Transgenerational Heat Exposure Triggers Unexpected Compensatory Sex Ratio Responses in a Temperature-Sensitive Fish Under Climate Warming.

Rising global temperatures threaten species with environmental sex determination by skewing population sex ratios. However, predictions of demographic collapse often overlook the potential for multigenerational adaptation mechanisms. Here, we investigated the transgenerational impacts of elevated temperature on sex ratios and reproductive physiology in the European sea bass (Dicentrarchus labrax), a modern teleost with a polygenic sex determination system highly sensitive to temperature. Over more than a decade and using > 3000 fish, we reared three successive generations (F0-F2) under control or elevated temperatures. In this study, we report detailed data from ~1500 juveniles of the F2 generation distributed across eight groups with unique thermal histories. Direct developmental exposure consistently induced masculinization, but we uncovered a novel compensatory parental effect. The influence of ancestral thermal exposure did not follow a simple cumulative pattern. Instead, its direction depends on the line's inherent sex tendency. Paternal lines with baseline sex biases produced offspring with a sex ratio skewed in the opposite direction when exposed to elevated temperatures. This significant plasticity suggests a potential adaptive mechanism that may counteract extreme demographic imbalances. Gonad histological analysis further revealed a significant delay in spermatogenesis in heat-exposed males at one year, whereas female gonadal development and chemical composition were unaffected by temperature. Our findings demonstrate that predicting the impacts of climate change requires a multigenerational perspective. Transgenerational plasticity can generate complex compensatory responses that may enhance demographic resilience, whereas genetic variability among lines can modulate these effects on sex ratios. Whether this phenomenon is unique to sea bass or widespread among other temperature-sensitive species remains to be determined. By integrating ancestral thermal exposure into eco-evolutionary models, our results expand the discussion on population responses to global warming, and highlight the need for comparable multigenerational studies across taxa.