Abstract
Overharvesting, habitat degradation, and disease have resulted in a century of decline for Atlantic Coast populations of the eastern oyster Crassostrea virginica (Gmelin). The introduction of oysters with superior disease resistance (e.g. oysters from different geographical areas, or genetically improved strains) may be useful in restoration efforts. In 1997 the Oyster Recovery Partnership and the University of Maryland Center for Environmental Science planted more than four million Louisiana oysters in the Choptank River, which flows into the Chesapeake Bay, Maryland, USA. These oysters, which may be distinguished from Atlantic oysters by diagnostic single-nucleotide polymorphisms (SNPs) in their mitochondrial DNA, were expected to display enhanced survival and reproduction as a result of their superior resistance to Dermo disease. A high-throughput, synthesis-by-sequencing technique (Pyrosequencing) was used to determine the mitochondrial haplotypes of spat collected in the Choptank River and nearby regions of the bay. Of 3,545 spat collected in 1999, 2000, and 2001, 3,349 (94.47%) possessed the North Atlantic haplotype, 176 (4.68%) had the South Atlantic haplotype, and 3 individuals (0.08%) had the Gulf Coast haplotype. Detection of newly recruited oysters possessing the Gulf Coast haplotype in the Choptank River confirmed the survival and reproduction of the outplanted Louisiana oysters. If appropriate genetic tags are available, effective monitoring of stock-enhancement projects can be achieved with high-throughput molecular genoty** techniques.
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References
Abbe GR, Sanders JG (1988) Rapid decline in oyster condition in the Patuxent River, Maryland. J Shellfish Res 7:57–59
Alderborn A, Kristofferson A, Hammerling U (2000) Determination of single-nucleotide polymorphisms by real-time pyrophosphate DNA sequencing. Genome Res 10:1249–1258
Andrews JD (1983) Transport of bivalve larvae in James River, Virginia. J Shellfish Res 3:29–40
Andrews JD, Hewatt WG (1957) Oyster mortality studies in Virginia. II. The fungus disease caused by Dermocystidium marinum in oysters of Chesapeake Bay. Ecol Monogr 27:1–25
Andrews JD, McHugh JL (1957) The survival and growth of South Carolina seed oysters in Virginia waters. Proc Natl Shellfish Assoc 47:3–17
Avise JC (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63:62–76
Banks MA, Hedgecock D, Waters C (1993) Discrimination between closely related Pacific oyster species (Crassostrea) via mitochondrial DNA sequences coding for large subunit rRNA. Mol Mar Biol Biotechnol 2:129–136
Boicourt WC (1982) Estuarine larval retention mechanisms on two scales. In: Kennedy VS (ed) Estuarine comparisons. Academic, New York, pp 445–457
Bushek D (1994) Dermo disease in American oysters: genetics of host parasite interactions. PhD dissertation, Rutgers University, New Brunswick, N.J., USA
Campbell NJH, Harriss FC, Elphinstone MS, Baverstock PR (1995) Outgroup heteroduplex analysis using temperature gradient gel electrophoresis: high resolution, large scale, screening of DNA variation in the mitochondrial control region. Mol Ecol 4:407–418
Carlton JT, Mann R (1996) Transfers and world-wide introductions. In: Kennedy VS, Newell RIE (eds) The eastern oyster, Crassostrea virginica. Maryland Sea Grant, College Park, pp 691–706
Carriker MR (1951) Ecological observations on the distribution of oyster larvae in New Jersey estuaries. Ecol Monogr 21:19–38
Carvalho GR, Hauser L (1994) Molecular genetics and the stock concept in fisheries. Rev Fish Biol Fishes 4:326–350
Coe WR (1934) Alternation of sexuality in oysters. Am Nat 68:236–251
Crozier WW, Moffett IJJ (1995) Application of low frequency genetic marking in GPI-3* and MDH-B1,2* loci to assess supplementary stocking of Atlantic salmon, Salmo salar L., in a Northern Irish stream. Fish Manag Ecol 2:27–36
Ford SE (1985) Effects of salinity on survival of the MSX parasite Haplosporidium nelsoni (Haskin, Stauber, and Mackin) in oysters. J Shellfish Res 5:85–90
Ford SE, Tripp MR (1996) Diseases and defense mechanisms. In: Kennedy VS, Newell RIE (eds) The eastern oyster, Crassostrea virginica. Maryland Sea Grant, College Park, pp 581–660
Gaffney PM (1996) Biochemical and population genetics. In: Kennedy VS, Newell RIE (eds) The eastern oyster, Crassostrea virginica. Maryland Sea Grant, College Park, pp 423–442
Gaffney PM, Bushek D (1996) Genetic aspects of disease resistance in oysters. J Shellfish Res 15:135–140
Garcia de Leaniz C, Verspoor E, Hawkins AD (1989) Genetic determination of the contribution of stocked and wild Atlantic salmon, Salmo salar L., to the angling fisheries in two Spanish rivers. J Fish Biol 35:261–270
Grewe PM, Krueger CC, Marsden JE, Aquadro CF, May B (1994) Hatchery origins of naturally produced lake trout fry captured in Lake Ontario: temporal and spatial variability based on allozyme and mitochondrial DNA data. Trans Am Fish Soc 123:309–320
Haley LE (1977) Sex determination in the American oyster. J Hered 68:114–116
Haley LE (1979) Genetics of sex determination in the American oyster. Proc Natl Shellfish Assoc 69:54–57
