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Genetic Mapping and QTL Analysis of Growth-Related Traits in the Pacific Oyster

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Abstract

The Pacific oyster (Crassostrea gigas) is one of the most important oysters cultured worldwide. To analyze the oyster genome and dissect growth-related traits, we constructed a sex-averaged linkage map by combining 64 genomic simple sequence repeats, 42 expressed sequence tag-derived SSRs, and 320 amplified fragment length polymorphism markers in an F1 full-sib family. A total of 426 markers were assigned to 11 linkage groups, spanning 558.2 cM with an average interval of 1.3 cM and 94.7% of genome coverage. Segregation distortion was significant for 18.8% of the markers (P < 0.05), and distorted markers tended to occur on some genetic regions or linkage groups. Most growth-related quantitative traits were highly significantly (P < 0.01) correlated, and principal component analysis obtained four principal components. Quantitative trait locus (QTL) analysis identified three significant QTLs for two principal components, which explained 0.6–13.9% of the phenotypic variation. One QTL for sex was detected on linkage group 6, and the inheritabilities of sex for parental alleles and maternal alleles on that locus C15 are 39.8% and 0.01%, respectively. The constructed linkage map and determined QTLs can provide a tool for further genetic analysis of the traits and be potential for marker-assisted selection in C. gigas breeding.

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References

  • Ahmed M, Sparks AK (1967) A preliminary study of chromosomes of two species of oysters (Ostrea lurida and Crassostrea gigas). J Fish Res Board Can 24:2155–2159

    Article  Google Scholar 

  • Baghurst BC, Mitchell JG (2002) Sex-specific growth and condition of the Pacific oyster (Crassostrea gigas Thunberg). Aquac Res 33:1253–1263

    Article  Google Scholar 

  • Bai J, Li Q, Cong RH, Sun WJ, Liu J, Feng YW (2011) Development and characterization of 68 EST-SSR markers in the Pacific oyster, Crassostrea gigas. J World Aquacult Soc 42(3):444–455

    Article  Google Scholar 

  • Bucklin KA (2002) Analysis of the genetic basis of inbreeding depression in the Pacific oyster Crassostrea gigas. PhD thesis, University of California, Davis, CA, USA

  • Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:175–182

    PubMed  CAS  Google Scholar 

  • Chistiakov D, Hellemans B, Volckaert F (2006) Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture 255:1–29

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait loci mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • Dégremont L, Bédier E, 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 299:21–29

    Article  Google Scholar 

  • Evans S, Langdon C (2006) Direct and indirect responses to selection on individual body weight in the Pacific oyster (Crassostrea gigas). Aquaculture 261:546–555

    Article  Google Scholar 

  • FAO (2011) Yearbook of fisheries statistics summary tables. Available from ftp://ftpfaoorg/fi/STAT/summary/defaulthtm#aqua. Accessed March 2011

  • Fishman L, Kelly AJ, Morgan E, Willis JH (2001) A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159:1701–1716

    PubMed  CAS  Google Scholar 

  • Georges M (2007) Mapping, fine mapping, and molecular dissection of quantitative trait loci in domestic animals. Annu Rev Genom Hum G 8:131–162

    Article  CAS  Google Scholar 

  • Graner A, Jahoor A, Schondelmaier J, Siedler H, Pilier K (1991) Construction of an RFLP map of barley. Theor Appl Genet 83:250–256

    Article  Google Scholar 

  • Guo X, Hedgecock D, Hershberger WK, Cooper K, Allen SK (1998) Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution 52:394–402

    Article  Google Scholar 

  • Guo X, Wang Y, Wang L, Lee JH (2008) Oysters. In: Kocher TD, Kole C (eds) Genome mapping, genomics in animals, volume 2: genome mapping, genomics in fishes and aquatic animals. Springer, Berlin, pp 163–175

    Chapter  Google Scholar 

  • Hackett CA, Broadfoot LB (2003) Effects of genotyping errors, missing values, segregation distortion in molecular marker data on the construction of linkage maps. Heredity 90:33–38

    Article  PubMed  CAS  Google Scholar 

  • Hedgecock D, Cooper K, Hershberger W, Guo X (1993) Body size at harvest, sex ratio, and mantle color of pedigreed Pacific oysters (Crassostrea gigas) from controlled crosses [abstract]. Aquaculture 111:299

