Polyploidy has been suggested to negatively impact environmental stress tolerance, resulting in increased susceptibility to extreme climate events. In this study, we compared the genomic and physiological response of diploid (2n) and triploid (3n) Pacific oysters (Crassostrea gigas) to conditions present during an atmospheric heatwave that impacted the Pacific Northwestern region of the United States in the summer of 2021. Climate stressors were applied either singly (single stressor; elevated seawater temperature, 30°C) or in succession (multiple stressor; elevated seawater temperature followed by aerial emersion at 44°C), replicating conditions present within the intertidal over a tidal cycle during the event. Oyster mortality rate was elevated within stress treatments with respect to the control and was significantly higher in triploids than diploids following multiple stress exposure (36.4% vs. 14.8%). Triploids within the multiple stressor treatment exhibited signs of energetic limitation, including metabolic depression, a significant reduction in ctenidium Na+/K+ ATPase activity, and the dysregulated expression of genes associated with stress response, innate immunity, glucose metabolism, and mitochondrial function. Functional enrichment analysis of ploidy‐specific gene sets identified that biological processes associated with metabolism, stress tolerance, and immune function were overrepresented within triploids across stress treatments. Our results suggest that triploidy impacts the transcriptional regulation of key processes that underly the stress response of Pacific oysters, resulting in downstream shifts in physiological tolerance limits that may increase susceptibility to extreme climate events that present multiple environmental stressors. The impact of chromosome set manipulation on the climate resilience of marine organisms has important implications for domestic food security within future climate scenarios, especially as triploidy induction becomes an increasingly popular tool to elicit reproductive control across a wide range of species used within marine aquaculture.

Polyploidy has been shown to negatively impact environmental stress tolerance, resulting in increased susceptibility to extreme climate events such as marine heatwaves (MHWs). In this study, we used the response of the Pacific oysterCrassostrea gigasto MHWs as a model system to identify key ploidy-specific differences in the physiological and transcriptomic response of oysters to environmental stress. In this study, adult diploid (2n) and triploid (3n) oysters were exposed to elevated seawater temperature (single stressor; 30°C), elevated temperature followed by acute desiccation stress (multiple stressor; 30°C + emersion at an aerial temperature of 44°C for 4h), or a control (17°C) within a hatchery setting. Oyster mortality rate was elevated within stress treatments with respect to the control and was significantly higher in triploids than diploids following multiple stress exposure (36.4% vs. 14.8%). Triploids within the multiple stressor treatment exhibited signs of energetic limitation, including metabolic depression, a significant reduction in ctenidium Na+/K+ATPase activity, and the dysregulated expression of key genes associated with heat tolerance, the inhibition of apoptosis, and mitochondrial function. Functional enrichment analysis of ploidy-specific gene sets identified that biological processes associated with metabolism, stress tolerance, and immune function were overrepresented within triploids across stress treatments. Our results demonstrate that triploidy impacts the transcriptional regulation of key metabolic processes that underly the environmental stress response of Pacific oysters, resulting in downstream shifts in physiological tolerance limits that may be detrimental to survival. The impact of chromosome set manipulation on the climate resilience of marine populations has important implications for the adaptability of marine populations and domestic food security within future climate scenarios, especially as triploidy induction becomes an increasingly popular tool to elicit reproductive control across a wide range of marine organisms used within marine aquaculture.