Journal of Ocean University of China

, Volume 17, Issue 4, pp 947–956 | Cite as

A Preliminary Genetic Linkage Map of Sinonovacula constricta (Lamarck, 1818) Based on Microsatellites Derived from RAD Sequencing

  • Xueping Wu
  • Yanwei Feng
  • Hailin Jiang
  • Xiangquan LiuEmail author
  • Ying PanEmail author


Sinonovacula constricta is one of the important economic aquaculture species in China. In this study, we constructed genetic linkage maps of S. constricta based on 300 microsatellite markers derived from RAD-seq using an F1 full-sib family. The female map contained 204 microsatellites assigned to 22 linkage groups, which covered 1529.5 cM with an average interval of 10.3 cM. The male consisted of 187 microsatellites in 19 linkage groups corresponding to the haploid chromosome number (n=19), which spanned 1429.3 cM with an average interval of 8.7 cM. The genome coverage was approximately 83.5% and 81.4%, respectively. An integrated map was constructed according to the common markers in parental linkage groups, which had a total length of 1683.8 cM with an average interval of 7.3 cM. The genome coverage of the integrated map was approximately 86.3%. The genetic linkage map would form the foundation for further studies on the quantitative trait loci (QTL), as well as accelerating the breeding process of this species.

Key words

linkage maps Sinonovacula constricta microsatellite marker RAD sequencing 


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The study was supported by the grants from the Natural Science Foundation of Shandong Province (No. ZR2012 CM037), the Shandong Provincial Agriculture Thoroughbred Project, and the Innovation Project of Guangxi Graduate Education (No. YCBZ2015007).