    Article  Google Scholar 

  • Hedgecock D, McGoldrick DJ, Bayne BL (1995) Hybrid vigor in Pacific oysters: an experimental approach using crosses among inbred lines. Aquaculture 137:285–298

    Article  Google Scholar 

  • Hedgecock D, Li G, Voigt ML (2007) Mapping heterosis QTL in the Pacific oyster Crassostrea gigas. Aquaculture 272:268

    Google Scholar 

  • Hedrick PW, Hedgecock D (2010) Sex determination: genetic models for oysters. J Hered 101:602–611

    Article  PubMed  Google Scholar 

  • Hu ZQ, Xu SZ (2009) PROC QTL—a SAS procedure for mapping quantitative trait loci. Int J Plant Genomics 2009:141234–141234

    PubMed  Google Scholar 

  • Hubert S, Hedgecock D (2004) Linkage maps of microsatellite DNA markers for the Pacific oyster Crassostrea gigas. Genetics 168:351–362

    Article  PubMed  CAS  Google Scholar 

  • Hubert S, Cognard E, Hedgecock D (2009) Centromere mapping in triploid families of the Pacific oyster Crassostrea gigas (Thunberg). Aquaculture 288:172–183

    Article  CAS  Google Scholar 

  • Huvet A, Boudry P, Ohresser M, Delsert C, Bonhomme F (2000) Variable microsatellites in the Pacific oyster Crassostrea gigas and other cupped oyster species. Anim Genet 31:71–72

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute (2000) SAS SQL procedure user’s guide, version 8. SAS Institute Inc, Cary

    Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Lallias D, Lapegue S, Hecquet C, Boudry P, Beaumont AR (2007a) AFLP-based genetic linkage maps of the blue mussel (Mytilus edulis). Anim Genet 38:340–349

    Article  PubMed  CAS  Google Scholar 

  • Lallias D, Beaumont AR, Haley CS, Boudry P, Heurtebise S, Lapègue S (2007b) A first-generation genetic linkage map of the European flat oyster Ostrea edulis (L) based on AFLP and microsatellite markers. Anim Genet 38:560–568

    Article  PubMed  CAS  Google Scholar 

  • Langdon C, Evans F, Jacobson D, Blouin M (2003) Yields of cultured Pacific oysters Crassostrea gigas Thunberg improved after one generation of selection. Aquaculture 220:227–244

    Article  Google Scholar 

  • Launey S, Hedgecock D (2001) High genetic load in the Pacific oyster Crassostrea gigas. Genetics 159:255–265

    PubMed  CAS  Google Scholar 

  • Li L, Guo XM (2004) AFLP-based genetic linkage maps of the Pacific oyster Crassostrea gigas Thunberg. Mar Biotechnol 6:26–36

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Park C, Kijima A (2002) Isolation and characterization of microsatellite loci in the Pacific abalone, Haliotis discus hannai. J Shellfish Res 21:811–815

    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  CAS  Google Scholar 

  • Li L, Xiang J, Liu X, Zhang Y, Dong B, Zhang X (2005) Construction of AFLP-based genetic linkage map for Zhikong scallop, Chlamys farreri Jones et Preston and mapping of sex-linked markers. Aquaculture 245:63–73

    Article  CAS  Google Scholar 

  • Li Q, Chen LM, Kong LF (2009a) A genetic linkage map of the sea cucumber, Apostichopus japonicus (Selenka), based on AFLP and microsatellite markers. Anim Genet 40:678–685

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Liu SK, Kong LF (2009b) Microsatellites within genes and ESTs of the Pacific oyster Crassostrea gigas and their transferability in five other Crassostrea species. Electron J Biotechn 12:3

    Google Scholar 

  • Li Q, Wang QZ, Qi MJ, Ge JL, Cong RH (2011) Development, characterization, and inheritance of 113 novel EST-SSR markers in the Pacific oyster (Crassostrea gigas). Genes Genom 33(3):313–316

    Article  Google Scholar 

  • Magoulas A, Ghjetvaj B, Terzoglou V, Zouros E (1998) Three polymorphic microsatellites in the Japanese oyster Crassostrea gigas (Thunberg). Anim Genet 29:69–70

    CAS  Google Scholar 

  • McGoldrick DJ (1997) An experimental investigation of the genetic basis of heterosis in the Pacific oyster Crassostrea gigas PhD thesis, University of California, Davis, CA, USA

  • McGoldrick D, Hedgecock D, English LJ, Baoprasertkul 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 

