Abstract
Linkage disequilibrium (LD) can be applied for mapping the actual genes responsible for variation of economically important traits through association mapping. The feasibility and efficacy of association studies are strongly dependent on the extent of LD which determines the number and density of markers in the studied population, as well as the experimental design for an association analysis. In this study, we first characterized the extent of LD in a wild population and a cultured mass-selected line of Pacific oyster (Crassostrea gigas). A total of 88 wild and 96 cultured individuals were selected to assess the level of genome-wide LD with 53 microsatellites, respectively. For syntenic marker pairs, no significant association was observed in the wild population; however, three significant associations occurred in the cultured population, and the significant LD extended up to 12.7 cM, indicating that strong artificial selection is a key force for substantial increase of genome-wide LD in cultured population. The difference of LD between wild and cultured populations showed that association studies in Pacific oyster can be achieved with reasonable marker densities at a relatively low cost by choosing an association mapping population. Furthermore, the frequent occurrence of LD between non-syntenic loci and rare alleles encourages the joint application of linkage analysis and LD mapping when mapping genes in oyster. The information on the linkage disequilibrium in the cultured population is useful for future association mapping in oyster.
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Allendorf, F. W., 1986. Genetic drift and the loss of alleles versus heterozygosity. Zoo Biology, 5(2): 181–190.
Appleyard, S. A., and Ward, R. D., 2006. Genetic diversity and effective population size in mass selection lines of Pacific oyster (Crassostrea gigas). Aquaculture, 254 (1-4): 148–159.
Barnaud, A., Laucou, V., This, P., Lacombe, T., and Doligez, A., 2010. Linkage disequilibrium in natural French grapevine, Vitis vinifera L. subsp. Silvestris Heredity, 104: 431–437.
Baxter, I., Brazelton, J. N., Yu, D., Huang, Y. S., Lahner, B., Yakubova, E., Li, Y., Bergelson, J., Borevitz, J. O., Nordborg, M., Vitek, O., and Salt, D. E., 2010. A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT 1: 1. PLoS Genetics, 6: e1001193.
Bradbury, P. J., Zhang, Z., Kroon, D. E., Casstevens, T. M., Ramdoss, Y., and Buckler, E. S., 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23(19): 2633–2635.
Brazauskasa, G., Lenkb, I., Pedersenb, M. G., Studerc, B., and Lübberstedt, T., 2011. Genetic variation, population structure, and linkage disequilibrium in European elite germplasm of perennial ryegrass. Plant Science, 181(4): 412–420.
Chapuis, M. P., and Estoup, A., 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Ecology Evolution, 24: 621–631.
Cong, R. H., and Li, Q., 2014. Selective breeding of fast-growing Crassostrea gigas strains and association analyses of important functional genes with growth and glycogen content traits. PhD thesis. Ocean University of China.
Conrad, D. F., Jakobsson, M., Coop, G., Wen, X. Q., Wall, J. D., Rosenberg, N. A., and Pritchard, J. K., 2006. A worldwide survey of haplotype variation and linkage disequilibrium in the human genome. Nature Genetics, 38: 1251–1260.
Dégremont, L., Bédier, E., and Boudry, P., 2010. Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). II. Response to selection for survival and its influence on growth and yield. Aquaculture, 299 (1-4): 21–29.
Dieringer, D., and Schlötterer, C., 2003. Microsatellite analyser (MSA): A platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 3(1): 167–169.
Du, F. X., Clutter, A. C., and Lohuis, M. M., 2007. Characterizing linkage disequilibrium in pig populations. International Journal of Biological Sciences, 3(3): 166–178.
Evans, S., and Langdon, C., 2006. Direct and indirect responses to selection on individual body weight in the Pacific oyster (Crassostrea gigas). Aquaculture, 261: 546–555.
Famoso, A. N., Zhao, K. Y., Clark, R. T., Tung, C. W., Wright, M. H., Bustamante, C., Kochian, L. V., and McCouch, S. R., 2011. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genetics, 7: e1002221.
