Hostname: page-component-77c89778f8-n9wrp Total loading time: 0 Render date: 2024-07-18T12:43:06.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Isolation and characterization of microsatellite markers in the queen scallop Aequipecten opercularis and their application to a population genetic study

Published online by Cambridge University Press:  28 April 2010

Alberto Arias ,
Ruth Freire ,
Josefina Méndez  and
Ana Insua
Get access

Abstract

Microsatellites are one of the most popular markers in genetic studies but typically they need to be isolated and characterized de novo for each species. In this work, a genomic library enriched for a trinucleotide motif was constructed to identify polymorphic microsatellite loci in Aequipecten opercularis, a scallop species commercially fished in Europe, and to examine the level of genetic variation and genetic differentiation in samples from Spain and Northern Ireland. Sequencing of 83 clones led to the identification of 30 microsatellite-containing sequences which showed often other repeated sequences. Five microsatellite loci were successfully amplified and found polymorphic. The number of alleles and the expected heterozygosity per locus ranged from 9 to 86 and 0.341 to 0.927, respectively, all localities showing similar levels of genetic variation (allelic richness, 13.164–15.487; expected heterozygosity, 0.527–0.638). Discrepancies in genotype proportions from Hardy-Weinberg equilibrium were observed in 11 out of 25 locality-locus combinations, a heterozygote deficiency occurring in all cases probably due to null alleles. Significant genetic differentiation was detected among A. opercularis from Northern Ireland, Fuengirola (southern Spain) and the homogeneous samples from northwest Spain. Isolation by distance was the most likely hypothesis to explain the differentiation detected.

