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Comparative study of shell shape and muscle scar pigmentation in the closely related cupped oysters Crassostrea angulata,C. gigas and their reciprocal hybrids

Published online by Cambridge University Press:  05 April 2008

Frederico M. Batista ,
Radhouan Ben-Hamadou ,
Vera G. Fonseca ,
Nicolas Taris ,
Francisco Ruano ,
Maria A. Reis-Henriques  and
Pierre Boudry
Frederico M. Batista
Affiliation:
Instituto Nacional de Investigação Agrária e das Pescas (INIAP/IPIMAR), CRIPSul, Av. 5 de Outubro, 8700-305 Olhão, Portugal Instituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Largo Prof. Abel Salazar 2, 4099-003 Porto, Portugal
Radhouan Ben-Hamadou
Affiliation:
Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
Vera G. Fonseca
Affiliation:
Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Laboratoire de Génétique et Pathologie (LGP), 17390 La Tremblade, France
Nicolas Taris
Affiliation:
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Laboratoire de Génétique et Pathologie (LGP), 17390 La Tremblade, France
Francisco Ruano
Affiliation:
Instituto Nacional de Investigação Agrária e das Pescas (INIAP/IPIMAR), Departamento de Aquicultura, Av. de Brasília, 1449-006 Lisboa, Portugal
Maria A. Reis-Henriques
Affiliation:
Instituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Largo Prof. Abel Salazar 2, 4099-003 Porto, Portugal
Pierre Boudry
Affiliation:
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Laboratoire de Génétique et Pathologie (LGP), 17390 La Tremblade, France
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Abstract

The taxonomic status of the cupped oysters Crassostrea angulata and C. gigas has received considerable attention in the last decades. Based on larval shell morphology, experimental hybridization, allozymes and nuclear DNA studies several authors have considered these two taxa as being synonymous. However, mitochondrial data showed clear genetic differences between the two taxa. In addition, microsatellite-based studies and cytogenetic studies have also provided evidence that supports their differentiation. Considerable differences have also been observed at the phenotypic level in terms of growth rate and ecophysiological parameters. In the present study, C. angulata from Sado estuary (Portugal) and C. gigas from Seudre estuary (France) were collected and factorial crosses were performed. Juveniles of the different progenies were reared in Ria Formosa (Portugal) under common conditions to determine if they exhibited differences in shell shape and in pigmentation of the adductor muscle scar. Significant morphometric differences between C. angulata and C. gigas progenies were indicated by univariate and multivariate analyses. Univariate analysis of size-adjusted shell measurements revealed significant differences between the two taxa for shell depth, muscle scar height, and length of ligamental area. Both reciprocal hybrids showed intermediate morphometric characters between parental lines. In addition, significant differences were also observed between C. angulata and C. gigas progenies in terms of pigmentation of adductor muscle scar. C. angulata and both reciprocal hybrid progenies showed highly pigmented adductor muscle scars whereas in C. gigas progeny the pigmentation was lighter. The differences in shell shape and muscle scar pigmentation observed in the present study support the distinction of the two taxa.

Keywords

Shell morphologyShell pigmentationHybridizationCrassostrea angulataCrassostrea gigas
Type
Research Article
Information
Aquatic Living Resources , Volume 21 , Issue 1 , January 2008 , pp. 31 - 38
Copyright
© EDP Sciences, IFREMER, IRD, 2008

