The Reversible Sex of Gonochoristic Fish: Insights and Consequences

Abstract

Fish sex reversal is a means to understand sex determination and differentiation, but it is also used to control sex in aquaculture. This review discusses sex reversal in gonochoristic fish, with the coexistence of genetic and environmental influences. The different periods of fish sensitivity to sex reversal treatments are presented with the mechanisms implicated. The old players of sex differentiation are revisited with transcriptome data and loss of function studies following hormone- or temperature-induced sex reversal. We also discuss whether cortisol is the universal mediator of sex reversal in fish due to its implication in ovarian meiosis and 11KT increase. The large plasticity in fish for sex reversal is also evident in the brain, with a reversibility existing even in adulthood. Studies on epigenetics are presented, since it links the environment, gene expression, and sex reversal, notably the association of DNA methylation in sex reversal. Manipulations with exogenous factors reverse the primary sex in many fish species under controlled conditions, but several questions arise on whether this can occur under wild conditions and what is the ecological significance. Cases of sex reversal in wild fish populations are shown and their fitness and future perspectives are discussed.

Ovarian transcriptomic signatures of zebrafish females resistant to different environmental perturbations

“…Fish gonadal development is quite plastic and in many species, the response to environmental perturbations that encompass the period of sex differentiation is masculinization (Baroiller & D'Cotta, ; Ospina‐Alvarez & Piferrer, ; Piferrer, ). The masculinization of genotypic females generates phenotypic males (Hliwa, Bah, Kuźmiński, Dobosz, & Ciereszko, ) that are termed neomales (Pandian & Sheela, ).…”

Reproductive phenotype predicts adult bite‐force performance in sex‐reversed dragons (Pogona vitticeps)

“…The accumulating evidence of species that employ both primary cues (genes and environment) to determine sex (transitional systems; Hill, Burridge, Ezaz, & Wapstra, 2018; Holleley et al, 2015; Holleley, Sarre, O'Meally, & Georges, 2016; Radder, Quinn, Georges, Sarre, & Shine, 2008; Shine, Elphick, & Donnellan, 2002), points to the existence of a continuum of states from complete genetic control via sex chromosomes to complete dependence on environmental influence over sex (Sarre, Georges, & Quinn, 2004). The potential for naturally occurring sex reversal (Baroiller & D'Cotta, 2016; Ginot, Claude, Perez, & Veyrunes, 2017; Holleley et al, 2015; Jiménez, Burgos, Caballero, & De La Guardia, 1988) is the hallmark of transitional systems. A small number of studies of terrestrial vertebrates indicate that the de‐coupling of chromosomal and phenotypic sex, via sex reversal, can result in individuals bearing a mixture of male‐like, female‐like, or novel traits (Deveson et al, 2017; Ginot et al, 2017; Li, Holleley, Elphick, Georges, & Shine, 2016).…”

Climate change, sex reversal and lability of sex‐determining systems

“…Climate change can cause the loss of a sex chromosome and a transition to ESD. An increasing number of vertebrate species with sex chromosomes display sex reversal in response to high incubation temperatures, and this susceptibility may be a widespread trait in ectothermic, gonochoristic vertebrates (Baroiller & D’Cotta, ; Flament, ; Holleley et al, ). The conclusions apply analogously to polygenic taxa (multiple loci contributing quantitatively to sex; Beukeboom & Perrin, ) if there are some genetic combinations that are susceptible to sex reversal and others which are not (e.g., male signal curves that show continuous variation in height among individuals).…”

“…For example, in medaka fish, a copy of the DMRT1 gene on the Y chromosome triggers male development in XY individuals; however, high developmental temperatures induce expression of autosomal DMRT1 genes and lead to male development in XX individuals (Hattori et al, ; Matsuda et al, ; Nanda et al, ). Sex reversal owing to extreme temperatures or exposure to exogenous hormones has been demonstrated in captivity in an increasing number of vertebrate species, with many more species likely to be susceptible (Baroiller & D’Cotta, ; Devlin & Nagahama, ; Flament, ; Holleley, Sarre, O’Meally, & Georges, ; Senior & Nakagawa, ). Moreover, discordant animals have been caught in the wild in a handful of species (Baroiller & D’Cotta, ; Holleley et al, , ; Perrin, ).…”

“…Sex reversal owing to extreme temperatures or exposure to exogenous hormones has been demonstrated in captivity in an increasing number of vertebrate species, with many more species likely to be susceptible (Baroiller & D’Cotta, ; Devlin & Nagahama, ; Flament, ; Holleley, Sarre, O’Meally, & Georges, ; Senior & Nakagawa, ). Moreover, discordant animals have been caught in the wild in a handful of species (Baroiller & D’Cotta, ; Holleley et al, , ; Perrin, ). Sex reversal may therefore be widespread and occur with significant frequency across wild ectothermic vertebrates under changing environmental conditions.…”