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Genetic Variation in Wild and Hatchery Stocks of Suminoe Oyster (Crassostrea ariakensis) Assessed by PCR-RFLP and Microsatellite Markers

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Abstract

Genetic variation in wild Asian populations and U.S. hatchery stocks of Crassostrea ariakensis was examined using polymerase chain reactions with restriction fragment length polymorphism (PCR-RFLP) analysis of both the mitochondrial COI gene and the nuclear internal transcribed spacer (ITS) 1 region and using 3 microsatellite markers. Hierarchical analysis of molecular variance and pairwise comparisons revealed significant differentiation (P < 0.05) between samples from the northern region, represented by collections from China and Japan, and 2 of 3 samples from southern China. PCR-RFLP patterns were identified that were diagnostic for the northern (N-type) and southern (S-type) groups. Microsatellite marker profiles were used to assign each oyster to one of the two northern or two southern populations. Results for more than 97% of the oysters were consistent with the PCR-RFLP patterns observed for each individual in that oysters with N-type patterns were assigned to one of the northern populations and those with S-type patterns to one of the southern populations. At one site of the Beihai (B) region in southern China a mix of individuals with either the N-type or S-type PCR-RFLP genotypes was found. No heterozygotes at the nuclear ITS-1 locus were found in the sample, possibly indicating reproductive isolation in sympatry. Microsatellite assignment test results of the B individuals were also consistent with identifications as either the N-type or S-type based on PCR-RFLP patterns. The parental population for one hatchery stock was this B sample, which initially was composed of almost equal numbers of northern and southern genetic types. After hatchery spawns, however, more than 97% of the progeny fell into the northern genetic group by PCR-RFLP and microsatellite assignment test analyses, indicating that the individuals with the southern genotype contributed little to the spawn, owing to gametic incompatibility, differential larval survival, or a difference in timing of sexual maturity. Overall, results suggested that oysters collected as C. ariakensis in this study, and likely in other studies as well, include two different sympatric species with some degree of reproductive isolation.

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References

  • Ahmed M (1971) Oyster species of West Pakistan. Pak J Zool 3: 229–236

    Google Scholar 

  • Ahmed M (1975) Speciation in living oysters. Adv Mar Biol 13: 357–397

    Google Scholar 

  • Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Proceedings of the workshop on genetic management of captive populations. Zoo Biol 5: 181–190

    Article  Google Scholar 

  • Band M, Ron M (1997) Heterozygote deficiency caused by a null allele at the bovine AR023 microsatellite. Anim Biotechnol 8: 187–190

    Article  Google Scholar 

  • Barkati S, Khan RM (1987) Relative growth in three species of oysters. Pak J Sci Ind Res 30: 624–627

    Google Scholar 

  • Boudry P, Heurtebise S, Lapègue S (2003) Mitochondrial and nuclear DNA sequence variation of presumed Crassostrea gigas and Crassostrea angulata specimens: a new oyster species in Hong Kong? Aquaculture 228: 15–25

    Article  Google Scholar 

  • Breese WP, Malouf RE (1977) Hatchery rearing techniques for the oyster Crassostrea rivularis Could. Aquaculture 12: 123–126

    Article  Google Scholar 

  • Breitburg D, Luckenback M, Kramer J (2004) Identifying and prioritzing research required to evaluate ecological risks and benefits of introducing diploid Crassostrea ariakensis to restore oysters to Chesapeake Bay. Annapolis, Md.: Report of the STAC Workshop

  • Cagbn AR (1950) Oyster culture in Japan. Fish Leafl Fish Wildl Serv 383: 1–80

    Google Scholar 

  • Cai Y, Li X (1990) Oyster culture in the People’s Republic of China. World Aquaculture 21: 67–72

    Google Scholar 

  • Callen DF, Thompson AD, Shen Y, Phillips HA, Richards RI, Mulley JC, Sutherland GR (1993) Incidence and origin of ‘null’ alleles in the (AC)n microsatellite markers. Am J Hum Genet 52: 922–927

    Google Scholar 

  • Calvo GW, Luckenbach MW, Allen SK Jr, Burrenson EM (2001) A comparative field study of Crassostrea ariakensis (Fujita 1913) and Crassostrea virginica (Gmelin 1791) in relation to salinity in Virginia. J Shellfish Res 20: 221–229

