Epigenetics underpins phenotypic plasticity of protandrous sex change in fish

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.