Oral transfer of chemical cues, growth proteins and hormones in social insects
Adria C LeBoeuf,
Patrice Waridel,
Colin S Brent,
Andre N Gonçalves,
Laure Menin,
Daniel Ortiz,
Oksana Riba-Grognuz,
Akiko Koto,
Zamira G Soares,
Eyal Privman,
Eric A Miska,
Richard Benton,
Laurent Keller
Affiliations
Adria C LeBoeuf
Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland; Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
Patrice Waridel
Protein Analysis Facility, University of Lausanne, Lausanne, Switzerland
Colin S Brent
Arid Land Agricultural Research Center, USDA-ARS, Maricopa, United States
Andre N Gonçalves
Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais, Brazil; Gurdon Institute, University of Cambridge, Cambridge, United Kingdom
Laure Menin
Institute of Chemical Sciences and Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
Daniel Ortiz
Institute of Chemical Sciences and Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
Oksana Riba-Grognuz
Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
Akiko Koto
The Department of Genetics, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, Japan
Zamira G Soares
Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais, Brazil; Gurdon Institute, University of Cambridge, Cambridge, United Kingdom
Eyal Privman
Department of Evolutionary and Environmental Biology, Institute of Evolution, University of Haifa, Haifa, Israel
Eric A Miska
Gurdon Institute, University of Cambridge, Cambridge, United Kingdom; Department of Genetics, University of Cambridge, Cambridge, United Kingdom; Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, United Kingdom
Richard Benton
Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland
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.
