Epigenetics underpins phenotypic plasticity of protandrous sex change in fish

Abstract

Phenotypic plasticity is an important driver of species resilience. Often mediated by epigenetic changes, phenotypic plasticity enables individual genotypes to express variable phenotypes in response to environmental change. Barramundi (Lates calcarifer) are a protandrous (male‐first) sequential hermaphrodite that exhibits plasticity in length‐at‐sex change between geographic regions. This plasticity is likely to be mediated by changes in DNA methylation (DNAm), a well‐studied epigenetic modification. To investigate the relationships between length, sex, and DNAm in a sequential hermaphrodite, here, we compare DNAm in four conserved vertebrate sex‐determining genes in male and female barramundi of differing lengths from three geographic regions of northern Australia. Barramundi first mature as male and later sex change to female upon the attainment of a larger body size; however, a general pattern of increasing female‐specific DNAm markers with increasing length was not observed. Significant differences in DNAm between males and females of similar lengths suggest that female‐specific DNAm arises rapidly during sex change, rather than gradually with fish growth. The findings also reveal that region‐specific differences in length‐at‐sex change are accompanied by differences in DNAm and are consistent with variability in remotely sensed sea temperature and salinity. Together, these findings provide the first in situ evidence for epigenetically and environmentally mediated sex change in a protandrous hermaphrodite and offer significant insight into the molecular and ecological processes governing the marked and unique plasticity of sex in fish.

Potential implications of sperm DNA methylation functional properties in aquaculture management

“…117 Therefore, imprinted genes of vertebrates might be identified in fish, however, maintaining the imprinting mechanism is delicate and subtle. 62,118 In another example, the hypermethylated region was detected in the goldfish (Carassius auratus) igf2 gene, which is the paternal expression gene in the imprinting centre 1, but the methylation pattern of this gene was not maintained in embryo. 109 From these analogical studies, it seems that parental imprinting probably does not stabilize in fish, or that a special unknown inheriting mechanism may be present.…”

“…In zebrafish, peg1/mest , an ortholog of the mammalian imprinted gene PEG1/MEST , is expressed during embryogenesis; however, mest is not the imprinted gene 117 . Therefore, imprinted genes of vertebrates might be identified in fish, however, maintaining the imprinting mechanism is delicate and subtle 62,118 . In another example, the hypermethylated region was detected in the goldfish ( Carassius auratus ) igf2 gene, which is the paternal expression gene in the imprinting centre 1, but the methylation pattern of this gene was not maintained in embryo 109 .…”

Characterization of thePristionchus pacificus“epigenetic toolkit” reveals the evolutionary loss of the histone methyltransferase complex PRC2

“…The microbivorous morph is narrow, deep, and contains a single dorsal “tooth” while the omnivorous morph is wide, shallow, and contains two teeth. Several studies have now pointed to epigenetic mechanisms as a way to translate environmental signals into gene expression changes that underly the development of different traits (Valena and Moczek 2012; Duncan et al 2014; Yan et al 2014; Kilvitis et al 2017; Thorson et al 2017; Budd et al 2022; Toker et al 2022; Jordan et al 2023; Werner et al 2023). We recently showed that perturbing histone acetylation/deacetylation with chemical inhibitors alters both mouth-form phenotype and the expression of key “switch genes,” indicating that epigenetic pathways are, at least in part, responsible for the regulation of mouth-form development (Werner et al 2023).…”