The Drosophila ovary produces three follicle waves similar to those in mice
Discuss this preprint
Start a discussion What are Sciety discussions?Listed in
This article is not in any list yet, why not save it to one of your lists.Abstract
Ovarian follicles in some species develop in subgroups known as "waves." Mouse fetal ovaries generate wave 2 follicles that form an ovarian reserve and wave 1.5 follicles that support early fertility. Wave 1 mouse follicles undergo atresia in juvenile animals that amplifies thecal cells and androgen production during puberty. We identified three similar follicle waves in Drosophila by tracking >6,000 individual lineage-labeled clones from individual germline or somatic cells in developing pupal ovaries. 40 of ∼100 larval primordial germ cells (PGCs) associate with forming germline stem cell (GSC) niches. After a delay of >30 hours during early pupal stages, GSCs begin division and ultimately produce cysts that ensure a lifetime supply of wave 2 eggs. Wave 1.5 follicles develop directly from many of the remaining PGCs to g enerate ∼20 cysts and all 80 ovarian follicles present at adult eclosion. Adult-like but unstable follicle stem cells (FSCs) generate most follicle cells for wave 1.5, with a contribution from the basal stalk. Unexpectedly, a true wave 1 subpopulation arises from relatively few posterior PGCs. Drosophila wave 1 germ cells increase rapidly to 250-350 cells by dividing and then forming germline cysts. They subsequently interact with somatic swarm cells before undergoing an atresia-like process and exiting the ovary. Our results argue that production of specific ovarian follicle waves, including an initial wave that undergoes atresia during adult tissue development, has been conserved during evolution.
SIGNIFICANCE
Here we show that Drosophila oogenesis takes place in three follicle waves matching the follicle waves recently described in mice. Previously, ovaries were thought to generate one follicle type dedicated to reproduction and follicles undergoing atresia were considered defective. By better documenting pupal ovary development at single-cell resolution, we demonstrate that each wave derives from distinct PGCs and interacts with different somatic cells. The previously unknown Drosophila wave 1 follicles, amplify rapidly from ∼10 to 300 germ cells, break from the ovary and release their contents into the hemolymph coincident with the pupal ecdysone peak. Follicle wave conservation argues that ovaries produce multiple germ cell types that evolved for distinct roles, including the promotion of adult development.