Farnir, F., Coppieters, W., Arranz, J.-J., Berzi, P., Cambisano, N., Grisart, B., Karim, L., Marcq, F., Moreau, L., Mni, M., Nezer, C., Simon, P., Vanmanshoven, P., Wagenaar, D., and Georges, M., 2000. Extensive genome-wide linkage disequilibrium in cattle. Genome Research, 10 (2): 220–227.
Flint-Garcia, S. A., Thornsberry, J. M., and Buckler, E. S., 2003. Structure of linkage disequilibrium in plants. Annual Review of Plant Biology, 54: 357–374.
Georges, M., 2007. Mapping, fine Mapping, and molecular dissection of quantitative trait loci in domestic animals. Annual Review of Genomics and Human Genetics, 8: 131–162.
Goudet, J., 2001. FSTAT: A program to estimate and test gene diversities and fixation indices (Version 2.9.3). Available from http://www.unil.ch/dee/page36921_en.html.
Gray, M. M., Granka, J. M., Bustamante, C. D., Sutter, N. B., Boyko, A. R., Zhu, L., Ostrander, E. A., and Wayne, R. K., 2009. Linkage disequilibrium and demographic history of natural and domestic canids. Genetics, 181(4): 1493–1505.
Guo, X., Li, Q., Wang, Q. Z., and Kong, L. F., 2012. Genetic mapping and QTL analysis of growth-related traits in the Pacific oyster. Marine Biotechnology, 14(2): 218–226.
Gupta, P. K., Rustgi, S., and Kulwal, P. L., 2005. Linkage disequilibrium and association studies in higher plants: Present status and future prospects. Plant Molecular Biology, 57(4): 461–485.
Hubert, S., and Hedgecock, D., 2004. Linkage maps of microsatellite DNA markers for the Pacific oyster Crassostrea gigas. Genetics, 168(1): 351–362.
Karim, L., Takeda, H., Lin, L., Druet, T., Arias, J. A. C., Baurain, D., Cambisano, N., Davis, S. R., Farnir, F., Grisart, B., Harris, B. L., Keehan, M. D., Littlejohn, M. D., Spelman, R. J., Georges, M., and Coppieters, W., 2011. Variants modulating the expression of a chromosome domain encompassing PLAG1 influence bovine stature. Nature Genetics, 43(5): 405–413.
Kump, K. L., Bradbury, P. J., Wisser, R. J., Buckler, E. S., Belcher, A. R., Oropeza-Rosas, M. A., Zwonitzer, J. C., Kresovich, S., McMullen, M. D., Ware, D., Balint-Kurti, P. J., and Holland, J. B., 2011. Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nature Genetics, 43: 163–168.
Lam, H. M., Xu, X., Liu, X., Chen, W. B., Yang, G. H., Wong, F. L., Li, M. W., He, W. M., Qin, N., Wang, B., Li, J., Jian, M., Wang, J., Shao, G. H., Wang, J., Sun, S. M., and Zhang, G. Y., 2010. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nature Genetics, 42: 1053–1059.
Lander, E. S., 2011. Initial impact of the sequencing of the human genome. Nature, 470: 187–197.
Launey, S., and Hedgecock, D., 2001. High genetic load in the Pacific oyster Crassostrea gigas. Genetics, 159: 255–265.
Li, L., and Guo, X. M., 2004. AFLP-based genetic linkage maps of the Pacific oyster Crassostrea gigas Thunberg. Marine Biotechnology, 6(1): 26–36.
Li, M. H., and Merilä, J., 2010. Extensive linkage disequilibrium in a wild bird population. Heredity, 104: 600–610.
Li, M. H., and Merilä, J., 2011. Population differences in levels of linkage disequilibrium in the wild. Molecular Ecology, 20(14): 2916–2928.