    Google Scholar 

  • Carriker MR, Gaffney PM (1996) A catalogue of selected species of living oysters (Ostrea) of the world. In: The Eastern Oyster, Kennedy VS, Newell REI, Eble AF, eds. Maryland Sea Grant College Publication UM-SG-TS-96-01, 1–18

  • Coan EV, Scott PH, Bernard FR (1995) Bivalve seashells of western North American. In: Marine Bivalve Mollusks from Arctic Alaska to Baja California. (Santa Barbara, Calif: Santa Barbara Museum of Natural History)

  • Coughlan JP, Imsland AK, Galvin PT, Fitzgerald RD, Naevdal G, Cross TF (1998) Microsatellite DNA variation in wild populations and farmed strains of turbot from Ireland and Norway: a preliminary study. J Fish Biol 52: 916–922

    Article  Google Scholar 

  • Egglestontott ML, Delvalle A, Dileanis S, Wictum E, Bowling AT (1997) A single base transversion in the flanking region of an equine microsatellite locus affects amplification of one allele. Anim Genet 28: 438–440

    Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3: 294–299

    Google Scholar 

  • Francis E, Reece KS, Allen SK Jr (2000) Species designation among sympatric oysters Crassostrea ariakensis, C. gigas, and C. sikamea. J Shellfish Res 19, 662–663

    Google Scholar 

  • Galstoff PS (1964) Taxonomy. The American Oyster Crassostrea virginica Gmelin, U.S. Fish Wildlife Serv Fish Bull 64: 1–15

    Google Scholar 

  • Glude JB (1971) Identification of oysters of the South Pacific Islands. (Seattle, Wash.: National Marine Fisheries Service)

    Google Scholar 

  • Gould AA (1861) Descriptions of new species of shells from the North Pacific Exploring Expedition. Proc Boston Soc Nat His 8: 39–46

    Google Scholar 

  • Guo X, Ford S, Zhang F (1999) Mollusca aquaculture in China. J Shellfish Res 18: 19–31

    Google Scholar 

  • Hallerman E, Leffler M, Mills S, Allen SK Jr (2001) Aquaculture of triploid C. ariakensis in Chesapeake Bay: a symposium report. Maryland Publication UM-SG-TS-2002-01, Virginia Publication VSG-02-03

    Google Scholar 

  • Harry HW (1981) Nominal species of living oysters proposed during the last fifty years. Veliger 24: 39–45

    Google Scholar 

  • Hedgecock D, Li G, Banks MA, Kain Z (1999) Occurrence of the Kumamoto oyster Crassostrea sikamea in the Ariake Sea, Japan. Mar Biol 133: 65–68

    Article  Google Scholar 

  • Jones AG, Stockwell A, Walker D, Avise JC (1998) The molecular basis of a microsatellite null allele from the White Sands pupfish. J Heredity 89: 339–342

    Article  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17: 1244–1245

    Article  Google Scholar 

  • Lam K, Morton B (2003) Mitochondrial DNA and morphological identification of a new species of Crassostrea (Bivalvia: Ostreidae) cultured for centuries in the Pearl River Delta, Hong Kong, China. Aquaculture 228: 1–13

    Article  Google Scholar 

  • Li G, Hubert S, Bucklin K, Ribes V, Hedgecock D (2003) Characterization of 79 microsatellite DNA markers in the Pacific oyster Crassostrea gigas. Mol Ecol Notes 3: 228–232

    Article  Google Scholar 

  • Li Y, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11: 2453–2465

    Article  Google Scholar 

  • Littlewood DTJ (1994) Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequence. Mol Phylogenet Evol 3: 221–229

    Google Scholar 

  • Liu B, Dai J (1998) Studies on genetic diversity in oysters, Crasostrea. J Fish China 22: 193–198

    Google Scholar 

  • Mann R, Burreson EM, Baker PK (1991) The decline of the Virginia oyster fishery in Chesapeake Bay: considerations for introduction of non-endemic species, Crassostrea gigas (Thunberg, 1973). J Shellfish Res 10: 379–388

    Google Scholar 

  • McGoldrick DJ, Hedgecock D, English LJ, Baoprasertul P, Ward RD (2000) The transmission of microsatellite alleles in Australian and North American stocks of the Pacific oyster (Crassostrea gigas): selection and null alleles. J Shellfish Res 19: 779–788

    Google Scholar 

  • Naciri Y, Vigouroux Y, Dallas J, Desmarais E, Delsert C, Bonhomme F (1995) Identification and inheritance of (GA/TC)n and (AC/GT)n repeats in the European flat oyster Ostrea edulis (L.). Mol Mar Biol Biotechnol 4: 83–89

