Thermal stress induces dual damages to physiology and reproductive capacity of Galaxea fascicularis during its reproductive stage.

Driven by ocean warming and intensifying marine heatwaves, increasingly frequent and severe coral bleaching events are causing declines in coral populations worldwide. Post-disturbance coral population recovery relies heavily on sexual reproduction, yet this reproductive process often sustains long-term detrimental impacts under thermal stress. Here, we investigated the effects of varying degrees of thermal stress on physiological function and reproductive capacity, as well as the underlying molecular responses in the heat-resistant coral Galaxea fascicularis. Our results showed that even 7 days at 29 °C induced mild coral bleaching accompanied by significant declines in physiological performance and sexual reproductive capacity, highlighting the vulnerability of corals during their reproductive period. KEGG enrichment analysis of the coral host transcriptome indicated that glutathione metabolism, peroxisome, and the TCA cycle were significantly enriched for upregulated genes. Meanwhile, the Symbiodiniaceae community shifted from clade C17 to C1, with a high abundance of thermotolerant microbes of the family Rhodothermaceae. Together, these changes might indicate the recovery potential of mildly bleached corals. However, when thermal stress intensified to 32 °C, there was a massive loss of symbiotic Symbiodiniaceae, severe depletion of energy reserves, and significant reductions in oocyte size and abundance. Downregulated genes were significantly enriched in the base excision repair and mRNA surveillance pathways, which may predict the emergence of irreversible cellular damage. Findings of this study advance our understanding of how broadcast-spawning G. fascicularis responds to varying degrees of thermal stress, and highlight the necessity of assessing environmental tolerance in corals during the reproductive period.