Journal Article

Mechanosensory interactions drive collective behaviour in Drosophila

Ramdya, Pavan, Benton, Richard, Cruchet, Steeve, Frisch, Lukas, Tse, Winnie, Floreano, Dario, Lichocki, Pawel

2015

Overview

Collective behaviour in animal groups can improve individual perception and decision-making, but the neural mechanisms involved have been hard to access in classic models for these phenomena; here it is shown that Drosophila ’s olfactory responses are enhanced in groups of flies, through mechanosensory neuron-dependent touch interactions. How fruit-fly swarms stay in touch Schooling fish, flocking birds and human crowds can enhance the perception and decision-making of individuals in the group, but the neural mechanisms involved have been hard to determine. Richard Benton and colleagues use a more accessible model in which to study group behaviour: they show that weak odour-avoidance in individual fruitflies can be enhanced in groups of flies, thanks to cascades of appendage touch interactions between pairs of flies. By identifying the mechanosensory neurons and ion channels involved, the authors open the door to a neural-circuit dissection of collective behaviour in animal groups. Collective behaviour enhances environmental sensing and decision-making in groups of animals 1 , 2 . Experimental and theoretical investigations of schooling fish, flocking birds and human crowds have demonstrated that simple interactions between individuals can explain emergent group dynamics 3 , 4 . 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 5 , 6 . 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.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14 / 14/1 / 14/19 / 14/35 / 631/378 / 64/24 / Analysis / Animal behavior / Animal Communication / Animals / Avoidance Learning - physiology / Collective behavior / Computer Simulation / Drosophila / Drosophila melanogaster - cytology / Drosophila melanogaster - genetics / Drosophila melanogaster - physiology / Drosophila Proteins - metabolism / Escape Reaction - physiology / Extremities - physiology / Female / Genetic aspects / Humanities and Social Sciences / Insects / letter / Male / Mass Behavior / Mechanoreceptors / Mechanoreceptors - cytology / Mechanoreceptors - physiology / Mechanotransduction, Cellular / multidisciplinary / Neurons / Odorants - analysis / Odors / Optogenetics / Physiological aspects / Psychological aspects / Science / Sensilla - cytology / Sensilla - physiology / Sensory perception / Touch - physiology / Transient Receptor Potential Channels - metabolism