Sex-specific responses of small RNAs and transposable elements to thermal stress in zebrafish germ cells

Abstract

Climate change-induced thermal stress threatens germline genome stability and triggers a molecular response of small RNA pathways involved transposable element (TE) regulation. The difference in mitotic and meiotic activity in male and female germ cells suggests that this response differs, but the mechanisms are elusive. Here we integrate whole-genome and transcriptome sequencing, and small RNA profiling to examine how mild thermal elevation affects TE regulation in male and female zebrafish gonads. We find that ovaries maintain genomic integrity through coordinated upregulation of piRNAs and miRNAs linked to heat-shock responses, limiting TE mobilisation. In contrast, testes exhibit reduced small RNA abundance, widespread TE activation, and increased de novo insertions, reflecting compromised genome defence. Multi-omic network analyses reveal a piRNA-TE-miRNA regulatory network preserved in ovaries but disrupted in testes under thermal stress. These findings reveal a sex-specific divergence in genome defence mechanisms, with implications for fertility and heritable genome stability in changing environments.