Keywords

Aequipecten opercularisGenetic variationpopulation differentiationMicrosatellite markerQueen scallop
Type
Research Article
Information
Aquatic Living Resources , Volume 23 , Issue 2 , April 2010 , pp. 199 - 207
Copyright
© EDP Sciences, IFREMER, IRD 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J.H., Zhang, Z., Miller, W., Lipman, D.J., 1997, Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402.CrossRefGoogle ScholarPubMed
An, H.S., Park, J.Y., Lee, Y.G., Lee, D.S., Lee, C., 2005, Ten polymorphic microsatellite loci in the giant scallop (Mizuhopecten yessoensis). Mol. Ecol. Notes 5, 806–808.CrossRefGoogle Scholar
Arias, A., Freire, R., Méndez, J., Insua, A., 2009, Intron characterization and their potential as molecular markers for population studies in the scallops Aequipecten opercularis and Mimachlamys varia . Hereditas 146, 46–57.CrossRefGoogle ScholarPubMed
Arias, A., Freire, R., Boudry, P., Heurtebise, S., Méndez, J., Insua, A., 2009, Single nucleotide polymorphism for population studies in the scallops Aequipecten opercularis and Mimachlamys varia . Conserv. Genet. 10, 1491–1495.CrossRefGoogle Scholar
Balloux, F., Lugon-Moulin, N., 2002, The estimation of population differentiation with microsatellite markers. Mol. Ecol. 11, 155–165.CrossRefGoogle ScholarPubMed
Beaumont A., 2006, Genetics. In: Shumway S. E., Parsons G. J. (Eds.) Scallops: biology, ecology and aquaculture. Amsterdam, Elsevier, pp. 543–594.
Beaumont, A.R., 1982, Geographic-variation in allele frequencies at three loci in Chlamys opercularis from Norway to the Brittany Coast. J. Mar. Biol. Assoc. UK 62, 243–261.CrossRefGoogle Scholar
Beaumont, A.R., Beveridge, C.M., 1984, Electrophoretic survey of genetic variation in Pecten maximus, Chlamys opercularis, Chlamys varia and Chlamys distorta from the Irish Sea. Mar. Biol. 81, 299–306.CrossRefGoogle Scholar
Belkhir K., Borsa P., Chikhi L., Raufaste N., Bonhomme F., 2004, GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier (France). Available from: http://www.genetix.univmontp2.fr/genetix/genetix.htm.
Benson, G., 1999, Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580.CrossRefGoogle ScholarPubMed
Billote, N., Lagoda, P.J.L., Risterucci, A.M., Baurens, F.C., 1999, Microsatellite-enriched libraries: applied methodology for the development of SSR markers in tropical crops. Fruits 54, 277–288.Google Scholar
Boudry, P., Collet, B., Cornette, F., Hervouet, V., Bonhomme, F., 2002, High variance in reproductive success of the Pacific oyster (Crassostrea gigas, Thunberg) revealed by microsatellite-based parentage analysis of multifactorial crosses. Aquaculture 204, 283–296.CrossRefGoogle Scholar
Brand A.R., 2006, The European scallop fisheries for Pecten maximus, Aequipecten opercularis and Mimachlamys varia. In: Shumway S. E., Parsons G. J. (Eds.) Scallops: biology, ecology and aquaculture. Amsterdam, Elsevier, pp. 991–1058.
Brookfield, J.F., 1996, A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5, 453–455.CrossRefGoogle ScholarPubMed
Cabranes, C., Fernandez-Rueda, P., Martinez, J.L., 2008, Genetic structure of Octopus vulgaris around the Iberian Peninsula and Canary Islands as indicated by microsatellite DNA variation. ICES J. Mar. Sci. 65, 12–16.CrossRefGoogle Scholar
Chambers, G.K., MacAvoy, E.S., 2000, Microsatellites: consensus and controversy. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 126, 455–476.CrossRefGoogle ScholarPubMed
Chapuis, M.P., Estoup, A., 2007, Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621–631.CrossRefGoogle ScholarPubMed
Chistiakov, D.A., Hellemans, B., Volckaert, F.A.M., 2006, Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture 255, 1–29.CrossRefGoogle Scholar
Cragg S.M., Crisp D.J., 1991, The biology of scallop larvae. In: Shumway S. E. (Ed.) Scallops: Biology, Ecology and Aquaculture. Amsterdam, Elsevier, pp. 75–132.
Cruz, F., Pérez, M., Presa, P., 2005, Distribution and abundance of microsatellites in the genome of bivalves. Gene 346, 241–247.CrossRefGoogle ScholarPubMed
Diz, A.P., Presa, P., 2008, Regional patterns of microsatellite variation in Mytilus galloprovincialis from the Iberian Peninsula. Mar. Biol. 154, 277–286.CrossRefGoogle Scholar
Edwards, K.J., Barker, J.H.A., Daly, A., Jones, C., Karp, A., 1996, Microsatellite libraries enriched for several microsatellite sequences in plants. BioTechniques 20, 758. Google ScholarPubMed
Evans, B.S., Knauer, J., Taylor, J.J.U., Jerry, D.R., 2006, Development and characterization of six new microsatellite markers for the silver- or gold-lipped pearl oyster, Pinctada maxima (Pteriidae). Mol. Ecol. Notes 6, 835–837.CrossRefGoogle Scholar
Excoffier, L., Laval, G., Schneider, S., 2005, Arlequin version 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform, Online 1, 50. Google Scholar
Fernández-Moreno, M., Arias-Pérez, A., Freire, R., Méndez, J., 2008, Genetic analysis of Aequipecten opercularis and Mimachlamys varia (Bivalvia: Pectinidae) in several Atlantic and Mediterranean localities, revealed by mitochondrial PCR-RFLPs: a preliminary study. Aquac. Res. 39, 474–481.CrossRefGoogle Scholar
Fernández-Tajes, J., Méndez, J., 2007, Identification of the razor clam species Ensis arcuatus, E. siliqua, E. directus, E. macha, and Solen marginatus using PCR-RFLP analysis of the 5S rDNA region. J. Agric. Food Chem. 55, 7278–7282.CrossRefGoogle Scholar
Gaffney P.M., 1994, Heterosis and heterozygote deficiencies in marine bivalves: more light? In: Beaumont A. R. (Ed.) Genetics and evolution of aquatic organisms. London, Chapman & Hall, pp. 146–153.
