Abstract

Mating and gametogenesis are two essential components of animal reproduction. Gametogenesis must be modulated by the need for gametes, yet little is known of how mating, a process that utilizes gametes, may modulate the process of gametogenesis. Here, we report that mating stimulates female germline stem cell (GSC) proliferation in Drosophila melanogaster. Mating-induced increase in GSC number is not simply owing to the indirect effect of emission of stored eggs, but rather is stimulated by a male-derived Sex Peptide (SP) and its receptor SPR, the components of a canonical neuronal pathway that induces a post-mating behavioral switch in females. We show that ecdysteroid, the major insect steroid hormone, regulates mating-induced GSC proliferation independently of insulin signaling. Ovarian ecdysteroid level increases after mating and transmits its signal directly through the ecdysone receptor expressed in the ovarian niche to increase the number of GSCs. Impairment of ovarian ecdysteroid biosynthesis disrupts mating-induced increase in GSCs as well as egg production. Importantly, feeding of ecdysteroid rescues the decrease in GSC number caused by impairment of neuronal SP signaling. Our study illustrates how female GSC activity is coordinately regulated by the neuroendocrine system to sustain reproductive success in response to mating.

Highlights

  • Gametogenesis is modulated by stimuli from environments surrounding individual organisms

  • Gametogenesis is supported by germline stem cells (GSCs)

  • It remains unclear how GSC proliferation is regulated in response to such external signals at the molecular and cellular levels

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Summary

Introduction

Gametogenesis is modulated by stimuli from environments surrounding individual organisms. One such example is mating stimulus, which accelerates egg production [1]. Because mating is a process that utilizes many eggs, it is plausible that mating may modulate the process of gametogenesis. It remains largely unclear how mating affects gametogenesis at a cellular level. Drosophila GSCs reside in a specialized microenvironment, or niche, where they are exposed to local signals required for stem cell function (Fig 1A) [2,3]. Little is known about whether and how GSC number is regulated by the signals from the external environment

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