The Sex-Determination Genes fruitless and doublesex Specify a Neural Substrate Required for Courtship Song

Abstract

Courtship song is a critical component of male courtship behavior in Drosophila, making the female more receptive to copulation and communicating species-specific information [1Kyriacou C.P. Hall J.C. The function of courtship song rhythms in Drosophila.Anim. Behav. 1982; 30: 794-801Crossref Scopus (180) Google Scholar, 2Kyriacou C.P. Hall J.C. Learning and memory mutants impair acoustic priming of mating behavior in Drosophila.Nature. 1984; 314: 171-173Crossref Scopus (25) Google Scholar, 3Kyriacou C.P. Hall J.C. Interspecific genetic control of courtship song production and reception in Drosophila.Science. 1986; 232: 494-497Crossref PubMed Scopus (150) Google Scholar, 4Griffith L.C. Verselis L.M. Aitken K.M. Kyriacou C.P. Danho W. Greenspan R.J. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity.Neuron. 1993; 10: 501-509Abstract Full Text PDF PubMed Scopus (190) Google Scholar, 5Ritchie M.G. Halsey E.J. Gleason J.M. Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song.Anim. Behav. 1999; 58: 649-657Crossref PubMed Scopus (169) Google Scholar, 6Rybak F. Aubin T. Moulin B. Jallon J.M. Acoustic communication in Drosophila melanogaster courtship: Are pulse- and sine-song frequencies important for courtship success?.Can. J. Zool. 2002; 80: 987-996Crossref Scopus (28) Google Scholar]. Sex mosaic studies have shown that the sex of certain regions of the central nervous system (CNS) is critical to song production [7von Schilcher F. Hall J.C. Neural topography of courtship song in sex mosaics of Drosophila melanogaster.J. Comp. Physiol. [A]. 1979; 129: 85-95Crossref Scopus (62) Google Scholar]. Our examination of one of these regions, the mesothoracic ganglion (Msg), revealed the coexpression of two sex-determination genes, fruitless (fru) and doublesex (dsx). Because both genes are involved in creating a sexually dimorphic CNS [8Taylor B.J. Truman J.W. Commitment of abdominal neuroblasts in Drosophila to a male or female fate is dependent on genes of the sex-determining hierarchy.Development. 1992; 114: 625-642PubMed Google Scholar, 9Kimura K. Ote M. Tazawa T. Yamamoto D. fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain.Nature. 2005; 438: 229-233Crossref PubMed Scopus (215) Google Scholar] and are necessary for song production [10Ryner L.C. Goodwin S.F. Castrillon D.H. Anand A. Villella A. Baker B.S. Hall J.C. Taylor B.J. Wasserman S.A. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene.Cell. 1996; 87: 1079-1089Abstract Full Text Full Text PDF PubMed Scopus (400) Google Scholar, 11Villella A. Hall J.C. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster.Genetics. 1996; 143: 331-344Crossref PubMed Google Scholar, 12Villella A. Gailey D.A. Berwald B. Ohshima S. Barnes P.T. Hall J.C. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants.Genetics. 1997; 147: 1107-1130PubMed Google Scholar, 13Goodwin S.F. Taylor B.J. Villella A. Foss M. Ryner L.C. Baker B.S. Hall J.C. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster.Genetics. 2000; 154: 725-745PubMed Google Scholar], we investigated the individual contributions of fru and dsx to the specification of a male CNS and song production. We show a novel requirement for dsx in specifying a sexually dimorphic population of fru-expressing neurons in the Msg. Moreover, by using females constitutively expressing the male-specific isoforms of fru (FruM), we show a critical requirement for the male isoform of dsx (DsxM), alongside FruM, in the specification of courtship song. Therefore, although FruM expression is sufficient for the performance of many male-specific behaviors [14Demir E. Dickson B.J. fruitless splicing specifies male courtship behavior in Drosophila.Cell. 2005; 121: 785-794Abstract Full Text Full Text PDF PubMed Scopus (340) Google Scholar], we have shown that without DsxM, the determination of a male-specific CNS and thus a full complement of male behaviors are not realized.