Non-canonical function of theSex-lethalgene controls the protogyny phenotype inDrosophila melanogaster

Abstract

AbstractMany 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 flyDrosophila melanogastereclose 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 developedDrosophilaIndividual 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-factortra2, which retained the protogyny phenotype. In addition, disruption of dosage compensation bymale-specific lethal(msl-2) knockdown did not affect the protogyny phenotype. TheDrosophilamaster sex switch gene—Sxlpromotes female differentiation viatraand turns off male dosage compensation through the repression ofmsl-2.However, we observed that stage-specific whole-body knockdown and mutation ofSxlinduced disturbance of the protogyny phenotype. These results suggest that an additional, non-canonical function ofSxlinvolves establishing the protogyny phenotype inD. 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 flyDrosophila—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,DrosophilaIndividual 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.