Aggression is regulated by pheromones in many animal species1,2,3. However, in no system have aggression pheromones, their cognate receptors and corresponding sensory neurons been identified. Here we show that 11-cis-vaccenyl acetate (cVA), a male-specific volatile pheromone, robustly promotes male–male aggression in the vinegar fly Drosophila melanogaster. The aggression-promoting effect of synthetic cVA requires olfactory sensory neurons (OSNs) expressing the receptor Or67d4,5,6, as well as the receptor itself. Activation of Or67d-expressing OSNs, either by genetic manipulation of their excitability or by exposure to male pheromones in the absence of other classes of OSNs, is sufficient to promote aggression. High densities of male flies can promote aggression by the release of volatile cVA. In turn, cVA-promoted aggression can promote male fly dispersal from a food resource, in a manner dependent on Or67d-expressing OSNs. These data indicate that cVA may mediate negative-feedback control of male population density, through its effect on aggression. Identification of a pheromone–OSN pair controlling aggression in a genetic organism opens the way to unravelling the neurobiology of this evolutionarily conserved behaviour.
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Shorey, H. H. Behavioral responses to insect pheromones. Annu. Rev. Entomol. 18, 349–380 (1973)
Keverne, E. B. Mammalian pheromones: from genes to behaviour. Curr. Biol. 12, R807–R809 (2002)
Chamero, P. et al. Identification of protein pheromones that promote aggressive behaviour. Nature 450, 899–902 (2007)
Ha, T. S. & Smith, D. P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila . J. Neurosci. 26, 8727–8733 (2006)
van der Goes van Naters, W. & Carlson, J. R. Receptors and neurons for fly odors in Drosophila . Curr. Biol. 17, 606–612 (2007)
Kurtovic, A., Widmer, A. & Dickson, B. J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542–546 (2007)
Sturtevant, A. H. Experiments on sex recognition and the problem of sexual selection in Drosophila . Anim. Behav. 5, 351–366 (1915)
Chen, S., Lee, A. Y., Bowens, N. M., Huber, R. & Kravitz, E. A. Fighting fruit flies: a model system for the study of aggression. Proc. Natl Acad. Sci. USA 99, 5664–5668 (2002)
Vrontou, E., Nilsen, S. P., Demir, E., Kravitz, E. A. & Dickson, B. J. fruitless regulates aggression and dominance in Drosophila . Nature Neurosci. 9, 1469–1471 (2006)
Baier, A., Wittek, B. & Brembs, B. Drosophila as a new model organism for the neurobiology of aggression? J. Exp. Biol. 205, 1233–1240 (2002)
Dierick, H. A. & Greenspan, R. J. Molecular analysis of flies selected for aggressive behavior. Nature Genet. 38, 1023–1031 (2006)
Dierick, H. A. & Greenspan, R. J. Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nature Genet. 39, 678–682 (2007)
Wang, L., Dankert, H., Perona, P. & Anderson, D. J. A common genetic target for environmental and heritable influences on aggressiveness in Drosophila . Proc. Natl Acad. Sci. USA 105, 5657–5663 (2008)
Hoyer, S. C. et al. Octopamine in male aggression of Drosophila . Curr. Biol. 18, 159–167 (2008)
Zhou, C., Rao, Y. & Rao, Y. A subset of octopaminergic neurons are important for Drosophila aggression. Nature Neurosci. 11, 1059–1067 (2008)
Xu, P., Atkinson, R., Jones, D. N. M. & Smith, D. P. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45, 193–200 (2005)
Laughlin, J. D., Ha, T. S., Jones, D. N. M. & Smith, D. P. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133, 1255–1265 (2008)
Bartelt, R. J., Schaner, A. M. & Jackson, L. L. cis-vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster . J. Chem. Ecol. 11, 1747–1756 (1985)
Ejima, A. et al. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr. Biol. 17, 599–605 (2007)
Dankert, H., Wang, L., Hoopfer, E. D., Anderson, D. J. & Perona, P. Automated monitoring and analysis of social behavior in Drosophila . Nature Methods 6, 297–303 (2009)
Certel, S. J., Savella, M. G., Schlegel, D. C. F. & Kravitz, E. A. Modulation of Drosophila male behavioral choice. Proc. Natl Acad. Sci. USA 104, 4706–4711 (2007)
Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T. & Bate, M. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523–1531 (2001)
Ren, D. et al. A prokaryotic voltage-gated sodium channel. Science 294, 2372–2375 (2001)
Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714 (2004)
Schlief, M. L. & Wilson, R. I. Olfactory processing and behavior downstream from highly selective receptor neurons. Nature Neurosci. 10, 623–630 (2007)
Hoffmann, A. A. A laboratory study of male territoriality in the sibling species Drosophila melanogaster and D. simulans . Anim. Behav. 35, 807–818 (1987)
Benton, R. Sensitivity and specificity in Drosophila pheromone perception. Trends Neurosci. 30, 512–519 (2007)
Ono, M., Terabe, H., Hori, H. & Sasaki, M. Insect signalling: components of giant hornet alarm pheromone. Nature 424, 637–638 (2003)
Kou, R., Chen, S.-C., Chen, Y.-R. & Ho, H.-Y. 3-Hydroxy-2-butanone and the first encounter fight in the male lobster cockroach, Nauphoeta cinerea . Naturwissenschaften 93, 286–291 (2006)
Datta, S. R. et al. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452, 473–477 (2008)
We thank B. Dickson, M. Heisenberg and L. Vosshall for providing fly stocks, R. Axel, C. Bargmann, J. Levine and L. Vosshall for comments on the manuscript and L. Zipursky for discussions. This work was supported in part by NSF grants EF-0623527 and MCB-0418479. D.J.A. is an Investigator of the Howard Hughes Medical Institute.
Author Contributions L.W. carried out all the experiments and performed the data analysis. L.W. and D.J.A. together conceived the research and wrote the manuscript.
The authors declare no competing financial interests.
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Wang, L., Anderson, D. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227–231 (2010). https://doi.org/10.1038/nature08678
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