  1. Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., Lewis, Z. A., Seiker, E. U., Cresko, W. A., and Johnson, E. A., 2008. Rapid SNP discovery and genetic mapping using sequencing RAD markers. PLoS One, 3: e3376.CrossRefGoogle Scholar
  2. Bai, Z. Y., Han, X. K., Luo, M., Lin, J. Y., Wang, G. L., and Li, J. L., 2015. Constructing a microsatellite-based linkage map and identifying QTL for pearl quality traits in triangle pearl mussel (Hyriopsis cumingii). Aquaculture, 37: 102–110.CrossRefGoogle Scholar
  3. Baranski, M., Gopikrshna, G., Robinson, N. A., Katneti, V. K., Shekhar, M. S., Shanmugakarthik, J., Jothivel, S., Gopal, C., Ravichandran, P., and Kent, M., 2014. The development of a high density linkage map for black tiger shrimp (Penaeus monodon) based on cSNPs. PLoS One, 9: e85413.CrossRefGoogle Scholar
  4. Cervera, M. T., Storme, V., Ivens, B., Gusmão, J., Liu, B. H., Hpstyn, V., Slycken, J. V., Montagu, M. V., and Boerjan, W., 2001. Dense genetic linkage maps of three Populus species (Populus deltoids, P. igra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics, 158: 787–809.Google Scholar
  5. Chakravarti, A., Lasher, L. K., and Reefer, J. E., 1991. A maximum likelihood method for estimating genome length using genetic linkage data. Genetics, 128: 175–182.Google Scholar
  6. Chu, G. N., Jiang, L. M., Yan, H., Yu, H. Y., Wang, Z. G., Jiang, H. B., and Zhang, Q. Q., 2014. A micirosatellite genetic linkage map of black rockfish (Sebastes schlegeli). Journal of Ocean University of China, 13: 1078–1086.CrossRefGoogle Scholar
  7. Cui, Z., Hui, M., Liu, Y., Song, C., Li, X., Li, Y., Liu, L., Shi, G., Wang, S., Li, F., Zhang, X., Liu, C., Xiang, J., and Chu, K. H., 2015. High-density linkage mapping aided by transcriptomics documents ZW sex determination system in the Chinese mitten crab Eriocheir sinensis. Heredity (Edinb), 115: 206–215.CrossRefGoogle Scholar
  8. da Fonseca, R. R., Albrechtsen, A., Themudo, G. E., Ramos-Madrigal, J., Sibbesen, J. A., Maretty, L., Zepeda-Mendoza, M. L., Campos, P. F., Heller, R., and Pereira, R. J., 2016. Next-generation biology: Sequencing and data analysis approached for non-model organisms. Marine Genomics, 30: 3–13.CrossRefGoogle Scholar
  9. Daniel, R. Z., and Ewan, B., 2008. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Research, 18: 821–829.CrossRefGoogle Scholar
  10. Du, W. J., Wang, C. D., Wang, J., Li, L. X., Niu, D. H., Li, J. L., and Shen, H. D., 2016. Comparison of early growth in Sinonovacula constricta selection group and family. Journal of Fisheries of China, 40: 604–611 (in Chinese with English abstract).Google Scholar
  11. Fais, J., Ladomada, B., and Gill, B., 1998. Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics, 149: 319–327.Google Scholar
  12. Feng, B., Dong, L. L., Niu, D. H., Meng, S., Zhang, B., Liu, D. B., Hu, S. N., and Li, J. L., 2010. Identification of immune genes of the agamaki clam (Sinonovacula constricta) by sequencing and bioinformatic analysis of ESTs. Marine Biotechnology, 12: 282–291.CrossRefGoogle Scholar
  13. Fishman, L., Kelly, A. J., Morgan, E., and Willis, J. H., 2001. A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics, 159: 1701–1716.Google Scholar
  14. Franch, R., Louro, B., Tsalavouta, M., Chatziplis, D., Tsigenopoulos, C. S., Sarropoulou, E., Antonello, J., Magoulas, A., Mylonas, C. C., Babbucci, M., Patarnello, T., Power, D. M., Kotoulas, G., and Bargelloni, L., 2006. A genetic linkage map of the hermaphrodite teleost fish Sparus aurata L. Genetics, 174: 851–861.CrossRefGoogle Scholar
  15. Gonen, S., Lowe, N. R., Cezard, T., Gharbi, K., Bishop, S., and Houston, R., 2014. Linkage maps of the Atlantic salmon (Salmon salar) genome derived from RAD sequencing. BMC Genomics, 15: 166.CrossRefGoogle Scholar
  16. 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: 218–226.CrossRefGoogle Scholar
  17. Haldane, J. B. S., 1922. Sex ration and unisexual sterility in hybrid animals. Journal of Genetics, 12: 101–109.CrossRefGoogle Scholar
