Skip to main content
SpringerLink
Log in

Allozyme variation in European populations of the oyster Ostrea edulis

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Variations at 22 enzyme coding loci were surveyed in 11 populations of the oyster Ostrea edulis L., which were sampled between 1988 and 1990 along the Atlantic and Mediterranean coasts of Europe. Atlantic oyster beds suffered a steady decline during the last century, and restocking of beds with oysters of foreign origin has probably resulted in a high degree of interbreeding of natural oyster stocks from all Atlantic Europe. Our study confirms the low levels of genetic variability previously reported for the oyster populations from the Atlantic coasts, and extends it to the Mediterranean coasts. The locus arginine-kinase (ARK *) exhibited a high degree of interpopulation differentiation (F ST=0.289), resulting from extensive variation in gene frequencies along a geographical cline. However, the overall genetic differentiation between populations was slight, and similar to that reported for other local populations of bivalves (mean genetic distance between populations is 0.010, mean F ST=0.062). A general pattern of increasing differentiation along the coastline in an Atlantic-mediterranean direction emerged; but genetic differentiation among the Atlantic populations was not significantly lower than that observed among the Mediterranean populations. This and other results suggest that the effects of extensive transplantation of oysters among various areas in Europe are detectable only in some particular localities. The geographical distribution of low-frequency alleles suggests a restriction to gene flow outwards from the Mediterranean Sea, across the Straits of Gibraltar.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Alderman, D. J. (1979). Epizootiology of Marteilia refringens in Europe. Mar. Fish. Rev. 41: 67–69

    Google Scholar 

  • Alvarez, G., Zapata, C., Amaro, R., Guerra, A. (1989). Multilocus heterozygosity at protein loci and fitness in the European oyster, Ostrea edulis L. Heredity, Lond. 63: 359–372

    Google Scholar 

  • Andrews, J. D. (1979). Pelecypoda: Ostreidae. In: Giese, A. C., J. S. Pearse (eds.) Reproduction of marine invertebrates. Vol. 5. Pelecypods and lesser classes. Academic Press, New York

    Google Scholar 

  • Bachère, E., Grizel, H. (1983). Receptivité de trois populations naturelles d'huîtres plates Ostrea edulis L. au protozoaire Bonamia ostreae (Pichot et al., 1980). Revue Trav. Inst. (scient. tech.) Pêch. marit. 47: 234–240

    Google Scholar 

  • Beaumont, A. R. (1991). Genetic studies of laboratory reared mussels, Mytilus edulis: heterozygote deficiencies, heterozygosity and growth. Biol. J. Linn. Soc. 44: 273–285

    Google Scholar 

  • Blanc, F., Jaziri, H., Durand, P. (1986a). Isolement génétique et taxonomie des huîtres plates dans une lagune du sud de la Méditerranée Occidentale. C. r. hebd. Séanc. Acad. Sci., Paris 303: 207–210

    Google Scholar 

  • Blanc, F., Pichot, P., Attard, J. (1986b). Genetic variability in the European oyster, Ostrea edulis: geographic variation between local French stocks. Aquaculture, Amsterdam 57: 362–363 [Gall, G. A. E., Busack, C. A. (eds.) Genetics in aquaculture II. 2nd International Symposium, Davis 1985 (Abstract)]

    Google Scholar 

  • Buroker, N. E. (1982). Allozyme variation in three nonsibling Ostrea species. J. Shellfish Res. 2: 157–163

    Google Scholar 

  • Buroker, N. (1985). Evolutionary patterns in the family Ostreidae: larviparity vs oviparity. J. exp. mar. Biol. Ecol. 90: 233–247

    Google Scholar 

  • Buroker, N. E., Hersberger, W. K., Chew, K. K. (1979). Population genetics of the family Ostreidae. I. Intraspecific studies of Crassostrea gigas and Saccostrea commercialis. Mar. Biol. 54: 157–169

    Google Scholar 

  • Collier, A. W. (1970). Oceans and coastal waters as life-supporting environments. In: Kinne, O. (ed.) Marine ecology. Vol I. Environmental factors. Wiley-Interscience, London, p. 1–91

    Google Scholar 

  • Dando, P. R., Storey, K. B., Hochachka, P. W., Storey, J. M. (1981). Multiple dehydrogenases in marine molluses: electrophoretic analysis of alanopine dehydrogenase, strombine dehydrogenase, octopine dehydrogenase and lactate dehydrogenase. Mar. Biol. Lett. 2: 249–257

    Google Scholar 

  • Endler, J. A. (1977). Geographic variation, speciation and clines. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Gaffney, P., Scott, T. M., Koehn, R. K., Diehl, W. J. (1990). Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics, Austin, Tex. 124: 687–699

