Molecular evidence for pre-chordate origins of ovarian cell types and neuroendocrine control of reproduction

Abstract

Sexual reproduction in animals requires the development of oocytes, or egg cells. This process, termed oogenesis, requires complex interactions amongst germline and somatic cell types in the ovary. How did these cell types and their signaling interactions evolve? Here we use the sea star Patiria miniata as a non-chordate deuterostome representative to define the ovarian cell type toolkit in echinoderms. Sea stars continuously produce millions of new oocytes throughout their lifespan, making them a practical system to understand the mechanisms that drive oogenesis from a biomedical and evolutionary perspective. We performed scRNA-seq combined with high-resolution 3D-imaging to reveal the ovarian cell types and their spatial organization. Our data support the presence of actively dividing oogonial stem cells and granulosa-like and theca-like cells, which display similarities and possible homology with their mammalian counterparts. Lastly, our data support the existence of an endocrine signaling system between oogonial stem cells and intrinsic ovarian neurons with striking similarities to the vertebrate hypothalamic-pituitary-gonadal axis. Overall, this study provides molecular evidence supporting the possible pre-chordate origins of conserved ovarian cell types, and the presence of an intrinsic neuroendocrine system which potentially controls oogenesis and predates the formation of the hypothalamic-pituitary-gonadal axis in vertebrates.