Doublesex controls specification and maintenance of the gonad stem cell niches in Drosophila

Abstract

Sex-specific development of the gonads is a key aspect of sexual dimorphism that is regulated by Doublesex/Mab3 Related Transcription Factors (DMRTs) in diverse animal species. We find that in mutants for Drosophila dsx, important components of the male and female gonad stem cell niches (hubs and terminal filaments/cap cells, respectively) still form. Initially, gonads in all dsx mutants (both XX and XY) initiate the male program of development, but later half of these gonads switch to form female stem cell niche structures. One individual can have both male-type and female-type gonad niches, however male and female niches are usually not observed in the same gonad, indicating that cells make a “group decision” about which program to follow. We conclude that dsx does not act in an instructive manner to regulate male vs. female niche formation, as these structures form in the absence of dsx function. Instead, dsx acts to “tip the balance” between the male or female programs, which are then executed independent of dsx. We show that bric a brac acts downstream of dsx to control the male vs. female niche decision. These results indicate that, in both flies and mammals, the sexual fate of the somatic gonad is remarkably plastic and is controlled by a combination of autonomous and non-autonomous cues.