Sex change in aquarium systems establishes the New Zealand spotty wrasse (Notolabrus celidotus) as a temperate model species for the investigation of sequential hermaphroditism

Abstract

Many studies of vertebrate sex change focus on subtropical and tropical teleosts. This study presents the protogynous New Zealand spotty wrasse, Notolabrus celidotus, as a temperate model. Captive fish were induced to change sex using either aromatase inhibition or manipulation of social groups. The endocrine and genetic cascade underlying this process was investigated using time-series sampling coupled with histological staging, sex steroid quantification and nanoString nCounter mRNA analysis. Seasonality affected sex ratios and sex steroid profiles; the likelihood of sex change increased when social manipulations were performed outside of the breeding season. Early-stage decreases in plasma 17β-estradiol (E2) concentrations or gonadal aromatase (cyp19a1a) expression were not detected in spotty wrasse, despite these being associated with the onset of sex change in many protogynous hermaphrodites. Gonadal expression of 21 candidate genes was examined in relation to gonadal histology and sex steroid concentrations across sex change. When compared to other species, some genes previously implicated in sex determination and differentiation showed typical sex-specific gonadal expression patterns (foxl1, dmrt1, amh), while other critical male- and female-pathway genes exhibited unexpected patterns (cyp19a1a, rspo1, sox9a). Moreover, expression of the masculinising factor amh (anti-Müllerian hormone) increased during early sex change, implying a potential role as a proximate trigger for sex change. Dynamic expression of DNA methyltransferase genes suggested a key role of epigenetic regulation during the ovary-to-testis transformation in this species. Collectively, these data provide a foundation for the spotty wrasse as a new teleost model to study sex change and cell fate in vertebrates.