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ABSTRACT Triploid oysters are commonly used as the basis for production in the aquaculture of eastern oysters along the USA East and Gulf of Mexico coasts. While they are valued for their rapid growth, incidents of triploid mortality during summer months have been well documented in eastern oysters, especially at low salinity sites. We compared global transcriptomic responses of diploid and triploid oysters bred from the same three maternal source populations at two different hatcheries and outplanted to a high (annual mean salinity = 19.4 ± 6.7) and low (annual mean salinity = 9.3 ± 5.0) salinity site. Oysters were sampled for gene expression at the onset of a mortality event in the summer of 2021 to identify triploid‐specific gene expression patterns associated with low salinity sites, which ultimately experienced greater triploid mortality. We also examined chromosome‐specific gene expression to test for instances of aneuploidy in experimental triploid oyster lines, another possible contributor to elevated mortality in triploids. We observed a strong effect of hatchery conditions (cohort) on triploid‐specific mortality (field data) and a strong interactive effect of hatchery, ploidy, and outplant site on gene expression. At the low salinity site where triploid oysters experienced high mortality, we observed downregulation of transcripts related to calcium signaling, ciliary activity, and cell cycle checkpoints in triploids relative to diploids. These transcripts suggest dampening of the salinity stress response and problems during cell division as key cellular processes associated with elevated mortality risk in triploid oysters. No instances of aneuploidy were detected in our triploid oyster lines. Our results suggest that triploid oysters may be fundamentally less tolerant of rapid decreases in salinity, indicating that oyster farmers may need to limit the use of triploid oysters to sites with more stable salinity conditions.

The eastern oyster, Crassostrea virginica, is a keystone species native to the Gulf of Mexico and Atlantic coasts of the United States and Canada. It provides habitat for other marine organisms and makes up the majority of oyster production in the United States. Despite its tolerance to hypoxic conditions, C. virginica is threatened by anthropogenic climate change, which is increasing both average temperature and the frequency and severity of hypoxic events. In this study, we explore the differences in hypoxia-transcriptional response between two populations of eastern oysters with known differences in hypoxia tolerance at three time points over the course of a 5-day hypoxia treatment. We identified sets of genes involved in the hypoxia response and found differences in both the timing and baseline expression of hypoxia-responsive genes between tolerant and sensitive populations, consistent with a scenario of local adaptation. Analysis of differential gene expression between the two populations and conditions revealed two gene modules with higher baseline expression of hypoxia-sensitive genes in the more hypoxia tolerant population. Key GO terms for genes corresponding to differences between populations include DNA repair, ribosome biogenesis, and ribonucleotide binding. Our results imply that differences in hypoxia tolerance between populations could be due to genetic frontloading of hypoxia response pathways in the more tolerant population.