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.
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
Lineages of rod-shaped bacteria such as Escherichia coli exhibit a temporal decline in elongation rate in a manner comparable to cellular or biological aging. The effect results from the production of asymmetrical daughters, one with a lower elongation rate, by the division of a mother cell. The slower daughter compared to the faster daughter, denoted respectively as the old and new daughters, has more aggregates of damaged proteins and fewer expressed gene products. We have examined further the degree of asymmetry by measuring the density of ribosomes between old and new daughters and between their poles. We found that ribosomes were denser in the new daughter and also in the new pole of the daughters. These ribosome patterns match the ones we previously found for expressed gene products. This outcome suggests that the asymmetry is not likely to result from properties unique to the gene expressed in our previous study, but rather from a more fundamental upstream process affecting the distribution of ribosomal abundance. Because damage aggregates and ribosomes are both more abundant at the poles of E. coli cells, we suggest that competition for space between the two could explain the reduced ribosomal density in old daughters. Using published values for aggregate sizes and the relationship between ribosomal number and elongation rates, we show that the aggregate volumes could in principle displace quantitatively the amount of ribosomes needed to reduce the elongation rate of the old daughters.