Goudet J., 2001, FSTAT, a program to estimate and test gene diversities and fixation indices. Institut d’Ecologie, Université de Lausanne, Dorigny, Switzerland.http://www2.unil.ch/popgen/softwares/fstat.htm.
Hall, T.A., 1999, BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
Jensen, J.L., Bohonak, A.J., Kelley, S.T., 2005, Isolation by distance, web service. BMC Genet. 6, 13. CrossRefGoogle ScholarPubMed
Jørgensen, H.B.H., Hansen, M.M., Bekkevold, D., Ruzzante, D.E., Loeschcke, V., 2005, Marine landscapes and population genetic structure of herring (Clupea harengus L.) in the Baltic Sea. Mol. Ecol. 14, 3219–3234.CrossRefGoogle Scholar
Kenchington, E.L., Patwary, M.U., Zouros, E., Bird, C.J., 2006, Genetic differentiation in relation to marine landscape in a broadcast-spawning bivalve mollusc (Placopecten magellanicus). Mol. Ecol. 15, 1781–1796.CrossRefGoogle Scholar
Launey, S., Ledu, C., Boudry, P., Bonhomme, F., Naciri-Graven, Y., 2002, Geographic structure in the European flat oyster (Ostrea edulis L.) as revealed by microsatellite polymorphism. J. Hered. 93, 331–351.CrossRefGoogle ScholarPubMed
Lewis, R.I., Thorpe, J.P., 1994, Temporal stability of gene frequencies within genetically heterogeneous populations of the queen scallop Aequipecten (Chlamys) opercularis . Mar. Biol. 121, 117–126.CrossRefGoogle 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.CrossRefGoogle Scholar
Li, Y.C., Korol, A.B., Fahima, T., Beiles, A., Nevo, E., 2002, Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol. Ecol. 11, 2453–2465.CrossRefGoogle ScholarPubMed
Louis, E.J., Dempster, E.R., 1987, An exact test for Hardy-Weinberg and multiple alleles. Biometrics 43, 805–811.CrossRefGoogle ScholarPubMed
Ma, H., Yu, Z., 2009, Development of twenty-two polymorphic microsatellite loci in the noble scallop, Chlamys nobilis . Conserv. Genet. 10, 1587–1590.CrossRefGoogle Scholar
Macleod, J.A.A., Thorpe, J.P., Duggan, N.A., 1985, A biochemical genetic study of population structure in queen scallop (Chlamys opercularis) stocks in the Northern Irish Sea. Mar. Biol. 87, 77–82.CrossRefGoogle Scholar
Mathers, N.F., 1975, Environmental variability at the phosphoglucose isomerase locus in the genus Chlamys . Biochem. Syst. Ecol. 3, 123–127.CrossRefGoogle Scholar
Meglecz, E., 2007, MICROFAMILY (version 1): a computer program for detecting flanking-region similarities among different microsatellite loci. Mol. Ecol. Notes 7, 18–20.CrossRefGoogle Scholar
Nei, M., 1978, Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.Google ScholarPubMed
Nève, G., Meglécz, E., 2000, Microsatellite frequencies in different taxa. Trends Ecol. Evol. 15, 376–377.CrossRefGoogle ScholarPubMed
Quesada, H., Zapata, C., Alvarez, G., 1995, A multilocus allozyme discontinuity in the mussel Mytilus galloprovincialis: the interaction of ecological and life-history factors. Mar. Ecol. Prog. Ser. 116, 99–115.CrossRefGoogle Scholar
Raymond, M., Rousset, F., 1995, Genepop (Version-1.2): population-genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.CrossRefGoogle Scholar
Reece, K.S., Ribeiro, W.L., Gaffney, P.M., Carnegie, R.B., Allen, S.K. Jr, 2004, Microsatellite marker development and analysis in the eastern oyster (Crassostrea virginica): confirmation of null alleles and non-Mendelian segregation ratios. J. Hered. 95, 346–352.CrossRefGoogle ScholarPubMed
Rice, W.R., 1989, Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle ScholarPubMed
Ríos, C., Sanz, S., Saavedra, C., Pena, J.B., 2002, Allozyme variation in populations of scallops, Pecten jacobaeus (L.) and P. maximus (L.) (Bivalvia: Pectinidae), across the Almeria-Oran front. J. Exp. Mar. Biol. Ecol. 267, 223–244.CrossRefGoogle Scholar
Rychlik, W., Rhoads, R.E., 1989, A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucleic Acids Res. 17, 8543–8551.CrossRefGoogle ScholarPubMed
Vadopalas, B., Leclair, L.L., Bentzen, P., 2004, Microsatellite and allozyme analyses reveal few genetic differences among spatially distinct aggregations of geoduck clams Panopea abrupta (Conrad, 1849). J. Shellfish Res. 23, 693–706.Google Scholar
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004, MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538.CrossRefGoogle Scholar
Wagner, H.P., 1991, Review of the European Pectinidae. Vita Marina 41, 1–48.Google Scholar
Was, A., Gosling, E., McCrann, K., Mork, J., 2008, Evidence for population structuring of blue whiting (Micromesistius poutassou) in the Northeast Atlantic. ICES J. Mar. Sci. 65, 216–225.CrossRefGoogle Scholar
Watts, P.C., Mallanaphy, W.J., McCarthy, C., Beukers-Stewart, B.D., Mosley, M.W.J., Brand, A.R., Saccheri, I.J., 2005, Polymorphic microsatellite loci isolated from the great scallop, Pecten maximus (Bivalvia: Pectinidae). Mol. Ecol. Notes 5, 902–904.CrossRefGoogle Scholar
Weir, B.S., Cockerham, C.C., 1984, Estimating F-statistics for the analysis of population-structure. Evolution 38, 1358–1370.Google ScholarPubMed
Zane, L., Bargelloni, L., Patarnello, T., 2002, Strategies for microsatellite isolation: a review. Mol. Ecol. 11, 1–16.CrossRefGoogle ScholarPubMed
Zhan, A., Bao, Z., Hu, X., Hui, M., Wang, M., Peng, W., Zhao, H., Hu, J., 2007, Isolation and characterization of 150 novel microsatellite markers for Zhikong scallop (Chlamys farreri). Mol. Ecol. Notes 7, 1015–1022.CrossRefGoogle Scholar
Zhan, A., Hu, J., Hu, X., Hui, M., Wang, M., Peng, W., Huang, X., Wang, S., Lu, W., Sun, C., Bao, Z., 2009, Construction of microsatellite-based linkage maps and identification of size-related quantitative trait loci for Zhikong scallop (Chlamys farreri). Anim. Genet. 40, 821–831.CrossRefGoogle Scholar