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
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
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Social exchange of chemical cues, growth proteins and hormones through trophallaxisPublicly available at ProteomeXchange (accession no. PXD004825).
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Camponotus fellah Transcriptome or Gene expressionPublicly available at the NCBI BioProject database (accession no: PRJNA339034).
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Camponotus floridanus Transcriptome or Gene expressionPublicly available at the NCBI BioProject database (accession no: PRJNA338939).
Article and author information
Author details
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
© 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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Oral transfer of chemical cues, growth proteins and hormones in social insects
eLife 5:e20375.
https://doi.org/10.7554/eLife.20375
Further reading
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- Evolutionary Biology
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.
