Collective Cell Sorting Requires Contractile Cortical Waves in Germline Cells

Encapsulation of germline cells by layers of somatic cells forms the basic unit of female reproduction called primordial follicles in mammals and egg chambers in Drosophila. How germline and somatic tissues are coordinated for the morphogenesis of each separated unit remains poorly understood. Here, using improved live imaging of Drosophila ovaries, we uncovered periodic actomyosin waves at the cortex of germ cells. These contractile waves are associated with pressure release blebs, which project from germ cells into somatic cells. We demonstrate that these cortical activities, together with cadherin-based adhesion, are required to sort each germline cyst as one collective unit. Genetic perturbations of cortical contractility, bleb protrusion, or adhesion between germline and somatic cells induced encapsulation defects resulting from failures to encapsulate any germ cells, or the inclusion of too many germ cells per egg chamber, or even the mechanical split of germline cysts. Live-imaging experiments revealed that reducing contractility or adhesion in the germline reduced the stiffness of germline cysts and their proper anchoring to the somatic cells. Germline cysts can then be squeezed and passively pushed by constricting surrounding somatic cells, resulting in cyst splitting and cyst collisions during encapsulation. Increasing germline cysts activity or blocking somatic cell constriction movements can reveal active forward migration of germline cysts. Our results show that germ cells play an active role in physical coupling with somatic cells to produce the female gamete.