Epigenetic Regulation and Environmental Sex Determination in Cichlid Fishes

Abstract

Studying environmental sex determination (ESD) in cichlids provides a phylogenetic and comparative approach to understand the evolution of the underlying mechanisms, their impact on the evolution of the overlying systems, and the neuroethology of life history strategies. Natural selection normally favors parents who invest equally in the development of male and female offspring, but evolution may favor deviations from this 50:50 ratio when environmental conditions produce an advantage for doing so. Many species of cichlids demonstrate ESD in response to water chemistry (temperature, pH, and oxygen concentration). The relative strengths of and the exact interactions between these factors vary between congeners, demonstrating genetic variation in sensitivity. The presence of sizable proportions of the less common sex towards the environmental extremes in most species strongly suggests the presence of some genetic sex-determining loci acting in parallel with the ESD factors. Sex determination and differentiation in these species does not seem to result in the organization of a final and irreversible sexual fate, so much as a life-long ongoing battle between competing male- and female-determining genetic and hormonal networks governed by epigenetic factors. We discuss what is and is not known about the epigenetic mechanism behind the differentiation of both gonads and sex differences in the brain. Beyond the well-studied tilapia species, the 2 best-studied dwarf cichlid systems showing ESD are the South American genus <i>Apistogramma</i> and the West African genus <i>Pelvicachromis</i>. Both species demonstrate male morphs with alternative reproductive tactics. We discuss the further neuroethology opportunities such systems provide to the study of epigenetics of alternative life history strategies and other behavioral variation.

Rapid turnover and evolution of sex-determining regions amongSebastesrockfishes

“…Other abiotic factors, such as salinity (Saillant et al, 2003) and pH (Reddon & Hurd, 2013) have also been shown to induce skewed sex ratios in fishes. This variety of SD systems within a recently speciated clade is not unprecedented; African cichlid fishes exhibit an enormous diversity of SD mechanisms, including several independently evolved sex chromosomes (Gammerdinger & Kocher, 2018; El Taher et al, 2021), polygenic GSD (Roberts et al, 2016), ESD (Renn & Hurd, 2021), and intraspecific variation in SD mechanisms (Lichilín et al, 2023). Further investigation into the forces underlying ESD in these and other species is warranted, as warming and acidifying oceans leave species whose gonadal differentiation are influenced by environmental factors much more vulnerable to impacts on sex ratios.…”

Rapid turnover and evolution of sex‐determining regions in Sebastes rockfishes

“…Other abiotic factors, such as salinity (Saillant et al, 2003) and pH (Reddon & Hurd, 2013) have also been shown to induce skewed sex ratios in fishes. This variety of SD systems within a recently speciated clade is not unprecedented; African cichlid fishes exhibit an enormous diversity of SD mechanisms, including several independently evolved sex chromosomes (El Taher et al, 2021; Gammerdinger & Kocher, 2018), polygenic GSD (Roberts et al, 2016), ESD (Renn & Hurd, 2021) and intraspecific variation in SD mechanisms (Lichilín et al, 2023). Given the possibility of inaccurate sex data and lack of genomic signal, further research is required to disentangle the roles of genotype and environment on sex in these species.…”

Use of male-to-female sex reversal as a welfare scoring system in the protandrous farmed gilthead sea bream (Sparus aurata)

“…However, the success of reproductive performance, measured by means of fecundity, puberty onset, and sex reversal, can also have a high value from a retrospective point of view, as it is the end point of a complex cascade of developmental events that encompass a wide range of biotic and abiotic factors ( 18 – 22 ). In particular, the sex ratio in gonochoristic fish tends to be balanced in optimal culture conditions ( 23 ), although it can be affected by chemicals ( 24 ) and other environmental factors such as rearing density, temperature, pH, oxygen, and diet composition ( 25 – 29 ). Similarly, sex reversal in hermaphrodite species, such as in the protandrous gilthead sea bream, is socially controlled and endocrine-regulated by the circulating levels of estradiol (E 2 ) and 11-ketotestosterone (11-KT) ( 30 ), and intriguingly the exposure to synthetic estrogens (e.g., 17α-ethynylestradiol) prevents the male-to-female sex reversal ( 31 ).…”