Li, Q., Wang, Q. Z., Liu, S. K., and Kong, L. F., 2011. Selection response and realized heritability for growth in three stocks of the Pacific oyster Crassostrea gigas. Fisheries Science, 77: 643–648.
Li, Q., Yu, H., and Yu, R. H., 2006. Genetic variability assessed by microsatellites in cultured populations of the Pacific oyster (Crassostrea gigas) in China. Aquaculture, 259 (1-4): 95–102.
Lu, Y., Zhang, S. H., Shah, T., Xie, C., Hao, Z., Li, X., Farkhari, M., Ribaut, J. M., Cao, M., Rong, T., and Xu, Y., 2010. Joint linkage-linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proceedings of the National Academy of Sciences, 107(45): 19585–19590.
Mather, K. T., Caicedo, A. L., Polato, N. R., Olsen, K. M., McCouch, S., and Purugganan, M. D., 2007. The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics, 177(4): 2223–2232.
Myles, S., Peiffer, J., Brown, P. J., Ersoz, E. S., Zhang, Z., Costich, D. E., and Buckler, E. S., 2009. Association mapping: Critical considerations shift from genotyping to experimental design. Plant Cell, 21(8): 2194–2202.
Nordborg, M., and Tavaré, S., 2002. Linkage disequilibrium: What history has to tell us. Trends in Genetics, 18(2): 83–90.
Qanbari, S., Pimentel, E. C. G., Tetens, J., Thaller, G., Lichtner, P., Sharifi, A. R., and Simianer, H., 2009. The pattern of linkage disequilibrium in German Holstein cattle. Animal Genetics, 41(4): 346–356.
Rafalski, A., and Morgante, M., 2004. Corn and humans: Recombination and linkage disequilibrium in two genomes of similar size. Trends in Genetics, 20(2): 103–111
Rexroad, C. E., and Vallejo, R. L., 2009. Estimates of linkage disequilibrium and effective population size in rainbow trout. BMC Genetics, 10: 83.
Sauvage, C., Bierne, N., Lapègue, S., and Boudry, P., 2007. Single nucleotide polymorphisms and their relationship to codon usage bias in the Pacific oyster Crassostrea gigas. Gene, 406 (1-2): 13–22.
Sauvage, C., Boudry, P., de Koning, D. J., Haley, C. S., Heurtebise, S., and Lapègue, S., 2010. QTL for resistance to summer mortality and OsHV-1 load in the Pacific oyster (Crassostrea gigas). Animal Genetics, 41(4): 390–399.
Schuelke, M., 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology, 18: 233–234.
Slate, J., 2005. Quantitative trait locus mapping in natural populations: Progress, caveats and future directions. Molecular Ecology, 14(2): 363–379.
Steiner, C. C., Weber, J. N., and Hoekstra, H. E., 2007. Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biology, 5: e219.
Van-Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P., 2004. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4: 535–538.
Wang, Q. Z., Li, Q., Kong, L. F., and Yu, R. H., 2012. Response to selection for fast growth in the second generation of Pacific oyster (Crassostrea gigas). Journal of Ocean University of China, 11(3): 413–418.
Wang, Q. Z., Li, Q., Kong, L. F., and Yu, R. H., 2013. Third generation evaluation of the Pacific oyster (Crassostrea gigas) breeding lines selected for fast growth. Journal of Fisheries of China, 37(10): 1487–1494.
Weir, B. S., 2008. Linkage disequilibrium and association mapping. Annual Review of Genomics and Human Genetics, 9: 129–142.
Yu, J. M., and Buckler, E. S., 2006. Genetic association mapping and genome organization of maize. Current Opinion in Biotechnology, 17(2): 155–160.
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Guo, X., Li, Q., Kong, L. et al. Linkage disequilibrium in wild and cultured populations of Pacific oyster (Crassostrea gigas). J. Ocean Univ. China 15, 327–333 (2016). https://doi.org/10.1007/s11802-016-2832-0
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DOI: https://doi.org/10.1007/s11802-016-2832-0