Non-canonical function of the Sex-lethal gene controls the protogyny phenotype in Drosophila melanogaster

Abstract

Many animal species exhibit sex differences in the time period prior to reaching sexual maturity. However, the underlying mechanism for such biased maturation remains poorly understood. Females of the fruit fly Drosophila melanogaster eclose 4 h faster on average than males, owing to differences in the pupal period between the sexes; this characteristic is referred to as the protogyny phenotype. Here, we aimed to elucidate the mechanism underlying the protogyny phenotype in the fruit fly using our newly developed Drosophila Individual Activity Monitoring and Detecting System (DIAMonDS), which can continuously detect the precise timing of both pupariation and eclosion of individual flies. Via this system, following the laying of eggs, we detected the precise time points of pupariation and eclosion of a large number of individual flies simultaneously and succeeded in identifying the tiny differences in pupal duration between females and males. We first explored the role of physiological sex by establishing transgender flies via knockdown of the sex-determination gene, transformer (tra) and its co-factor tra2, which retained the protogyny phenotype. In addition, disruption of dosage compensation by male-specific lethal (msl-2) knockdown did not affect the protogyny phenotype. The Drosophila master sex switch gene--Sxl promotes female differentiation via tra and turns off male dosage compensation through the repression of msl-2. However, we observed that stage-specific whole-body knockdown and mutation of Sxl induced disturbance of the protogyny phenotype. These results suggest that an additional, non-canonical function of Sxl involves establishing the protogyny phenotype in D. melanogaster. Author summaryA wide variety of animals show differences in time points of sexual maturation between sexes. For example, in many mammals, including human beings, females mature faster than males. This maturation often takes several months or years, and precisely detecting the time point of maturation is challenging, because of the continuity of growth, especially in mammals. Moreover, the reason behind the difference in sexual maturation time points between sexes is not fully understood. The fruit fly Drosophila--a model organism--also shows biased maturation between the sexes, with females emerging 4 h faster than males (a characteristic known as the protogyny phenotype). To understand the mechanism underlying the protogyny phenotype, we used our newly developed system, Drosophila Individual Activity Monitoring and Detecting System (DIAMonDS), to detect the precise eclosion point in individual fruit flies. Surprisingly, our analysis of transgender flies obtained by knockdown and overexpression techniques indicated that a physiological gender might not be necessary requirement for protogyny and that a non-canonical novel function of the fruit fly master sex switch gene, Sxl, regulates protogyny in fruit flies.