Geographic variation in nuclear genes of the eastern oyster, Crassostrea virginica Gmelin

Journal of Shellfisheries Research, Jan, 2005 by Cindi A. Hoover, Patrick M. Gaffney

ABSTRACT The eastern oyster, Crassostrea virginica Gmelin, is a common inhabitant of estuarine and coastal waters from maritime Canada through the Gulf of Mexico. Because mitochondrial DNA haplotypes exhibit a distinct genetic break between Atlantic and Gulf oysters at Cape Canaveral, Florida, the degree of divergence between Atlantic and Gulf oysters in nuclear genes is less well known. We examined patterns of variation in four nuclear loci using restriction fragment analysis of amplified DNA (PCR-RFLP) in oysters (n = 317) from 16 locations spanning the geographic range of C. virginica. Marked differentiation was observed between Atlantic and Gulf populations, with smaller differences detected between North Atlantic and South Atlantic populations. Intermediate populations were observed in both eastern and northwest Florida. Regional population structure was also evident in the Gulf Coast, with Texas oysters highly divergent from all other populations.

KEY WORDS: Crassostrea virginica, oyster, genetics, nuclear DNA, RFLP

INTRODUCTION

The eastern oyster, Crassostrea virginica Gmelin, supports an important shellfish industry along the coasts of the Atlantic Ocean and the Gulf of Mexico. Its native range extends from the Gulf of St. Lawrence, Canada to the Gulf of Mexico. Reports of C. virginica from the Caribbean and South America (e.g., Nirchio et al. 2000) must be considered provisional, because the morphologically similar C. gasar has been observed in Brazil (Lapegue et al. 2002) and Venezuela (Gaffney, unpubl.).

Given the economic value of C. virginica, much interest has arisen in improving oyster stocks decimated during the last century by overfishing and disease (Galtsoff 1964, Ford & Haskin 1982, Rothschild et al. 1994). However, to allow effective enhancement of native oyster stocks, a better understanding of their basic population structure is essential. In particular, a more accurate picture of how intraspecific genetic diversity is distributed geographically will provide biologic guidance for regulating the transport of oysters, and for the selection of broodstock for hatchery-based restoration programs. Delineation and preservation of genetic variation is a central element in conservation biology programs, where the main goal is the survival and continued evolution of a species (Avise 1994, Driscoll 1998). Molecular genetic data, along with ecologic and morphologic data, can help inform efforts to preserve genetic and evolutionary diversity in a threatened or declining species (Mace et al. 1996).

Like most benthic marine invertebrates, C. virginica has a planktonic larval stage, which is in principle capable of widespread dispersal. If this occurs, then neutral (nonselected) genes should exhibit homogeneity across the geographic range of the species. However, evidence of geographic heterogeneity has been reported in both mitochondrial DNA (mtDNA) and nuclear DNA (nDNA) in C. virginica (Reeb & Avise 1990, Karl & Arise 1992, Hare & Arise 1996). Mitochondrial DNA haplotypes form 2 major assemblages, Atlantic (Gulf of St. Lawrence to Cape Canaveral) and Gulf Coast (including the Atlantic coast of Florida south of Cape Canaveral).

A similar genetic break has been observed in the distributions of other organisms such as the horseshoe crab, toadfish, and diamondback terrapin (Saunders et al. 1986, Avise et al. 1987). The geographical concordance in mtDNA divergence across species suggests a common set of historical factors initiating population genetic divergence and similar restrictions to gene flow (Reeb & Avise 1990). Considering the amount of mitochondrial DNA sequence divergence, Reeb and Avise (1990) estimated that the two oyster populations separated about 1.2 million years ago.

In addition, regional genetic discontinuities have been observed, particularly in peripheral populations. For example, oysters inhabiting Laguna Madre, Texas showed substantial genetic divergence from adjacent populations at 6 of 15 allozyme loci (King et al. 1994). Similarly, a comparison of samples from Florida and Nova Scotia showed fixation for alternative alleles at several allozyme loci (Buroker et al. 1979). This differentiation may be attributed to random genetic drift and/or natural selection in populations isolated by hydrogeographic barriers. For example, the distinct genetic composition of the Laguna Madre population has been attributed to prevailing currents that prevent transport of larvae in or out of the Laguna Madre (King et al. 1994). Genetic divergence may also be facilitated by natural selection. Laguna Madre oysters exhibit enhanced tolerance to hypersalinity, a factor which may serve both as a barrier to gene flow and as an agent of natural selection.

However, unlike mtDNA, studies of intraspecific differentiation in nuclear genes have yielded mixed results. Early allozyme surveys suggested little geographic differentiation over the entire species range, with the exception of peripheral populations (Buroker 1983, Gaffney 1996), although a reanalysis of Buroker's original data revealed a genetic break between Gulf and Atlantic populations (Cunningham & Collins 1994). In this case, the breakpoint occurred in northwest Florida, in contrast to that of mtDNA, which occurred on the Atlantic coast of Florida.