Award Abstract # 1756698
Collaborative Research: Spatial analysis of genetic differences in salinity tolerance resulting from rapid natural selection in estuarine oysters

NSF Org: OCE
Division Of Ocean Sciences
Recipient: RUTGERS, THE STATE UNIVERSITY
Initial Amendment Date: March 30, 2018
Latest Amendment Date: March 30, 2018
Award Number: 1756698
Award Instrument: Standard Grant
Program Manager: Cynthia Suchman
csuchman@nsf.gov
 (703)292-2092
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: December 15, 2018
End Date: May 31, 2022 (Estimated)
Total Intended Award Amount: $291,700.00
Total Awarded Amount to Date: $291,700.00
Funds Obligated to Date: FY 2018 = $291,700.00
History of Investigator:
  • Daphne Munroe (Principal Investigator)
    dmunroe@hsrl.rutgers.edu
Recipient Sponsored Research Office: Rutgers University New Brunswick
3 RUTGERS PLZ
NEW BRUNSWICK
NJ  US  08901-8559
(848)932-0150
Sponsor Congressional District: 12
Primary Place of Performance: Rutgers University Haskin Shellfish Research Lab
6959 Miller Ave
Port Norris
NJ  US  08349-3167
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): M1LVPE5GLSD9
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001819DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1174, 4444, 7377, 8214
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

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.

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

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
Modified by: Daphne M Munroe

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