Eastern oysters, Crassostrea virginica, are historically a keystone species in many of the estuaries in which they reside, with an estimated economic value of $5,500–$99,000 ha–1 y–1 [1]. They provide numerous functions that are critical to their ecosystems [2] including water filtration [2, 3], nitrogen conversion [4–6], sanctuary for juvenile fishes in the form of oyster reefs [7], and reducing wave energy from storm surge to protect shorelines [8, 9]. A cause for concern is that eastern oysters have been on the decline throughout the entirety of their range for several decades, which could prove to be catastrophic for some estuarine ecosystems [2, 10, 11], particularly estuaries in New England. The Gulf of Maine, where Great Bay Estuary (GBE), New Hampshire is located, currently is one of the fastest warming regions on Earth, where sea surface temperatures increased at a rate of 0.26°C y− 1 between 2004 and 2012 [12]. Eastern oyster populations in GBE presently are only 10% of what they were in the 1980s, with the most common causes of decline being attributed to disease, over harvesting, lack of substrate, and sedimentation leading to shell burial [13]. Studies that increase our knowledge of eastern oysters and that could lead to increased success of restoration strategies, are of great importance.
Eastern oyster restoration projects in GBE currently are underway through collaborative efforts of multiple agencies, such as the University of New Hampshire, The Nature Conservancy, New Hampshire Sea Grant, and New Hampshire Fish and Game. Restoration efforts from 2000–2018 included deployment of shell, live spat-on-shell, and transplantation of large, reproductively active cultivated oysters (deemed “uglies”) onto pre-selected restoration sites [14]. Following a large spat-on-shell restoration initiative by The Nature Conservancy in 2011, it was observed that approximately 5.8 × 104 oyster spat recruited to a 1-ha reef located at the Lamprey River [15], which subsequently showed indication of natural recruitment [13]. In 2013, a survey of multiple GBE oyster restoration sites indicated some levels of success (i.e. recruitment), but found numerous reef areas where few, if any, live oysters were found post-restoration [14–16]. In a 2015 project, only 3 of 9 sites had numbers of live oysters adequate to constitute a healthy, living oyster reef [13, 14]. A 2019 assessment provided similar results [14]. A 2021 project by The Nature Conservancy, titled “The Purchase Program” under their Supporting Oyster Aquaculture and Restoration initiative, deployed large aquacultured “uglies” at restoration sites (the success of this project is not yet known).
Most studies have emphasized the potential for larval recruitment of oysters in GBE, suggesting that recruitment may be efficient at sites near existing natural reefs with an established adult oyster population [17]. The historic decrease in the eastern oyster adult population in GBE may limit the potential for recruitment from native reefs [13]. Although the rough densities and locations of oysters in GBE are known [18], questions have arisen relating to the number of breeders, gene flow, and the potential for recruitment to both natural and artificial oyster reefs [19]. Because restoration has been challenging in GBE, detailed information on the population structure of eastern oysters in this estuary is needed to enhance restoration efforts.
A contemporary approach to examining population structure, population genomics, interrogates numerous regions of the genome to better understand genetic variation among populations [20]. This approach allows estimation of migration, population differentiation, effective number of breeders, random mating, etc. Historically, management decisions often have been made without consulting important genetic information [21], particularly with respect to marine invertebrates such as the eastern oyster. More recently, genomic studies are being introduced into marine management decisions [22–25]. Such studies (including this one) include several important parameters: inbreeding coefficients (FIS), population subdivision (FST), effective population size (Ne), heterozygosity, and population clustering. More often than not, in many restoration schemes the issue of preserving genetic diversity arises [26] as hatchery-reared individuals that perform better are inadvertently selected without considering the inbreeding consequences of non-random mating. This type of inadvertent selection within a restoration strategy can lead to loss of genetic diversity in the wild and lower effective population sizes [27]. Recent studies of marine oyster populations indicate strong population structure on a fine-scale [28, 29], alluding to the value of understanding these fine-scale population characteristics in estuarine regions to develop more appropriate restoration and management strategies. Bivalve restoration practices, including eastern oysters, commonly include supplementing native populations with hatchery-reared individuals in hopes of increasing total reproductive output, higher recruitment, and ultimately successful reef restoration [13, 15, 30]. This may not be the best strategy because cultivated transplants may have lower Ne, in which case alternative best practices for restoration may be necessary. This study aimed to address such scenarios.
This study used putatively adaptive single nucleotide polymorphisms (SNPs) to answer the necessary questions regarding eastern oyster population genomics in a well-mixed estuarine system. Great Bay Estuary, NH has a unique set of characteristics that separate it from other estuarine systems. Generally small freshwater fluxes (2% of tidal prism) [31] and strong tidal mixing result in negligible stratification (except very close to the river mouths) within the system [32]. Therefore, it is difficult to extend the knowledge from previous eastern oyster population genomics studies in other geographic areas [28, 33, 34] to GBE, as well as other studies from different oyster species, such as Crassostrea gigas [56] and Ostrea lurida [29]. To provide population genomic information to inform GBE restoration practices, low-coverage, whole-genome sequencing (lcWGS) was performed on 210 individuals from 7 different sites in GBE with approximately 5× coverage. The lcWGS approach is a powerful low cost tool that has been shown to be effective for describing population structure [35, 36]. Despite the reduction in depth of coverage and confidence in individual genotype assignment, researchers obtain with lcWGS greater breadth of coverage and larger sample sizes [35]. This study aimed to (1) assess the population genomic structure of cultivated, native, and restoration subpopulations of eastern oysters in GBE, (2) determine levels of genetic differentiation among subpopulations, and (3) estimate the effective breeding size of each subpopulation sampled. Due to the unique characteristics of GBE, especially its well-mixed nature and strong tidal currents [32], it was expected that genomic structure of native oyster groups would be homogenous, that the restoration specimens would show signs of either native or cultivated heritage, whichever group was most successful at that site, and that major differentiation between native and cultivated populations would be evident due to unique heritage and possible reproductive variance effects.