  • Nell JA (2001) The history of oyster farming in Australia. Mar Fish Rev 63:14–25

    Google Scholar 

  • Qi HG, Wu Q, Li L, Zhang GF (2009) Development and characterization of microsatellite markers for the Pacific oyster Crassostrea gigas. Conserv Genet Res 1:451–453

    Article  Google Scholar 

  • Qiu X, Xu L, Liu SZ, Wang XL, Meng XY (2008a) Eleven polymorphic simple sequence repeat markers from expressed sequence tags of Pacific oyster Crassostrea gigas EST database. Conserv Genet 10:1773–1775

    Article  Google Scholar 

  • Qiu XM, Liu SZ, Wang XL, Meng XY (2008b) Eight SSR loci from oyster Crassostrea gigas EST database and cross-species amplification in C. plicatula. Conserv Genet 10:1013–1015

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Sauvage C, Boudry P, de Koning DJ, Haley CS, Heurtebise S, Lapègue S (2010) QTL for resistance to summer mortality and OsHV-1 load in the Pacific oyster (Crassostrea gigas). Anim Genet 41:390–399

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • SPSS Inc. (2007) SPSS base 16.0 user’s guide. SPSS, Chicago

    Google Scholar 

  • Tan YD, Wan CL, Zhu YF, Lu C, Xiang ZH, Deng HW (2001) An amplified fragment length polymorphism map of the silkworm. Genetics 157:1277–1284

    PubMed  CAS  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0: software for the calculation of genetic linkage maps. Plant Research International, Wageningen

    Google Scholar 

  • Voorrips RE (2002) MapChart: software for the presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Ren R, Yu ZN (2008) Bioinformatic mining of EST-SSR loci in the Pacific oyster, Crassostrea gigas. Anim Genet 39:287–289

    Article  PubMed  CAS  Google Scholar 

  • Ward RD, English LJ, McGoldrick DJ, Maguire GB, Nell JA, Thompson PA (2000) Genetic improvement of the Pacific oyster Crassostrea gigas (Thunberg) in Australia. Aquac Res 31:35–44

    Article  Google Scholar 

  • Xu SZ (2008) Quantitative trait locus mapping can benefit from segregation distortion. Genetics 180:2201–2208

    Article  PubMed  Google Scholar 

  • Yamtich J, Voigt ML, Li G, Hedgecock D (2005) Eight microsatellite loci for the Pacific oyster Crassostrea gigas. Anim Genet 36:524

    PubMed  CAS  Google Scholar 

  • Yu ZN, Guo XM (2003) Genetic linkage map of the eastern oyster Crassostrea virginica Gmelin. Bioll Bull 204:327–338

    Article  CAS  Google Scholar 

  • Yu H, Li Q (2007) EST-SSR markers from the Pacific oyster, Crassostrea gigas. Mol Ecol Notes 7:860–862

    Article  CAS  Google Scholar 

  • Yu H, Li Q (2008) Exploiting EST databases for the development, characterization of EST-SSRs in the Pacific oyster (Crassostrea gigas). J Hered 99:208–214

    Article  PubMed  CAS  Google Scholar 

  • Yu ZN, Wang YH, Fu DK (2009) Development of 51 novel EST-SSR loci in the Pacific oyster, Crassostrea gigas by data mining from the public EST database. Conserv Genet Res 2:13–18

    Article  Google Scholar 

  • Zhan AB, Hu J, Hu X, Hui M, Wang M, Peng W, Huang X, Wang S, Lu W, Sun C, Bao ZM (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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the 973 Program (2010CB126406) and the National Marine Public Welfare Research Program (200905020).

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Correspondence to Qi Li.

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Table S1

AFLP primer combinations information (DOC 88 kb)

Table S2

A comparison of the characteristics of the linkage maps constructed for C. gigas (DOC 85 kb)

Table S3

Loadings of the separated traits on the principal component (n = 83) in F1 progeny (DOC 81 kb)

Table S4

A comparison of the female and male quantitative traits (DOC 82 kb)

Fig. S1

Quantile–quantile plot test for normal distribution of principal components. PC principal component (DOC 334 kb)

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Guo, X., Li, Q., Wang, Q.Z. et al. Genetic Mapping and QTL Analysis of Growth-Related Traits in the Pacific Oyster. Mar Biotechnol 14, 218–226 (2012). https://doi.org/10.1007/s10126-011-9405-4

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  • DOI: https://doi.org/10.1007/s10126-011-9405-4

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