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References

Anderson, M.J., 2001, A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32-46.
Batista, F.M., Leitão, A., Fonseca, V.G., Ben-Hamadou, R., Ruano, F., Henriques, M.A., Guedes-Pinto, H., Boudry, P., 2007, Individual relationship between aneuploidy of gill cells and growth rate in the cupped oysters Crassostrea angulata, C. gigas and their reciprocal hybrids. J. Exp. Mar. Biol. Ecol. 352, 226-233. CrossRef
Biocca, E., Matta, F., 1982, Crassostrea angulata (Lamarck, 1819), synonyme de Crassostrea gigas (Thunberg, 1793): études morphologiques et génétiques. Parasitologia 24, 211-222.
Boudry, P., Heurtebise, S., Collet, B., Cornette, F., Gérard, A., 1998, Differentiation between populations of the Portuguese oyster, Crassostrea angulata (Lamark) and the Pacific oyster, Crassostrea gigas (Thunberg) revealed by mtDNA RFLP analysis. J. Exp. Mar. Biol. Ecol. 226, 279-291. CrossRef
Boudry, P., Heurtebise, S., Lapègue, S., 2003, Mitochondrial and nuclear DNA sequence variation of presumed Crassostrea gigas and C. angulata specimens: a new oyster species in Hong Kong? Aquaculture 228, 15-25. CrossRef
Bougrier S., Raguenes G., Bachere E., Tige G., Grizel H., 1986, Essai de réimplantation de Crassostrea angulata en France. Résistance au chambrage et comportement des hybrides C. angulata – C. gigas. ICES, CM 1986/F: 38, 10 p.
Brake, J., Evans, F., Langdon, C., 2003, Is beauty in the eye of the beholder? Development of a simple method to describe desirable shell shape for the Pacific oyster industry. J. Shellfish Res. 22, 767-771.
Brake, J., Evans, F., Langdon, C., 2004, Evidence for genetic control of pigmentation of shell and mantle edge in selected families of Pacific oysters, Crassostrea gigas. Aquaculture 229, 89-98. CrossRef
Buroker, N.E., Hershberger, 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. CrossRef
Comps M., 1988, Epizootic diseases of oysters associated with viral infections. In: FisherW. S. (ed.), Disease processes in marine bivalve molluscs. Am. Fish. Soc. Spec. Publ. Bethesda, MD 8, 23-37.
Dillon, R.T., Manzi, J.J., 1989, Genetics and shell morphology in a hybrid zone between the hard clams Mercenaria mercenaria and M. campechiensis. Mar. Biol. 100, 217-222. CrossRef
Fabioux, C., Huvet, A., Lapègue, S., Heurtebise, S., Boudry, P., 2002, Past and present geographical distribution of populations of Portuguese (Crassostrea angulata) and Pacific (C. gigas) oysters along the European and north African Atlantic coasts. Haliotis 31, 33-44.
FAO, 2006, Global aquaculture production 1950-2004. FIGIS, fisheries global information system. http://www.fao.org/
Galtsoff, P.S., 1964, The American oyster Crassostrea virginica Gmelin. Fish. Bull. US 64, 1-480.
Gardner, J.P.A., 2004, A historical perspective of the genus Mytilus (Bivalvia: Mollusca) in New Zealand: multivariate morphometric analyses of fossil, midden and contemporary blue mussels. Biol. J. Linn. Soc. 82, 329-344. CrossRef
Goulletquer, P., Wolowicz, M., Latala, A., Geairon, P., Huvet, A., Boudry, P., 1999, Comparative analysis of oxygen consumption rates between cupped oyster spat of Crassostrea gigas of French, Japanese, Spanish and Taiwanese origins. Aquat. Living Resour. 12, 271-277. CrossRef
Guo, X., Ford, S.E., Zhang, F., 1999, Molluscan aquaculture in China. J. Shellfish Res. 18, 19-31.