Hare MP, Karl S, Avise JC (1996) Anonymous nuclear DNA markers in the American oyster and their implications for the heterozygote deficiency phenomenon in marine bivalves. Mol Biol Evol 13:334–345
Harrison RG (1989) Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends Ecol Evol 4:6–11
Haven DS, Hargis WJ, Kendall PC (1978) The oyster industry of Virginia: its status, problems and promise. Virginia Institute of Marine Science, Gloucester Point
Hayes PF, Menzel RW (1981) The reproductive cycle of early setting Crassostrea virginica (Gmelin) in the northern Gulf of Mexico, and its implications for population recruitment. Biol Bull (Woods Hole) 160:80–88
Kennedy VS (1980) Comparison of recent and past patterns of oyster settlement and seasonal fouling in Broad Creek and Tred Avon River, Maryland. Proc Natl Shellfish Assoc 70:36–46
Kennedy VS (1996) Biology of larvae and spat. In: Kennedy VS, Newell RIE (eds) The eastern oyster, Crassostrea virginica. Maryland Sea Grant, College Park, pp 371–421
Kessing B, Croom H, Mcintosh A, McMillan O, Palumbi S (1989) The simple fool’s guide to PCR. Department of Zoology, University of Hawaii, Honolulu
King TL, Ward RD, Gold JR (1995) Using genetics in the design of red drum and spotted seatrout stocking programs in Texas: a review. Am Fish Soc Symp 15:499–502
Korringa P (1952) Recent advances in oyster biology. Q Rev Biol 27:266–308
Krantz GE, Meritt DW (1977) An analysis of trends in oyster spat set in the Maryland portion of the Chesapeake Bay. Proc Natl Shellfish Assoc 67:53–59
Kristiansen TS, Jørstad KE, Otterå H, Paulsen OI, Svåsand T (1997) Estimates of larval survival of cod by releases of genetically marked yolk-sac larvae. J Fish Biol 51:264–283
Kwok PY (2001) Methods for genoty** single nucleotide polymorphisms. Annu Rev Genom Hum Genet 2:235–258
Lessa EP (1992) Rapid screening of DNA sequence variation in natural populations. Mol Biol Evol 9:323–330
Meritt DW (1977) Oyster spat set on natural cultch in the Maryland portion of the Chesapeake Bay (1939–1975). CEES special report, Horn Point Environmental Laboratory, University of Maryland, Cambridge
Milbury CA (2003) Using mitochondrial DNA markers to monitor oyster stock enhancement in the Choptank River, Chesapeake Bay. MS thesis, University of Delaware, Lewes
Moran P, Pendas AM, Garcia-Vazqeuz E, Izquierdo J (1991) Failure of a stocking policy, of hatchery reared brown trout, Salmo trutta L., in Asturias, Spain, detected using LDH-5* as a genetic marker. J Fish Biol 39:117–121
Ó Foighil D, Gaffney PM, Hilbish TJ (1995) Differences in mitochondrial 16S ribosomal gene sequences allow discrimination among American [Crassostrea virginica (Gmelin)] and Asian [C. gigas (Thunberg) C. ariakensis Wakiya] oyster species. J Exp Mar Biol Ecol 192:211–220
Oliver JL, Gaffney PM, Allen JSK, Faisal M, Kaattari S (2000) Protease inhibitory activity in selectively bred families of eastern oysters. J Aquat Anim Health 12:136–145
Reeb CA, Avise JC (1990) A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124:397–406
Ronaghi M (2001) Pyrosequencing sheds light on DNA sequencing. Genome Res 11:3–11
Saunders NC, Kessler LG, Avise JC (1986) Genetic variation and geographic differentiation in mitochondrial DNA of the horseshoe crab, Limulus polyphemus. Genetics 112:613–627
Sheffield VC, Cox DR, Myers RM (1990) Identifying DNA polymorphisms by denaturing gradient gel electrophoresis PCR protocols: a guide to methods and applications. Academic, New York, pp 206–218
Small MP, Chapman RW (1997) Intraspecific variation in the 16S ribosomal gene of Crassostrea virginica. Mol Mar Biol Biotechnol 6:189–196
Smith GF, Roach EB, Bruce DG (2003) The location, composition, and origin of oyster bars in mesohaline Chesapeake Bay. Estuar Coast Shelf Sci 56:391–409
Wakefield JR (1997) Sequence variation in the mitochondrial large subunit (16S) ribosomal gene of the American oyster, Crassostrea virginica. MS thesis, University of Delaware, Lewes
Wakefield JR, Gaffney PM (1996) DGGE reveals additional population structure in American oyster (Crassostrea virginica) populations. J Shellfish Res 15:513
Ward RD, Grewe PM (1994) Appraisal of molecular genetic techniques in fisheries. Rev Fish Biol Fishes 4:300–325
Wilson RRJ, Donaldson KA (1998) Restriction digest of PCR-amplified mtDNA from fin clips is an assay for sequence genetic “tags” among hundreds of fish in wild populations. Mol Mar Biol Biotechnol 7:39–47
Acknowledgements
We would like to recognize S. Tobash and C. Epifanio for their invaluable support and assistance. We would also like to thank K. Paynter and T. Koles for the dive survey data and input. This research was funded by the NMFS Saltonstall–Kennedy Program, Delaware Sea Grant, the Paul R. Austin Student Sea Grant Fellowship, and the Oyster Recovery Partnership.
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Communicated by J.P. Grassle, New Brunswick
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Milbury, C.A., Meritt, D.W., Newell, R.I.E. et al. Mitochondrial DNA markers allow monitoring of oyster stock enhancement in the Chesapeake Bay. Marine Biology 145, 351–359 (2004). https://doi.org/10.1007/s00227-004-1312-z
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DOI: https://doi.org/10.1007/s00227-004-1312-z