Award: OCE-1756698

Natural selection acts incrementally across generations to generate local adaptation across diverse habitats within a species range. The spatial scale of local adaptation is well understood to be a function of the strength of selection causing differentiation, the population size, and the magnitude and spatial breadth of dispersal-mediated gene flow. This classical theory leads to an expectation that there is little variation of interest in populations at spatial scales below average dispersal distance – all the interesting stuff happens between populations. A poorly explored exception to this generality involves species with very high offspring number per female and both dispersal and high mortality occur during early life history stages. In this project we tested the hypothesis that genomic variation in such species will show spatially and temporally dynamic responses caused by differential survivorship to environmental variation at small spatial scales relative to average dispersal distance. We focused on Eastern oysters (Crassostrea virginica) in Delaware Bay, and their ability to withstand stressful discharges of fresh water into the top of the estuary after storm events. Climate change models predict that the frequency and magnitude of such storms will increase. We collected adult oysters along a salinity gradient transect in each of three years. Historical salinity variation in Delaware Bay was analyzed with freshwater discharge rates to derive a model predicting bottom salinity at any time and place on the oyster beds based on river discharge. We used the model to estimate duration of exposure to stressful low salinity for our oyster collections. In two of the three years, long periods of very low salinity at the top of the bay caused locally elevated adult oyster mortality. Based on whole genome sequencing of transect population samples, and a test for association between low salinity exposure and genetic variant frequencies, each of two methods identified more than a thousand chromosomal loci with significant associations. Conservatively, the 119 DNA variants shared between methods were considered candidate loci responding to within-generation hyposalinity selection. Two experimental hyposalinity challenges of adults resulted in similarly polygenic within-generation responses to selection. For both the environmentally associated candidate loci, and the experimental challenge candidates, many were within genes with hypothesized functions. The gene functions that were statistically over-represented in both sets of results included cytoskeletal organization, motor protein function and regulation of ion transport – functions hypothesized to modify osmoregulation and responses to prolonged shell closure (hypoxia). Additional genomic metrics showed that these candidate loci are experiencing spatial balancing selection that can maintain elevated levels of genetic diversity, thereby promoting rapid evolutionary responses to environmental change. Further experiments on juvenile oysters (spat), using both hatchery-reared and wild caught spat, helped identify the impact of acute salinity changes applied at larval settlement or during postsettlement spat growth. In general, hyposalinity treatments slowed growth as expected, but early hyposalinity stress also elicited compensatory increases in later growth. Thus, in a robust, abundant oyster population we found that short term responses to environmental change included classical modes of phenotypic plasticity as well as dynamic, localized within-generation selection reshaping variation likely related to cytoskeletal and ion transporter phenotypes. Last Modified: 02/10/2023 Submitted by: Daphne M Munroe