Gonadal remodelling in socially driven sex change is associated with novel and known sex genes, epigenetic reprogramming, and inflammation-mediated apoptosis

Abstract

Many fish undergo dramatic, socially cued female-to-male sex change, yet the events that initiate and then regulate gonadal reprogramming and reorganisation during this phenomenal metamorphosis are broadly unknown. The New Zealand spotted wrasse, Notolabrus celidotus, is a temperate fish species that displays the extraordinary ability to undergo protogynous sex change. Removal of a terminal-phase male from a social group triggers the most dominant female to change sex and become a male. To characterise the molecular changes associated with gonadal metamorphosis in spotty, we used genomic and transcriptomic approaches, generating a high-quality genome and a transcriptomic time-series that captures the sex change process from start to finish. These data, together with paired histological data, reveal distinct transcriptional profiles that characterise the process of sex change. As expected, the expression of masculinising genes steadily increases, while feminising genes steadily decrease, throughout the transition. We further identify novel candidate genes, including genes involved in immune signalling and tissue remodelling through inflammation-mediated apoptosis, whose expression strongly correlates with key events in sex change, while also confirming the roles of known sex determination and differentiation genes in this process. Collectively these data give us new insights into how a normally committed developmental process remains plastic and is reversed to completely alter organ structures, and also sheds light on the evolution of sex determination in other animals. This work furthers the development of the spotty as a new tractable model for sex change research.