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

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.

Data availability

The following data sets were generated

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.

Metrics

  • 6,280
    Page views
  • 1,233
    Downloads
  • 60
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Adria C LeBoeuf
  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
  13. Laurent Keller
(2016)
Oral transfer of chemical cues, growth proteins and hormones in social insects
eLife 5:e20375.
https://doi.org/10.7554/eLife.20375

Further reading

    1. Evolutionary Biology
    Pierrick Bourrat et al.
    Research Article

    Evolutionary transitions in individuality (ETIs) involve the formation of Darwinian collectives from Darwinian particles. The transition from cells to multicellular life is a prime example. During an ETI, collectives become units of selection in their own right. However, the underlying processes are poorly understood. One observation used to identify the completion of an ETI is an increase in collective-level performance accompanied by a decrease in particle-level performance, for example measured by growth rate. This seemingly counterintuitive dynamic has been referred to as 'fitness decoupling' and has been used to interpret both models and experimental data. Extending and unifying results from the literature, we show that fitness of particles and collectives can never decouple because calculations of particle and collective fitness performed over appropriate and equivalent time intervals are necessarily the same provided the population reaches a stable collective size distribution. By way of solution, we draw attention to the value of mechanistic approaches that emphasise traits, and tradeoffs among traits, as opposed to fitness. This trait-based approach is sufficient to capture dynamics that underpin evolutionary transitions. In addition, drawing upon both experimental and theoretical studies, we show that while early stages of transitions might often involve tradeoffs among particle traits, later—and critical-stages are likely to involve the rupture of such tradeoffs. Thus, when observed in the context of ETIs, tradeoff-breaking events stand as a useful marker for these transitions.