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
The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than ten alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognized.