  18. Hollenbeck, C. M., Portnpy, D. S., and Gold, J. R., 2015. A genetic linkage map of red drum (Sciaenops ocellatus) and comparison of chromosomal syntenies with four other fish species. Aquaculture, 435: 265–274.CrossRefGoogle Scholar
  19. Huxley, J. S., 1928. Sexual difference of linkage in Gammarus Checreuxi. Journal of Genetics, 20: 145–156.CrossRefGoogle Scholar
  20. Ihara, N., Takasuga, A., Mizoshita, K., Takeda, H., Sugimoto, M., Mizoguchi, Y., Hirano, T., Itoch, T., Watanabe, T., Reed, K. M., Snelling, W. M., Kappes, S. M., Beattie, C. W., Beatti, C. W., Benett, C. L., and Sugimoto, Y., 2004. A comprehensive genetic map of the cattle genome based on 3802 microsatellites. Genome Research, 14: 1987–1998.CrossRefGoogle Scholar
  21. Jiang, L. M., Chu, G. N., Zhang, Q. Q., Wang, Z. G., Wang, X. B., Zhai, J. M., and Yu, H. Y., 2013. A microsatellite genetic linkage map of half smooth tongue sole (Cynoglossus semilaevis). Marine Genomics, 9: 17–23.CrossRefGoogle Scholar
  22. Jiang, Q., Li, Q., Yuan, Y., and Kong, L. F., 2010. Polymorphic microsatellite loci for population studies of the razor clam, Sinonovacila constricta. Consevation Genetics Resources, 2: 81–83.CrossRefGoogle Scholar
  23. Kosambi, D. D., 1994. The estimation of map distances from recombination values. Annals of Eugenics, 12: 172–175.CrossRefGoogle Scholar
  24. Lee, B. Y., Lee, W. J., Streelman, J. T., Carleton, K. L., Howe, A. E., Hulata, G., Slettan, A., Stern, J. E., Terai, Y., and Kocher, T. D., 2005. A second generation genetic linkage map of tilapia (Oreochromis spp.). Genetics, 170: 237–244.CrossRefGoogle Scholar
  25. Li, L. X., Du, W. J., Wang, C. D., Wang, J., Niu, D. H., Li, J. L., and Shen, H. D., 2016. Comparative analysis of growth and heat tolerance, salt tolerance traits among Sinonovacula constricta families. Journal of Shanghai Ocean University, 25: 516–521 (in Chinese with English abstract).Google Scholar
  26. Li, H. J., Liu, X., and Zhang, G. F., 2012. A consensus microsatellite-based linkage map for the hermaphroditic bay scallop (Argopecten irrdians) and its application in size-related QTL analysis. PLoS One, 7: e46926.CrossRefGoogle Scholar
  27. Li, Q., and Kijima, A., 2006. Microsatellites analysis of gynogenetic families in the Pacific oyster, Crassostrea gigas. Journal of Experimental Marine Biology and Ecology, 331: 1–8.CrossRefGoogle Scholar
  28. Li, Q., Qi, M. J., Nie, H. T., Kong, L. F., and Yu, H., 2016. Microsatellite-centromere mapping in Japanese scallop (Patinopecten yessoensis) through half-tetrad analysis in gynogenetic diploid families. Journal of Ocean University of China, 15: 541–548.CrossRefGoogle Scholar
  29. Lindahal, K. F., 1991. His and hers recombinational hotspots. Trends Genetics, 7: 273–276.CrossRefGoogle Scholar
  30. Liu, B., Wang, Q. Y., Li, J., and He, Y., 2010. A genetic linkage map of marine shrimp Penaeus (Fenneropenaeus) chinensis based on AFLP, SSR and RAPD markers. Chinnese Journal of Oceanology and Lomnology, 28: 815–825.CrossRefGoogle Scholar
  31. Liu, F., Sun, F., Li, J., Xia, H. J., Lin, G., Tu, R. J., and Yue, H. G., 2013. A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus × Oremochromis spp.) and mapping of sex-determining loci. BMC Genomics, 14: 58–71.CrossRefGoogle Scholar
  32. Liu, Q., Sakamoto, T., Kubota, S., Okamoto, N., Yamashita, H., Takagi, M., Shigenobu, Y., Nakamura, Y., Sano, M., Wuthisuthimethavee, S., and Ozaki, A., 2013. A genetic linkage map of kelp grouper (Epinephelus bruneus) based on microsatellite markers. Aquaculture, 415: 63–81.CrossRefGoogle Scholar
  33. Luzón, M. J. M., Hermida, M., Pérez, N. R., Robles, F., Navas, J. I., Rejón, C. R., Bouza, C., Martínez, P., and de la Herrán, R., 2015. First haploid genetic map based on microsatellite markers in Senegalese sole (Solea senegalensis, Kaup 1858). Marine Biotechnology, 17: 8–22.CrossRefGoogle Scholar
  34. Lyttle, T. W., 1991. Segregation distorters. Annual Review Genetics, 25: 51–557.CrossRefGoogle Scholar
  35. Lynn, A., Ashley, T., and Hassold, T., 2004. Variation in human meiotic recombination. Annual Review of Genomics and Human Genetics, 5: 317–349.CrossRefGoogle Scholar
