Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses

Abstract

Fishes exhibit remarkably diverse, and plastic, patterns of sexual development, most striking of which is sequential hermaphroditism, where individuals readily reverse sex in adulthood. How this stunning example of phenotypic plasticity is controlled at a genetic level remains poorly understood. Several genes have been implicated in regulating sex change, yet the degree to which a conserved genetic machinery orchestrates this process has not yet been addressed. Using captive and in-the-field social manipulations to initiate sex change, combined with a comparative qPCR approach, we compared expression patterns of four candidate regulatory genes among three species of wrasses (Labridae)—a large and diverse teleost family where female-to-male sex change is pervasive, socially-cued, and likely ancestral. Expression in brain and gonadal tissues were compared among the iconic tropical bluehead wrasse (Thalassoma bifasciatum) and the temperate spotty (Notolabrus celidotus) and kyusen (Parajulus poecilepterus) wrasses. In all three species, gonadal sex change was preceded by downregulation of cyp19a1a (encoding gonadal aromatase that converts androgens to oestrogens) and accompanied by upregulation of amh (encoding anti-müllerian hormone that primarily regulates male germ cell development), and these genes may act concurrently to orchestrate ovary-testis transformation. In the brain, our data argue against a role for brain aromatase (cyp19a1b) in initiating behavioural sex change, as its expression trailed behavioural changes. However, we find that isotocin (it, that regulates teleost socio-sexual behaviours) expression correlated with dominant male-specific behaviours in the bluehead wrasse, suggesting it upregulation mediates the rapid behavioural sex change characteristic of blueheads and other tropical wrasses. However, it expression was not sex-biased in temperate spotty and kyusen wrasses, where sex change is more protracted and social groups may be less tightly-structured. Together, these findings suggest that while key components of the molecular machinery controlling gonadal sex change are phylogenetically conserved among wrasses, neural pathways governing behavioural sex change may be more variable.

Peer Review #1 of "An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish (v0.1)"

“…However, three-spot wrasses live in tropical waters, and sex change in captive populations has been observed in under 40 days (Kuwamura et al, 2007), around half that required in spotty wrasse (60 -70 days (Thomas et al, 2019)). In the current study, it may be that spotty wrasse ovaries were not cultured long enough for 11KT to promote male germ cell proliferation, or that 11KT alone is insufficient to induce gonadal transformation in this species.…”

Peer Review #2 of "An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish (v0.2)"

“…We chose the New Zealand spotty wrasse (Notolabrus celidotus), a common and widespread marine species, to evaluate the effects of a suite of hormonal factors on gonadal architecture. In this diandric protogynous hermaphroditic species, sex change is socially regulated, whereby the removal of the dominant male from the social group induces sex change in a resident female (Thomas et al, 2019). Spotty wrasses exhibit sexual dimorphism with alternative male phenotypes.…”

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

“…This physically hardy species has a wide thermal tolerance (approximately 8 -25° C) and adapts well to captivity and tolerates experimental manipulation. Sexually mature fish will spawn in captivity and sex change is induced in IP fish through the manipulation of social structure (Thomas et al, 2019). This proclivity to complete natural sex change under laboratory conditions is of particular significance as other model species such as the bluehead wrasse (Thalassoma bifasciatum) adapt poorly to captivity leading to most sex change experiments being done in wild populations (Liu et al, 2015;Thomas et al, 2019;Todd et al, 2019).…”