Cellular and molecular mechanisms of seahorse male pregnancy

Abstract

Seahorses and their relatives (syngnathids) show a unique sex role reversal. Their male pregnancy is facilitated by an evolutionary novel organ—the brood pouch that functions analogously to the mammalian uterus and placenta despite originating from entirely different tissues. Here we use comparative single-cell multiomics and genomics analyses to investigate the transition from egg laying to pregnancy during syngnathid evolution and compare the convergently evolved life history of placental parental care with that in mammals. In vivo experiments show that a population of epithelial progenitors that possesses pouch-inducing potential and expresses androgen, not female hormones as in other live-bearers, can trigger pouch ontogeny. Two mechanisms ensure functionality of the pouch: recruitment of pseudo-placenta-related cells characterized by expressed orthologous genes also found in mammalian uteri and co-option of specific cells for sticky eggs attached to specialized skin patches of males that express novel seahorse-specific genes such as pastns and syn-lectins. These mechanisms combined drove pouch diversity and complexity in syngnathids.