The Drosophila ovary produces two waves of adult follicles and a novel pupal wave that turns over

Follicles in Drosophila and many other species are thought to develop using a single pathway. In contrast, we show by lineage tracing [~]3,000 single-cell clones, that three follicle "waves" arise in pupae that follow distinct programs, suggesting they evolved for distinct functions. Wave 1.5 follicles develop directly from primordial germ cells (PGCs) and provide the first [~]100 eggs, enough for some fertility in low nutritional environments. With adequate food, germline stem cell (GSC) divisions produce wave 2 follicles without limit that support high fecundity. Wave 1.5 follicle stem cells (FSCs) are specifically replaced in their niches with new FSCs to coat wave 2 germ cells with unique follicle cells. Previously unknown wave 1 follicles amplify rapidly in number, but soon undergo programmed degeneration and exit the ovary along with some somatic cells as they release lipophilic material. A subpopulation of testis germ cells behave in a similar manner. We propose that wave 1 germ cell breakdown contributes to the concomitant but unexplained pharate adult ecdysone pulse that mediates adult tissue developing, including the rewiring of reproductive behavior.