Skewed sex ratio and gametogenesis gene expression in eastern oysters (Crassostrea virginica) exposed to plastic pollution

Abstract

Plastic pollution is ubiquitous in the oceans, and numerous studies have documented the dangers from entanglement, ingestion, or exposure to individual xenoestrogenic plastic additives. Plastic degradation in seawater poses a complex threat through sorption of harmful organic pollutants, release of complex chemical ingredients that compose plastics, and fragmentation of plastic pieces. Therefore, a more holistic approach is needed to understand the impact of plastic exposure on marine organisms. The eastern oyster (Crassostrea virginica) is a keystone species that serves as an ecosystem engineer in western Atlantic estuaries. Individuals undergo annual gametogenesis and are able to change sex from one year to the next, typically from male to female. A 1:1 sex ratio is maintained at the population level by younger/smaller oysters that are mostly male and older/larger oysters that are mostly female. As sessile bivalves, oysters are susceptible to damaging effects from plastic that settle on the seafloor. The objective of this study was to quantify changes in survival, growth, sex ratio, and gene expression of eastern oysters in response to polyethylene terephthalate (PET) plastic exposure. Hatchery-produced larvae settled onto either oyster shell or PET plastic and metamorphosed into juveniles. One set of juvenile oysters was reared in an aquaculture facility for three months, and a second set was placed on natural reefs in the St. Mary's River of the Chesapeake Bay for ten months. Juvenile oysters grown on PET showed significantly higher mortality rates and reduced growth than those grown on shell after three months. After ten months of growth and maturation in natural waters, oysters grown on shell were 82% male while oysters grown on plastic had a significantly lower proportion of males (56% male). We measured differential gene expression of eight candidate genes involved in gametogenesis. In general, expression patterns followed expectations based on putative roles in either spermatogenesis or oogenesis. Exposure to plastic did not have a significant impact on gene expression. Small sample sizes limited statistical power to detect small effect sizes. Although not significant, females on plastic had higher median and mean expression than those on shell for all genes, except for the mean expression level of vitellogenin-6 (vit-6). Our findings suggest that plastic exposure alters the sex ratio of first-year oysters, resulting in more females than expected. Additional research into the expression of underlying genes that impact gamete differentiation and therefore sex determination is warranted.