Harry, H.W., 1985, Synopsis of the supraspecific classification of living oysters (Bivalvia: Gryphaeidae and Ostreidae). Veliger 28, 121-158.
Haure, J., Huvet, A., Palvadeau, H., Nourry, M., Penisson, C., Martin, J.L.Y., Boudry, P., 2003, Feeding and respiratory time activities in the cupped oysters Crassostrea gigas, Crassostrea angulata and their hybrids. Aquaculture 218, 539-551. CrossRef
Hedgecock, D., Li, G., Hubert, S., Bucklin, K., Ribes, V., 2004, Widespread null alleles and poor cross-species amplification of microsatellite DNA loci cloned from the Pacific oyster, Crassostrea gigas. J. Shellfish Res. 23, 379-385.
Héral M., Deslous-Paoli J.M., 1991, Oyster culture in European countries. In: Menzel W. (ed.), Estuarine and marine bivalve mollusk culture. CRC Press, Boca Raton, Florida, pp. 153-190.
His, E., 1972, Premiers éléments de comparaison entre l'huître portugaise et l'huître japonaise. Bull. Inst. Pêches Marit. 219, 1-9.
Huvet, A., Lapègue, S., Magoulas, A., Boudry, P., 2000, Mitochondrial and nuclear DNA phylogeography of Crassostrea angulata, the Portuguese oyster endangered in Europe. Conserv. Gen. 1, 251-262. CrossRef
Huvet, A., Gérard, A., Ledu, C., Phélipot, P., Heurtebise, S., Boudry, P., 2002, Is fertility of hybrids enough to conclude that the oysters Crassostrea gigas and Crassostrea angulata are the same species? Aquat. Living Resour. 15, 45-52. CrossRef
Imai, T., Sakai, S., 1961, Study of breeding of Japanese oyster, Crassostrea gigas. Tohoku J. Agric. Res. 12, 125-171.
Innes, D.J., Bates, J.A., 1999, Morphological variation of Mytilus edulis and Mytilus trossulus in eastern Newfoundland. Mar. Biol. 133, 691-699. CrossRef
Lapègue, S., Batista, F.M., Heurtebise, S., Yu, Z., Boudry, P., 2004, Evidence for the presence of the Portuguese oyster, Crassostrea angulata, in Northern China. J. Shellfish Res. 23, 759-763.
Lawrence, D.R., 1995, Diagnosis of the genus Crassostrea (Bivalvia, Ostreidae). Malacologia 36, 185-202.
Leitão, A., Boudry, P., Labat, J.P., Thiriot-Quiévreux, C., 1999a, Comparative karyological study of cupped oyster species. Malacologia 41, 175-186.
Leitão, A., Thiriot-Quiévreux, C., Boudry, P., Malheiro, I., 1999b, A “G” chromosome banding study of three cupped oyster species: Crassostrea gigas, Crassostrea angulata and Crassostrea virginica (Mollusca: Bivalvia). Genet. Sel. Evol. 31, 519-527. CrossRef
Leitão, A., Chaves, R., Santos, S., Guedes-Pinto, H., Boudry, P., 2004, Restriction enzyme digestion chromosome banding in Crassostrea and Ostrea species: comparative karyological analysis within Ostreidae. Genome 47, 781-788. CrossRef
Leitão, A., Chaves, R., Santos, S., Guedes-Pinto, H., Boudry, P., 2007, Interspecific hybridization in oysters: Restriction Enzyme Digestion Chromosome Banding confirms Crassostrea angulata $\times $ Crassostrea gigas F1 hybrids. J. Exp. Mar. Biol. Ecol. 343, 253-260. CrossRef
López-Flores, I., Hérran, R., Garrido-Ramos, M.A., Boudry, P., Ruiz-Rejón, C., Ruiz-Rejón, M., 2004, The molecular phylogeny of oysters based on a satellite DNA related to transposons. Gene 339, 181-188. CrossRef
Mahon, G.A.T., 1983, Selection goals in oyster breeding. Aquaculture 33, 141-148. CrossRef
Mallet, A.L., Carver, C.E., 1995, Comparative growth and survival patterns of Mytilus trossulus and Mytilus edulis in Atlantic Canada. Can. J. Fish. Aquat. Sciences 52, 1873-1880. CrossRef
