375 doi: 10.7554/eLife.20375

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

  1. 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.
  2. Patrice Waridel

    Protein Analysis Facility, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Colin S Brent

    Arid Land Agricultural Research Center, USDA-ARS, Maricopa, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. 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.
  5. 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.
  6. 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.
  7. Oksana Riba-Grognuz

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  8. 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.
  9. 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.
  10. 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.
  11. Eric A Miska

    Gurdon Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. 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.
  13. 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.
    ORCID icon "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

  1. Marcel Dicke, Wageningen University, Netherlands

Publication history

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

Copyright

© 2016, LeBoeuf et al.

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.

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