title: 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 antCamponotus floridanuscontains a set of specific digestion- and non-digestion related proteins, as well as hydrocarbons, microRNAs, and a key developmental regulator, juvenile hormone. WhenC. floridanusworkers' 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.
authors.affiliation: Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland.|Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
authors.forename: Adria C
authors.initials: AC
authors.lastname: LeBoeuf
authors.affiliation: Protein Analysis Facility, University of Lausanne, Lausanne, Switzerland.
authors.forename: Patrice
authors.initials: P
authors.lastname: Waridel
authors.affiliation: Arid Land Agricultural Research Center, USDA-ARS, Maricopa, United States.
authors.forename: Colin S
authors.initials: CS
authors.lastname: Brent
authors.affiliation: 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.
authors.forename: Andre N
authors.initials: AN
authors.lastname: Gonçalves
authors.affiliation: Institute of Chemical Sciences and Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.
authors.forename: Laure
authors.initials: L
authors.lastname: Menin
authors.affiliation: Institute of Chemical Sciences and Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.
authors.forename: Daniel
authors.initials: D
authors.lastname: Ortiz
authors.affiliation: Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
authors.forename: Oksana
authors.initials: O
authors.lastname: Riba-Grognuz
authors.affiliation: The Department of Genetics, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, Japan.
authors.forename: Akiko
authors.initials: A
authors.lastname: Koto
authors.affiliation: 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.
authors.forename: Zamira G
authors.initials: ZG
authors.lastname: Soares
authors.affiliation: Department of Evolutionary and Environmental Biology, Institute of Evolution, University of Haifa, Haifa, Israel.
authors.forename: Eyal
authors.initials: E
authors.lastname: Privman
authors.affiliation: 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.
authors.forename: Eric A
authors.initials: EA
authors.lastname: Miska
authors.affiliation: Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland.
authors.forename: Richard
authors.initials: R
authors.lastname: Benton
authors.affiliation: Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
authors.forename: Laurent
authors.identifier: http://orcid.org/0000-0002-5046-9953
authors.initials: L
authors.lastname: Keller
mesh_terms: D000818:Animals; D001000:Ants / Q000502:physiology*; D001522:Behavior, Animal; D001826:Body Fluids / Q000737:chemistry; D006728:Hormones / Q000378:metabolism; D019476:Insect Proteins / Q000378:metabolism; D007605:Juvenile Hormones / Q000378:metabolism*; D013058:Mass Spectrometry; D017423:Sequence Analysis, RNA; D012919:Social Behavior
chemical_list: D006728:Hormones; D019476:Insect Proteins; D007605:Juvenile Hormones
keywords: Apis mellifera; Camponotus fellah; Camponotus floridanus; Solenopsis invicta; collective behavior; evolutionary biology; genomics; social evolution