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
-
Social exchange of chemical cues, growth proteins and hormones through trophallaxisPublicly available at ProteomeXchange (accession no. PXD004825).
-
Camponotus fellah Transcriptome or Gene expressionPublicly available at the NCBI BioProject database (accession no: PRJNA339034).
-
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.
Metrics
-
- 7,107
- views
-
- 1,346
- downloads
-
- 98
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Oral transfer of chemical cues, growth proteins and hormones in social insects
eLife 5:e20375.
https://doi.org/10.7554/eLife.20375
Further reading
-
- Developmental Biology
- Evolutionary Biology
Despite rapid evolution across eutherian mammals, the X-linked MIR-506 family miRNAs are located in a region flanked by two highly conserved protein-coding genes (SLITRK2 and FMR1) on the X chromosome. Intriguingly, these miRNAs are predominantly expressed in the testis, suggesting a potential role in spermatogenesis and male fertility. Here, we report that the X-linked MIR-506 family miRNAs were derived from the MER91C DNA transposons. Selective inactivation of individual miRNAs or clusters caused no discernible defects, but simultaneous ablation of five clusters containing 19 members of the MIR-506 family led to reduced male fertility in mice. Despite normal sperm counts, motility, and morphology, the KO sperm were less competitive than wild-type sperm when subjected to a polyandrous mating scheme. Transcriptomic and bioinformatic analyses revealed that these X-linked MIR-506 family miRNAs, in addition to targeting a set of conserved genes, have more targets that are critical for spermatogenesis and embryonic development during evolution. Our data suggest that the MIR-506 family miRNAs function to enhance sperm competitiveness and reproductive fitness of the male by finetuning gene expression during spermatogenesis.
