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An olfactory receptor for food-derived odours promotes male courtship in Drosophila

Abstract

Many animals attract mating partners through the release of volatile sex pheromones, which can convey information on the species, gender and receptivity of the sender to induce innate courtship and mating behaviours by the receiver1. Male Drosophila melanogaster fruitflies display stereotyped reproductive behaviours towards females, and these behaviours are controlled by the neural circuitry expressing male-specific isoforms of the transcription factor Fruitless (FRUM)2,3,4,5. However, the volatile pheromone ligands, receptors and olfactory sensory neurons (OSNs) that promote male courtship have not been identified in this important model organism. Here we describe a novel courtship function of Ionotropic receptor 84a (IR84a), which is a member of the chemosensory ionotropic glutamate receptor family6, in a previously uncharacterized population of FRUM-positive OSNs. IR84a-expressing neurons are activated not by fly-derived chemicals but by the aromatic odours phenylacetic acid and phenylacetaldehyde, which are widely found in fruit and other plant tissues7 that serve as food sources and oviposition sites for drosophilid flies8. Mutation of Ir84a abolishes both odour-evoked and spontaneous electrophysiological activity in these neurons and markedly reduces male courtship behaviour. Conversely, male courtship is increased—in an IR84a-dependent manner—in the presence of phenylacetic acid but not in the presence of another fruit odour that does not activate IR84a. Interneurons downstream of IR84a-expressing OSNs innervate a pheromone-processing centre in the brain. Whereas IR84a orthologues and phenylacetic-acid-responsive neurons are present in diverse drosophilid species, IR84a is absent from insects that rely on long-range sex pheromones. Our results suggest a model in which IR84a couples food presence to the activation of the fruM courtship circuitry in fruitflies. These findings reveal an unusual but effective evolutionary solution to coordinate feeding and oviposition site selection with reproductive behaviours through a specific sensory pathway.

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Figure 1: Gene targeting of Ir84a , a candidate olfactory receptor in the fru M circuit.
Figure 2: Essential requirement for IR84a for spontaneous and odour-evoked neuronal responses.
Figure 3: IR84a is required for male courtship behaviour.
Figure 4: Anatomical integration of VL2a (IR84a-expressing) projection neurons in the pheromone processing centre.

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Acknowledgements

We are grateful to B. Dickson, A. Hofbauer, T. Lee, the Bloomington Drosophila Stock Center, the Drosophila Species Stock Center and the Developmental Studies Hybridoma Bank for provision of plasmid vectors, Drosophila strains and antibodies. We are also grateful to A. Wong, J. Wang, R. Axel, H.-H. Yu and T. Lee for sharing raw image data. We thank D. Featherstone, J.-F. Ferveur, T. Kawecki, L. Keller, S. Martin and members of the Benton laboratory for comments on the manuscript. Y.G., J.-P.F. and J.C. are supported by the Centre National de la Recherche Scientifique (CNRS), the Agence Nationale de la Recherche (ANR; JCJC, GGCB-2010) and the Conseil Régional de Bourgogne (FABER). R.R. was supported by a Roche Research Foundation fellowship. G.S.X.E.J. is supported by the Medical Research Council and a European Research Council Starting Investigator Grant. Research in R.B.’s laboratory is supported by the University of Lausanne, a European Research Council Starting Independent Researcher Grant and the Swiss National Science Foundation.

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Contributions

Y.G. and R.B. conceived the project. Y.G. performed the gene-targeting screen, contributed to the histological analysis and performed most of the behavioural experiments. R.R. performed the electrophysiological odour response screen, the fly odour stimulation assays and the phylogenetic analyses. J.-P.F. performed the chemical analysis. L.A. assisted in the generation and characterization of transgenic flies and contributed to the histological analysis. J.C. contributed to the behavioural experiments. G.S.X.E.J. performed the analysis of projection neurons. R.B. generated the DNA constructs, performed all other electrophysiological analyses and wrote the paper with contributions from Y.G., R.R., J.-P.F. and G.S.X.E.J.

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Correspondence to Richard Benton.

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Grosjean, Y., Rytz, R., Farine, JP. et al. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478, 236–240 (2011). https://doi.org/10.1038/nature10428

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