    Google Scholar 

  • Nei Z (1982) The culture of marine bivalve mollusks in China. In: Menzel W (ed.).Estuarine and Marine Bivalve Mollusk Culture, Boca Raton, Fla.: CRC Press, 261–276

    Google Scholar 

  • Norris AT, Bradley DG, Cunningham EP (1999) Microsatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations. Aquaculture 180: 247–264

    Article  Google Scholar 

  • Ó’Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7: 331–363

    Google Scholar 

  • O’Foighil D, Smith MJ (1994) Evolution of asexuality in the cosmopolitan marine clam Lasaea. Evolution 49: 140–150

    Google Scholar 

  • O’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. ariankensis (Wakiya). J Exp Mar Biol Ecol 192: 221–220

    Google Scholar 

  • Paetkau D, Calvert W, Sterling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4: 347–354

    Google Scholar 

  • Rao KS (1987) Taxonomy of Indian oysters. In: Nagappan K, Mahadevan S (eds). Oyster Culture-Status and Prospects Cochin, India: Central Marine Fisheries Research Institute, Indian Council of Agricultural Research, 1–6

    Google Scholar 

  • Reece KS, Ribeiro WL, Gaffney PM, Carnegie RB, Allen SK Jr, (2004) Microsatellite marker development and analysis in the eastern oyster, Crassostrea virginica: confirmation of null alleles and non-Mendelian segregation ratios. J Heredity 95: 355–361

    Article  Google Scholar 

  • Reynolds J, Weir BS, Cockerham CC (1983) Estimation of the co-ancestry coefficient: basis for a short-term genetic distance. Genetics 105: 767–779

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223–225

    Google Scholar 

  • Schneider S, Roessli D, Excoffer L (2000) Arlequin: A Software for Population Genetic Data Analysis, Version 2.000. Geneva, Switzerland: Genetic and Biometry Lab., Department of Anthropology, University of Geneva

  • Sekino M, Harab M, Taniguchi N (2002) Loss of microsatellite and mitochondrial DNA variation in hatchery strains of Japanese flounder Paralichthys olivaceus. Aquaculture 213: 101–122

    Article  Google Scholar 

  • Sekino M, Hamaguchi M, Aranishi F, Okoshi K (2003) Development of novel microsatellite DNA markers from the Pacific Oyster Crassostrea gigas. Mar Biotechnol 5: 227–233

    Article  Google Scholar 

  • Smith PJ (1987) Homozygous excess in sand flounder, Rhombosolea plebeia, produced by assortative mating. Mar Biol 95: 489–492

    Google Scholar 

  • Stenzel HB (1971) Oysters. In: Treatise on Invertebrate Paleontology, Moore KK, ed. (Boulder, Calo.: Geol. America Inc. and the University of Kansas) Part N, vol. 3, Mollusca 6

  • Tchang S, Lou T (1956) A study on Chinese Oysters. Acta Zool Sinica 8, 65–93

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370

    Google Scholar 

  • Zhang X, Xie Y (1960) Culture of major bivalves in China. Bull Biol Shengwu Xuebao 5: 197–201

    Google Scholar 

  • Zhuang Q (1992) Research on marine bivalves in the People’s Republic of China. Am Malacol Bull 9: 207–215

    Google Scholar 

  • Zouros E, Foltz DW (1984) Possible explanations of heterozygote deficiency in bivalve mollusks. Malacologica 25: 583–591

    Google Scholar 

  • Zhou M, Allen SK Jr (2003) A reviw of published work on Crassostrea ariakensis. J Shellfish Res 22: 1–20

    Google Scholar 

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Acknowledgments

We thank Karen Hudson for assistance in laboratory procedures and Elizabeth Walker for assisting with oyster hemolymph collection. We thank Dr. Jan McDowell for her advice and assistance in using ARLEQUIN and GENEPOP software and Dr. Jan Cordes for constructive criticism on the manuscript. This work was supported by the Virginia Sea Grant. Project number R/A-33. VIMS contribution number: 2682.

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Correspondence to Kimberly S. Reece.

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Zhang, Q., Allen, S.K. & Reece, K.S. Genetic Variation in Wild and Hatchery Stocks of Suminoe Oyster (Crassostrea ariakensis) Assessed by PCR-RFLP and Microsatellite Markers. Mar Biotechnol 7, 588–599 (2005). https://doi.org/10.1007/s10126-004-5105-7

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