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.

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.

Download links

Share this article

https://doi.org/10.7554/eLife.20375

Further reading

    1. Ecology
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.