Oral transfer of chemical cues, growth proteins and hormones in social insects
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
Version 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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Further reading
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- Evolutionary Biology
The RNA world hypothesis proposes that during the early evolution of life, primordial genomes of the first self-propagating evolutionary units existed in the form of RNA-like polymers. Autonomous, non-enzymatic, and sustained replication of such information carriers presents a problem, because product formation and hybridization between template and copy strands reduces replication speed. Kinetics of growth is then parabolic with the benefit of entailing competitive coexistence, thereby maintaining diversity. Here, we test the information-maintaining ability of parabolic growth in stochastic multispecies population models under the constraints of constant total population size and chemostat conditions. We find that large population sizes and small differences in the replication rates favor the stable coexistence of the vast majority of replicator species (‘genes’), while the error threshold problem is alleviated relative to exponential amplification. In addition, sequence properties (GC content) and the strength of resource competition mediated by the rate of resource inflow determine the number of coexisting variants, suggesting that fluctuations in building block availability favored repeated cycles of exploration and exploitation. Stochastic parabolic growth could thus have played a pivotal role in preserving viable sequences generated by random abiotic synthesis and providing diverse genetic raw material to the early evolution of functional ribozymes.