Global warming and biological adaptation: Thermal priming buffers the impact of heatwaves on the reproductive health of the Mediterranean mussel Mytilus galloprovincialis

Human excessive exploitation of natural resources has undermined the fragile balance of many ecosystems, accelerating global warming at unprecedented rates. Marine heatwaves (MHWs) threaten organisms, whose reproductive cycle is temperature-dependent. The impact of climate change was evaluated on reproductive health of the gonochoric Mediterranean mussel Mytilus galloprovincialis. Specimens were divided into a control group, maintained constantly at 17 ± 1 °C, and groups pre-adapted separately to 28, 30 and 32 °C for 2 h, returned to the control temperature for 24 h, and then exposed to heat shock (36 °C) for 2 h. A group directly exposed to 36 °C (dTS) was used to simulate MHWs. The mitigation of early spawning events induced by dTS and recall of basophilic haemocytes suggested that thermal priming implements remodelling strategies against high temperature in mussel gonads of both sexes. Metabolic enrichment and biological networks were consistent with NMR-based metabolomics, showing that bioenergy (glucose, succinate, lactate, mytilitol) is managed differently in male and female gonads, as confirmed by dPAS/PAS results highlighting a differential modulation of energy reserves (glycogen). Sex-dependent changes in defence mechanisms (glutamate, histidine) indicated that females are more sensitive to temperature, while the phenoloxidase activity appeared more resistant to heat shock in males. Overall, this study contributes to better understand the impact of current and projected global warming on the reproductive health and fitness of farmed aquatic shellfish, supporting thermal priming as an adaptive strategy in a sex-dependent manner to enhance tolerance to heat stress and resilience in key ecological species with high socio-economic value, especially farmed shellfish.