Mechanisms driving temperature-induced early sex change in barramundi (Lates calcarifer)

Abstract

Sex in fish is remarkably plastic. In some gonochoristic species, temperature exposure during early development can result in epigenetic changes and phenotypic reversal of an otherwise genetically encoded sex. In most of these cases, high temperatures result in an increased proportion of phenotypic males. In sequential hermaphrodites, such as the protandrous barramundi (Lates calcarifer), the effect of temperature on sex is largely unknown. Here, we reared 1-year-old barramundi under four different temperature profiles and examined the effects on mRNA expression, DNA methylation and phenotypic sex. Exposure to high temperature (34 °C) led to early sex change, skewing sex ratios toward transitional and female fish compared to the all-male control group. These phenotypic changes were accompanied by differences in methylation and/or expression of conserved sex-determining genes (e.g., cyp19a1a and dmrt1), and others with putative roles in cellular sensing and signal transduction. Global DNA methylation differences and alternative splicing were observed between sexes but not between temperatures, suggesting that these epigenetic mechanisms occur downstream of putative temperature-modulated signal transduction pathways. The results demonstrate that in contrast to gonochoristic fish, the gonads of sequential hermaphrodites maintain plasticity beyond the completion of sex differentiation, and that exposure to high temperatures leads to an increased proportion of females, rather than males. The findings may assist in the development of temperature as a consumer friendly strategy for sex control in aquaculture.