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

Thomas, Jodi T., Todd, Erica V., Muncaster, Simon, Lokman, P. Mark, Damsteegt, Erin L., Liu, Hui, Soyano, Kiyoshi, Gléonnec, Florence, Lamm, Melissa S., Godwin, John R., and Gemmell, Neil J. (2019) Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses. PeerJ, 7. e7032.

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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.

Item ID: 60050
Item Type: Article (Research - C1)
ISSN: 2167-8359
Keywords: protogynous sex change, bluehead wrasse, spotty wrasse, kyusen wrasse, quantitative real-time PCR, sex-biased gene expression, cyp19a1a, cyp19a1b, amh, isotocin
Copyright Information: © 2019 Thomas et al.
Funders: Royal Society of New Zealand Marsden Fund (RSNZ), Japan Society for the Promotion of Science (JSPS), National Science Foundation (NSF), Otago School of Medical Science Summer Scholarship
Projects and Grants: RSNZ UOO1308, JSPS L10703, NSF 1257791 & 1257761
Date Deposited: 03 Jul 2019 07:56
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060403 Developmental Genetics (incl Sex Determination) @ 100%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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