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Hierarchical chemosensory regulation of male-male social interactions in Drosophila

Abstract

Pheromones regulate male social behaviors in Drosophila, but the identities and behavioral role(s) of these chemosensory signals, and how they interact, are incompletely understood. We found that (z)-7-tricosene, a male-enriched cuticular hydrocarbon that was previously shown to inhibit male-male courtship, was essential for normal levels of aggression. The mechanisms by which (z)-7-tricosene induced aggression and suppressed courtship were independent, but both required the gustatory receptor Gr32a. Sensitivity to (z)-7-tricosene was required for the aggression-promoting effect of 11-cis-vaccenyl acetate (cVA), an olfactory pheromone, but (z)-7-tricosene sensitivity was independent of cVA. (z)-7-tricosene and cVA therefore regulate aggression in a hierarchical manner. Furthermore, the increased courtship caused by depletion of male cuticular hydrocarbons was suppressed by a mutation in the olfactory receptor Or47b. Thus, male social behaviors are controlled by gustatory pheromones that promote aggression and suppress courtship, and whose influences are dominant to olfactory pheromones that enhance these behaviors.

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Figure 1: Male cuticular hydrocarbons are important for the normal balance of male-male social behaviors.
Figure 2: (z)-7-tricosene reciprocally regulates male-male aggression and courtship.
Figure 3: Gr32a mediates the behavioral effects of (z)-7-tricosene and permits the aggression-promoting effect of cVA.
Figure 4: Or47b is required for elevated male-male courtship caused by depletion of male cuticular hydrocarbons.

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Acknowledgements

We thank members of the Anderson laboratory for helpful discussions, G. Mancuso for administrative assistance, G. Mosconi for lab management, and K. Scott and L. Vosshall for critical comments on the manuscript. Assistance from N.F. Dalleska and use of gas chromatography–mass spec instrumentation in the Environmental Analysis Center at the California Institute of Technology is gratefully acknowledged. We thank L. Vosshall for generously providing the Or47b mutant alleles generated by J.M. in her laboratory. D.J.A. is an investigator of the Howard Hughes Medical Institute.

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L.W. carried out the experiments and performed the data analysis. L.W. and D.J.A. conceived the research and wrote the manuscript. X.H. synthesized cuticular hydrocarbon molecules. J.M. generated and characterized Or47b mutant alleles. M.H. characterized the expression of Gr32a-GAL4. J.-C.B., T.M., H.A. and J.D.L. contributed fly strains.

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Correspondence to Liming Wang or David J Anderson.

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Wang, L., Han, X., Mehren, J. et al. Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 14, 757–762 (2011). https://doi.org/10.1038/nn.2800

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