    Google Scholar 

  • Galleguillos, R. A., Ward, R. D. (1982). Genetic and morphological divergence between population of the flatfish Platichtys flesus (L.) (Pleuronectidae). Biol. J. Linn. Soc. 17: 395–408

    Google Scholar 

  • Grant, W. S., Cherry, M. I. (1985). Mytilus galloprovincialis Lmk in South Africa. J. exp. mar. Biol. Ecol. 90: 179–191

    Google Scholar 

  • Green, R. H., Singh, S. M., Hicks, B., McCuaig, J. M. (1983). An aretic intertidal population of Macoma balthica (Mollusca, Pelecypoda): genotypic and phenotypic components of population structure. Can. J. Fish. aquat. Sciences 40: 1360–1371

    Google Scholar 

  • Hedgecock, D., Okazaki, N. B. (1984). Genetic diversity within and between populations of American oysters (crassostrea). Malacologia 25: 535–549

    Google Scholar 

  • Hilbish, T. J., Koehn, R. K. (1985). Dominance in physiological phenotypes and fitness at an enzyme locus. Science, N.Y. 229: 52–54

    Google Scholar 

  • Hsü, K. J., Montadert, L., Bernoulli, D., Cita, M. B., Erickson, A., Garrison, R. E., Kidd, R. B., Mèliéres, F., Müller, C., Wright, R. (1977). History of the Mediterranean salinity crisis. Nature, Lond. 267: 399–403

    Google Scholar 

  • Johannesson, K., Rödström, M. E., Aase, H. (1989). Low genetic variability in Scandinavian populations of ostrea edulis L. Possible causes and implications. J. exp. mar. Biol. Ecol. 128: 177–190

    Google Scholar 

  • Koehn, R. K., Gaffney, P. M. (1984). Genetic heterozygosity and growth rate in Mytilus edulis. Mar. Biol. 82: 1–7

    Google Scholar 

  • Koehn, R. K., Milkman, R., Mitton, J. B. (1976). Population genetics of marine pelecypods. IV. Selection, migration and genetic differentiation in the blue mussel Mytilus edulis. Evolution, Lawrence, Kansas 30: 2–32

    Google Scholar 

  • Koehn, R. K., Newell, R. I. E., Immernann, F. W. (1980). Maintenance of an aminopeptidase allele frequency cline by natural selection. Proc. natn. Acad. Sci. U.S.A. 77: 5385–5389

    Google Scholar 

  • Korringa, P. (1941). Experiments and observations on swarming, pelagic life and setting in the European flat oyster, Ostrea edulis L. Archs néer. Zool. 5: 1–249

    Google Scholar 

  • Le Pennec, M., Moraga, D., Blanc, F., Pichot, P., Thiriot-Quievreux, C. (1985). Recherche de différences morphogénétiques, biochimiques et cytogénétiques entre Ostrea edulis sensu stricto et O. edulis “pied de cheval”. Vie mar. 7: 29–39

    Google Scholar 

  • Magennis, B. A., Gosling, E., Wilkins, N. P. (1983). Irish oyster populations: a historical and genetic study. Proc. R. Ir. Acad. 83 B: 291–299

    Google Scholar 

  • McArdle, J. F., McKiernan, F., Foley, H., Jones, D. H. (1991). The current status of Bonamia disease in Ireland. Aquaculture, Amsterdam 93: 273–278

    Google Scholar 

  • Montes, J. (1991). Lag time for infestation of flat oyster (Ostrea edulis L.) by Bonamia ostreae in estuaries of Galicia (N. W. Spain). Aquaculture, Amsterdam 93: 235–239

    Google Scholar 

  • Nei, M. (1977). F-statistics and analysis of gene diversity in subdivided populations. Ann. hum. Genet. 41: 225–233

    Google Scholar 

  • Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, Austin, Tex. 89: 583–590

    Google Scholar 

  • Nei, M. (1987). Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei, A. H., Hull, C. H., Jenkins, J. G., Steinbrenner, K., Bent, D. H. (1970). SPSS statistical package for the social sciences. 2nd ed. McGraw-Hill, New York

    Google Scholar 

  • Pérès, J. M. (1989). Historia de la biota mediterranea y la colonización de las profundidades. In: Margalef (ed.) El mediterráneo occidental. Omega, Barcelona, p. 200–234

    Google Scholar 

  • Powers, D. A., Lauerman, T., Crawford, D., DiMichele, L. (1991). Genetic mechanisms for adapting to a changing environment. A. Rev. Genet. 25: 629–659

