Viviparity and beyond: captured endogenous retroviral envelope genes drive teleost physiological innovations.

Endogenous retroviral envelope (ERV env) genes, notably syncytins, are known for driving placental development in mammals and lizards. However, their broader contributions to non-mammalian vertebrates, particularly viviparous fish, remain largely unexplored. Here, we present the discovery and functional characterization of three co-opted/captured ERV env gene clades, including a Percom-env clade comprising previously reported percomORF in the viviparous teleost Sebastes schlegelii. Our findings reveal that each gene clade plays a distinct and critical role in neural regulation, reproductive maturation, and viviparity. Notably, Percom-env percomORF retains fusogenic activity and its brain-specific expression is driven by conserved regulatory elements across Percomorpha. Meanwhile, Seb-env4 env genes, expressed uniquely in the testis, support seasonal gonadal maturation and Sertoli cell maintenance. Lastly, Seb-env3 env genes, localized at the maternofetal interface, retain a robust fusion capacity essential for follicular placentation, and have persisted for approximately 15 million years in the Sebastes genus, thus identified as candidate syncytin-Seb, likely underpinning the emergence of viviparity. These findings demonstrate env co-option/capture drives teleost adaptations, extending retroviral env-mediated placentation beyond mammals and lizards, and highlight conserved mechanisms in vertebrate reproductive evolution.