Collaborative Research: Spatial analysis of genetic differences in salinity tolerance resulting from rapid natural selection in estuarine oysters

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Many marine animals have a bipartite life cycle consisting of a stationary bottom-dwelling adult stage and a mobile larval stage. The flow of water transports these larval offspring, and their genes, to different habitat patches. It is thought that animals from nearby patches will be more genetically similar than animals in patches that are further in proximity, but these patterns of genetic similarity may not be maintained if the nearby patches have different habitat characteristics. This idea is fundamental to our understanding of adaptation and evolution, but it has not been adequately tested with respect to the effects of rapid selection. This study applies new technologies to test if the genetic signatures of marine animals change even when patches with different environmental characteristics are closer together than the dispersal distance of larvae. This research focuses on eastern oysters (Crassostrea virginica) in Delaware Bay, and their ability to withstand variability in the amount of salt in the water. This study will provide new insights on factors that control oyster survival and growth in estuaries with different salinity profiles. The three investigators are sharing study results with resource managers and stakeholders to improve shellfish restoration and oyster stock management in Delaware Bay, Chesapeake Bay, and New York. A postdoctoral scholar at Cornell and graduate student at the University of Maryland are being trained and mentored during the project. The investigators are also working with teacher training programs in New York and New Jersey to develop and disseminate new curriculum materials on oyster ecology for middle-school students.The project will investigate whether hyposalinity tolerance of oysters is a function of viability selection during larval dispersal and after settlement. Gene flow across salinity zones within an estuary is expected to be high enough that adaptive differentiation will not result from Darwinian multigenerational processes. Instead, recurrent viability selection in each generation is expected to generate spatial variation in this trait at small spatial scales. This type of recurrent within-generation adaptation has been referred to as phenotype-environment mismatches and has been hypothesized to generate balanced polymorphisms, but it has never been studied beyond single gene cases. The project team is testing for spatially discrete patterns of selection by first collecting oysters from different salinity zones, measuring variation in their tolerance to low salinity and then testing for associations between this trait and genomic variation using whole genome sequencing. Experimental hyposalinity challenges enable within-generation, before/after genomic comparisons to identify DNA variants that change as a result of strong viability selection. Candidate genes and selectively neutral control loci will be assayed in larval, juvenile, and adult samples from the same salinity zones to test for an association between variation at candidate loci and lifetime hyposalinity exposure. Two years of environmental data will be collected and added to an existing long-term data set to map salinity variation. The observed spatial distribution of hyposalinity tolerance and genomic variation associated with it provide a test that could definitively reject the prevalent assumption that all larvae have similar capabilities. If larvae differ by parental source for traits that differentially affect their viability in the plankton, then phenotype-environment mismatches can have profound consequences for population connectivity. This project improves understanding about mechanisms that shape realized larval dispersal and recruitment variation in oyster populations.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.