    Google Scholar 

  • Robertson, A., Hill, W. G. (1984). Deviations from Hardy-Weinberg proportions: sampling variances and use in estimation of inbreeding coefficients. Genetics, Austin Tex. 107: 703–718

    Google Scholar 

  • Rodríguez, J. (1982). Oceanografia del mar mediterráneo. Ediciones Pirámide, Madrid

    Google Scholar 

  • Rohlf, F. J. (1990). NTSYS-pc. Numerical taxonomy and multivariate analysis system. Version 1.60. Exeter Software, Setauket

    Google Scholar 

  • Saavedra, C. (1991). Variabilidad alozímica en Ostrea edulis L.: estructura genética de poblaciones naturales y relación de la heterozigosis con caracteres cuantitativos. Tesis doctoral; Universidad de Santiago de Compostela

  • Saavedra, C., Zapata, C., Guerra, A., Alvarez, G. (1987). Genetic structure of populations of flat oyster (Ostrea edulis [Linneo, 1758]) from the NW of the Iberian Peninsula. Investigación pesq. 51: 225–241

    Google Scholar 

  • Schaal, B. A., Anderson, W. W. (1974). An outline of techniques for starch gel electrophoresis of enzymes from the American oysters, Crassostrea virginica Gmelin. Tech. Rep. Ser. Ga mar. Sci. Cent. Savannah A 74(3): 1–17

    Google Scholar 

  • Singh, S. M. (1982). Enzyme heterozygosity associated with growth at different developmental stages in oysters. Can. J. Genet. Cytol. 24: 451–458

    Google Scholar 

  • Singh, S. M., Zouros, E. (1978). Genetic variation associated with growth rate in the American oyster (Crassostrea virginica). Evolution, Lawrence, Kansas 32: 342–353

    Google Scholar 

  • Skibinski, D. O. F., Beardmore, J. A., Cross, T. F. (1983). Aspects of the population genetics of Mytilus (Mytilidae; Mollusca) in the British Isles. Biol. J. Linn. Soc. 19: 137–183

    Google Scholar 

  • Sneath, P. H. A., Sokal, R. R. (1973). Numerical taxonomy. W. H. Freeman & Company, San Francisco.

    Google Scholar 

  • Swofford, D. L., Selander, R. K. (1989). BIOSYS-1. A computer program for the analysis of allelic variation in population genetics and biochemical systematics. Illinois Natural History Survey, Champaign

    Google Scholar 

  • Thiede, J. (1978). A glacial Mediterranean. Nature, Lond. 276: 680–683

    Google Scholar 

  • Tintore, J., La Violette, P. E., Blade, I., Cruzado, A. (1988). A study of an intense density front in the Eastern Alboran Sea: the Almeria-Oran front. J. phys. Occanogr. 18: 1384–1397

    Google Scholar 

  • Van Banning, P. (1991). Observations on bonamiasis in the stock of the European flat oyster, Ostrea edulis, in the Netherlands, with special reference to the recent developments in Lake Grevelingen. Aquaculture, Amsterdam 93: 205–211

    Google Scholar 

  • Wilkins, N. P., Mathers, N. F. (1973). Enzyme polymorphisms in the European oyster, Ostrea edulis L. Anim. Blood Grps biochem. Genet. 4: 41–47

    Google Scholar 

  • Yonge, C. M. (1960). Oysters. 2nd ed. Collins, London

    Google Scholar 

  • Zouros, E., Foltz, D. W. (1984). Possible explanations of heterozygote deficiency in bivalve molluscs. Malacologia 25: 583–591

    Google Scholar 

  • Zouros, E., Romero-Dorey, M., Mallet, A. L. (1988). Heterozygosity and growth in marine bivalves: further data and possible explanations. Evolution, Lawrence, Kansas 42: 1332–1341

    Google Scholar 

  • Zouros, E., Singh, S. M., Miles, H. E. (1980). Growth rate in oysters: an overdominant genotype and its possible explanations. Evolution, Lawrence, Kansas 34: 856–867

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Biología Fundamental, Facultad de Biología, Universidad de Santiago de Compostela, E-15706, Santiago de Compostela, Spain

    C. Saavedra, C. Zapata & G. Alvarez

  2. Centro de Investigacións Mariñas, Consellería de Pesca, Xunta de Galicia, E-36600, Vilagarcía de Arousa (Pontevedra), Spain

    A. Guerra

Authors
  1. C. Saavedra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Zapata
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. M. Pérès, Marseille

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saavedra, C., Zapata, C., Guerra, A. et al. Allozyme variation in European populations of the oyster Ostrea edulis . Marine Biology 115, 85–95 (1993). https://doi.org/10.1007/BF00349389

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00349389

Keywords

Search

Navigation