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

Abstract

Ovarian follicles in most species are assumed to develop using a single pathway. However, in Drosophila pupae, lineage tracing 2,937 single-cell clones identified three follicle "waves" that follow distinct programs arrayed anterior to posterior in the germarium and developing ovarioles. 40 primordial germ cells (PGCs) become anterior germline stem cells (GSCs) that produce "wave 2" follicles throughout adulthood. 100 PGCs posterior to wave 2 develop into "wave 1.5" follicles that form the earliest laid eggs. Different follicle stem cells (FSCs) sequentially occupy the same two niches timed to provide both waves with specific follicle cells, consistent with programmed differences between waves 2 and 1.5. "Wave 1" PGCs located even further posterior proliferate, form cysts, interact with swarm cells, degenerate, break from the ovary 22-26 hours after puparium formation, and release lipid-enriched vacuoles. Some testis germ cells behave similarly. We speculate that wave 1 germ cells contribute directly or indirectly to the pharate adult ecdysone pulse that mediates adult development and sex-specific neural remodeling. Why Drosophila follicle waves generally resemble those clarified recently in mouse preadult ovaries merits additional study.