Mathers, N.F., Wilkins, N.P., Walne, P.R., 1974, Phosphoglucose isomerase and esterase phenotypes in Crassostrea angulata and C. gigas. Biochem. System. Ecol. 2, 93-96. CrossRef
Mattiucci, S., Villani, F., 1983, Allozyme study in oysters classified as Crassostrea gigas (Thunberg, 1793) and Crassostrea angulata (Lamark, 1819) (Mollusca: Ostreidae). Parasitologia 25, 21-27.
McCoy, M.W., Bolker, B.M., Osenberg, C.W., Miner, B.G., Vonesh, J.R., 2006, Size correction: comparing morphological traits among populations and environments. Oecologia 148, 547-554. CrossRef
McDonald, J.H., Seed, R., Koehn, R.K., 1991, Allozymes and morphometric characteristics of three species of Mytilus in the northern and southern hemispheres. Mar. Biol. 11, 323–333 CrossRef
Menzel, R.W., 1974, Portuguese and Japanese oysters are the same species. J. Fish. Res. Board Can. 31, 453-456. CrossRef
O'Foighil, D., Gaffney, P.M., Wilbur, A.E., Hilbish, T.J., 1998, Mitochondrial cytochrome oxidase I gene sequences support an Asian origin for the Portuguese oyster Crassostrea angulata. Mar. Biol. 131, 497-503. CrossRef
Parsons, K.J., Robinson, B.W., Hrbek, T., 2003, Getting into shape: an empirical comparison of traditional truss-based morphometric methods with a newer geometric method applied to New World cichlids. Environ. Biol. Fishes 67, 417–431. CrossRef
Poulet, S.A., Lennon, J., Plouvenez, F., Jalabert, F., Correc, G., Cueff, A., Lacoste, A., 2003, A nondestructive tool for the measurement of muscle strength in juvenile oysters Crassostrea gigas. Aquaculture 217, 49-60. CrossRef
Quayle, D.B., 1988, Pacific oyster culture in British Columbia. Can. Bull. Fish. Aquat. Sci. 218, 241.
Ranson, G., 1960, Les prodissoconques (coquilles larvaires) des ostréides vivants. Bull. Inst. Océanogr. Monaco 1, 1-41.
Soletchnik, P., Huvet, A., Le Moine, O., Razet, D., Geairon, P., Faury, N., Goulletquer, P., Boudry, P., 2002, A comparative field study of growth, survival and reproduction of Crassostrea gigas, C. angulata and their hybrids. Aquat. Living Resour. 15, 243-250. CrossRef
Stenzel H.B., 1971, Oysters. In: Moore K.C. (ed.) Treatise on invertebrate paleontology Part N. Vol. 3. Mollusca 6. Boulder Colorado. Geological Society of America Inc, Boulder, Colorado and the University of Kansas, Lawrence, pp N935-N1224.
Stephano, J.L., Gould, M., 1988, Avoiding polyspermy in the oyster (Crassostrea gigas). Aquaculture 73, 295-307. CrossRef
Taris, N., Ernande, B., McCombie, H., Boudry, P., 2006, Phenotypic and genetic consequences of size selection at the larval stage in the Pacific oyster (Crassostrea gigas). J. Exp. Mar. Biol. Ecol. 333, 147-158. CrossRef
Wada, K.T., 1994, Genetics of pearl oyster in relation to aquaculture. Jap. Agric. Res. Quart. 28, 276-282.
Ward R.D., Thompson P.A., Appleyard S.A., Swan A.A., Kube P.D., 2005, Sustainable genetic improvement of Pacific oysters in Tasmania and South Australia. CSIRO, Fisheries Research Development.
Wilbur, A.E., Gaffney, P., 1997, A genetic basis for geographic variation in shell morphology in the bay scallop, Argopecten irradians. Mar. Biol. 128, 97-105. CrossRef
Wilding, C.S., Latchford, J., Beaumont, A.R., 1998, An investigation of possible stock structure in Pecten maximus (L.) using multivariate morphometrics, allozyme electrophoresis and mitochondrial DNA polymerase chain reaction-restriction fragment length polymorphism. J. Shellfish Res. 17, 131-139.