title: Mechanosensory interactions drive collective behaviour in Drosophila.
abstract: Collective behaviour enhances environmental sensing and decision-making in groups of animals. Experimental and theoretical investigations of schooling fish, flocking birds and human crowds have demonstrated that simple interactions between individuals can explain emergent group dynamics. These findings indicate the existence of neural circuits that support distributed behaviours, but the molecular and cellular identities of relevant sensory pathways are unknown. Here we show that Drosophila melanogaster exhibits collective responses to an aversive odour: individual flies weakly avoid the stimulus, but groups show enhanced escape reactions. Using high-resolution behavioural tracking, computational simulations, genetic perturbations, neural silencing and optogenetic activation we demonstrate that this collective odour avoidance arises from cascades of appendage touch interactions between pairs of flies. Inter-fly touch sensing and collective behaviour require the activity of distal leg mechanosensory sensilla neurons and the mechanosensory channel NOMPC. Remarkably, through these inter-fly encounters, wild-type flies can elicit avoidance behaviour in mutant animals that cannot sense the odour--a basic form of communication. Our data highlight the unexpected importance of social context in the sensory responses of a solitary species and open the door to a neural-circuit-level understanding of collective behaviour in animal groups.
authors.affiliation: 1] Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne CH-1015, Switzerland [2] Laboratory of Intelligent Systems, Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne CH-1015, Switzerland.
authors.forename: Pavan
authors.initials: P
authors.lastname: Ramdya
authors.affiliation: 1] Laboratory of Intelligent Systems, Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne CH-1015, Switzerland [2] Department of Ecology and Evolution, University of Lausanne, Lausanne CH-1015, Switzerland.
authors.forename: Pawel
authors.initials: P
authors.lastname: Lichocki
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne CH-1015, Switzerland.
authors.forename: Steeve
authors.initials: S
authors.lastname: Cruchet
authors.affiliation: Master's Program in Microengineering, Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne CH-1015, Switzerland.
authors.forename: Lukas
authors.initials: L
authors.lastname: Frisch
authors.affiliation: Master's Program in Microengineering, Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne CH-1015, Switzerland.
authors.forename: Winnie
authors.initials: W
authors.lastname: Tse
authors.affiliation: Laboratory of Intelligent Systems, Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne CH-1015, Switzerland.
authors.forename: Dario
authors.initials: D
authors.lastname: Floreano
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne CH-1015, Switzerland.
authors.forename: Richard
authors.initials: R
authors.lastname: Benton
mesh_terms: D000819:Animal Communication; D000818:Animals; D001362:Avoidance Learning / Q000502:physiology; D003198:Computer Simulation; D029721:Drosophila Proteins / Q000378:metabolism; D004331:Drosophila melanogaster / Q000166:cytology / Q000235:genetics / Q000502:physiology*; D004924:Escape Reaction / Q000502:physiology*; D005121:Extremities / Q000502:physiology; D005260:Female; D008297:Male; D008399:Mass Behavior; D008465:Mechanoreceptors / Q000166:cytology / Q000502:physiology*; D040542:Mechanotransduction, Cellular; D009812:Odorants / Q000032:analysis*; D062308:Optogenetics; D058618:Sensilla / Q000166:cytology / Q000502:physiology*; D014110:Touch / Q000502:physiology; D050051:Transient Receptor Potential Channels / Q000378:metabolism
chemical_list: D029721:Drosophila Proteins; C405783:NOMPC protein, Drosophila; D050051:Transient Receptor Potential Channels