Developmental exposure to constant elevated temperatures and diel thermal variation alters microRNA expression and...

In their natural environments, fish are exposed to diel thermal fluctuations, the range of which is expected to increase dramatically with climate change. Recently, it has been posited that epigenetic modulators like microRNAs (miRNAs) could buffer fish against such changes. To investigate this, we conducted two sequential experiments using zebrafish (Danio rerio). In Experiment 1, we exposed zebrafish to constant control (CTRL; 28°C), fluctuating (FLUX; 28±5°C), or elevated (HEAT; 33°C) temperatures throughout early development (embryo to juvenile, up to 30 days post-fertilization [dpf]). Throughout early development, we assessed survival, metabolism, and the expression of seven thermosensitive miRNAs and three heat shock proteins (HSPs). While HEAT conditions significantly reduced survival, FLUX exposure did not. Both FLUX and HEAT juveniles exhibited metabolic compensation, though this was more pronounced in FLUX fish. Notably, miR-181a-5p, which regulates mitochondrial biogenesis and respiration, was significantly upregulated in FLUX juveniles, suggesting its involvement in improving metabolic performance. Experiment 2 evaluated the long-term effects of ontogenetic thermal variability. Starting at 30 dpf, remaining fish in both CTRL and FLUX treatments were maintained under CTRL conditions until adulthood. We then assessed miRNA expression in the brain and thermal tolerance (CT_max). miR-181a-5p remained elevated in the brains of adult fish with FLUX developmental histories, though CT_max was unaffected. Together, these findings suggest that early-life exposure to diel thermal fluctuations induces lasting epigenetic changes, potentially optimizing metabolic performance in the short-term at the cost of reduced capacity for further thermal tolerance and stress recovery later in life.