Activation of Latent Courtship Circuitry in the Brain of Drosophila Females Induces Male-like Behaviors

Abstract

Courtship in Drosophila melanogaster offers a powerful experimental paradigm for the study of innate sexually dimorphic behaviors [1Pavlou H.J. Goodwin S.F. Courtship behavior in Drosophila melanogaster: towards a “courtship connectome”.Curr. Opin. Neurobiol. 2013; 23: 76-83Crossref PubMed Scopus (92) Google Scholar, 2Auer T.O. Benton R. Sexual circuitry in Drosophila.Curr. Opin. Neurobiol. 2016; 38: 18-26Crossref PubMed Scopus (81) Google Scholar]. Fruit fly males exhibit an elaborate courtship display toward a potential mate [1Pavlou H.J. Goodwin S.F. Courtship behavior in Drosophila melanogaster: towards a “courtship connectome”.Curr. Opin. Neurobiol. 2013; 23: 76-83Crossref PubMed Scopus (92) Google Scholar, 2Auer T.O. Benton R. Sexual circuitry in Drosophila.Curr. Opin. Neurobiol. 2016; 38: 18-26Crossref PubMed Scopus (81) Google Scholar]. Females never actively court males, but their response to the male’s display determines whether mating will actually occur. Sex-specific behaviors are hardwired into the nervous system via the actions of the sex determination genes doublesex (dsx) and fruitless (fru) [1Pavlou H.J. Goodwin S.F. Courtship behavior in Drosophila melanogaster: towards a “courtship connectome”.Curr. Opin. Neurobiol. 2013; 23: 76-83Crossref PubMed Scopus (92) Google Scholar]. Activation of male-specific dsx/fru+ P1 neurons in the brain initiates the male’s courtship display [3von Philipsborn A.C. Liu T. Yu J.Y. Masser C. Bidaye S.S. Dickson B.J. Neuronal control of Drosophila courtship song.Neuron. 2011; 69: 509-522Abstract Full Text Full Text PDF PubMed Scopus (225) Google Scholar, 4Kohatsu S. Koganezawa M. Yamamoto D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila.Neuron. 2011; 69: 498-508Abstract Full Text Full Text PDF PubMed Scopus (183) Google Scholar], suggesting that neurons unique to males trigger this sex-specific behavior. In females, dsx+ neurons play a pivotal role in sexual receptivity and post-mating behaviors [1Pavlou H.J. Goodwin S.F. Courtship behavior in Drosophila melanogaster: towards a “courtship connectome”.Curr. Opin. Neurobiol. 2013; 23: 76-83Crossref PubMed Scopus (92) Google Scholar, 2Auer T.O. Benton R. Sexual circuitry in Drosophila.Curr. Opin. Neurobiol. 2016; 38: 18-26Crossref PubMed Scopus (81) Google Scholar, 5Rideout E.J. Dornan A.J. Neville M.C. Eadie S. Goodwin S.F. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster.Nat. Neurosci. 2010; 13: 458-466Crossref PubMed Scopus (232) Google Scholar, 6Kimura K. Sato C. Koganezawa M. Yamamoto D. Drosophila ovipositor extension in mating behavior and egg deposition involves distinct sets of brain interneurons.PLoS ONE. 2015; 10: e0126445Google Scholar, 7Zhou C. Pan Y. Robinett C.C. Meissner G.W. Baker B.S. Central brain neurons expressing doublesex regulate female receptivity in Drosophila.Neuron. 2014; 83: 149-163Abstract Full Text Full Text PDF PubMed Scopus (101) Google Scholar, 8Rezával C. Nojima T. Neville M.C. Lin A.C. Goodwin S.F. Sexually dimorphic octopaminergic neurons modulate female postmating behaviors in Drosophila.Curr. Biol. 2014; 24: 725-730Abstract Full Text Full Text PDF PubMed Scopus (102) Google Scholar, 9Rezával C. Pavlou H.J. Dornan A.J. Chan Y.B. Kravitz E.A. Goodwin S.F. Neural circuitry underlying Drosophila female postmating behavioral responses.Curr. Biol. 2012; 22: 1155-1165Abstract Full Text Full Text PDF PubMed Scopus (143) Google Scholar]. Yet it is still unclear how dsx+ neurons and dimorphisms in these circuits give rise to the different behaviors displayed by males and females. Here, we manipulated the function of dsx+ neurons in the female brain to investigate higher-order neurons that drive female behaviors. Surprisingly, we found that activation of female dsx+ neurons in the brain induces females to behave like males by promoting male-typical courtship behaviors. Activated females display courtship toward conspecific males or females, as well other Drosophila species. We uncovered specific dsx+ neurons critical for driving male courtship and identified pheromones that trigger such behaviors in activated females. While male courtship behavior was thought to arise from male-specific central neurons, our study shows that the female brain is equipped with latent courtship circuitry capable of inducing this male-specific behavioral program.