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) is a protandrous (male-first)
sequential hermaphrodite that exhibit 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.
However, region-specific relationships between length, sex and DNAm in
sequential hermaphrodites were previously unreported. To investigate these
relationships, here we compare DNAm in four conserved vertebrate
sex-determining genes in male and female barramundi of differing lengths
from three regions of northern Australia. Despite a strong association
between increasing length and male-to-female sex change, the data reveal
that DNAm becomes more sex-specific (rather than more female-specific)
with length. 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 growth. The findings also reveal
that region-specific differences in length-at-sex change are accompanied
by differences in DNAm, and were concurrent 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.