  36. Ma, H. T., Jiang, H. B., Liu, X. Q., Wu, X. P., and Wei, X. M., 2015. Polymorphic microsatellite loci for the razor clam, Sinonocacula constricta. Genetics and Molecular Research, 14 (1): 145–148.CrossRefGoogle Scholar
  37. Niu, D. H., Li, J. L., and Liu, D. B., 2008. Polymorphic microsatellite loci for population studies of the razor calm, Sinonovacula consticta. Conservation Genetic Resources, 9: 1393–1394.CrossRefGoogle Scholar
  38. Petersen, J. L., Baerwald, M. R., Ibarra, A. M., and May, B., 2012. A first-generation linkage map of the Pacific lion-paw scallop (Nodipecten subnodosus). Aquaculture, 350: 200–209.CrossRefGoogle Scholar
  39. Qiu, G. F., Xiong, L. W., Liu, Z. Q., Yan, Y. L., and Shen, H., 2016. A first generation microsatellite-based linkage map of the Chinese mitten crab Eriocheir sinensis and its application in quantitative trait loci (QTL) detection. Aquaculture, 451: 223–231.CrossRefGoogle Scholar
  40. Rick, C. M., 1969. Controlled introgression of chromosomes of Solanum pennellii into Lycopirsicon esculentum: Segregation and recombination. Genetics, 62: 753.Google Scholar
  41. Ruan, X. H., Wang, W. J., Kong, J., Yu, F., and Huang, X. Q., 2010. Genetic linkage mapping of turbot (Scophthalmus maximus L.) using microsatellite markers and its application in QTL analysis. Aquaculture, 308: 899–100.CrossRefGoogle Scholar
  42. Sahoo, L., Patel, A., Sahu, B. P., Mitra, S., Meher, P. K., Mahapatra, K. D., Dash, K. S., Jayasankar, P., and Das, P., 2015. Preliminary genetic linkage map of Indian major carp, Labeo rohita (Hamilton 1822) based on microsatellite markers. Journal of Genetics, 94: 271–277.CrossRefGoogle Scholar
  43. Sambrook, J. D., and Russell, W., 2000. Molecular Cloning: A Laboratory Manual. 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 543–554.Google Scholar
  44. Shi, Y. H., Wang, S., Gu, Z. F., Lv, J., Zhan, X., Yu, C. C., Bao, Z. M., and Wang, A. M., 2014. High-density single nucleotide polymorphism linkage and quantitative trait locus mapping of the pearl oyster, Pinctada fucata martensii Dunker. Aquaculture, 434: 376–384.CrossRefGoogle Scholar
  45. Singer, A., Perlman, H., Yan, Y., Walker, C., Corlry-Smith, G., Brandhorst, B., and Postlethwait, J., 2002. Sex-specific recombination rates in zebrafish (Danio rerio). Genetics, 160: 649–657.Google Scholar
  46. Song, W., Li, Y., Zhao, Y., Yan, Y., Liu, Y., Niu, Y., Pang, R., Miao, G., Liao, X., Shao, C., and Gao, F., 2012. Construction of a high-density microsatellite genetic linkage map and mapping of sexual and growth-related traits in half-smooths tongue sole (Cynoglossus semilaevis). PLoS One, 7: e52097.CrossRefGoogle Scholar
  47. Trivers, R., 1988. Sex differences in rated of recombination and sexual selection. In: The Evolution of Sex. Michod, R. E., and Levin, B. R., eds., Sinauer Associates, Sunderland MA, 270–286.Google Scholar
  48. Tsigenopoulos, C. S., Louro, B., Chatziplis, D., Lagnel, J., Vogiatzi, E., Loukovitis, D., Franch, R., Sarropoulou, E., and Power, D. M., 2014. Second generation genetic linkage map for the gilthead sea bream Sparus aurata L. Marine Genomics, 18: 77–82.CrossRefGoogle Scholar
  49. van Ooijen, J. W., 2006. JoinMap®4, Software for calculation of genetic linkage maps in experimental populations. Wageningen, Netherlands.Google Scholar
  50. Voorrips, R. E., 2002. MapChart: Software for the graphical presentation of linkage maps and QTLs. Journal of Heredity, 93: 77–78.CrossRefGoogle Scholar
  51. Wang, J. X., Zhao, X. F., Zhou, L. H., and Xiang, J. H., 1998. Research on chromosomes of Sinonovacula constricta. Chinese Journal of Oceanology and Limnology, 29: 191–196 (in Chinese).Google Scholar
  52. Wu, X. P., Feng, Y. W., Ma, H. T., Pan, Y., and Liu, X. Q., 2015. Characterization of new microsatellite loci from the razor clam (Sinonovacula constricta) and transferability to related species. Biochemical Systematic and Ecology, 61: 175–178.CrossRefGoogle Scholar
  53. Xia, J. H., Liu, F., Zhu, Z. Y., Fu, J., Feng, J., Li, J., and Yue, G. H., 2010. A consensus linkage map of the grass carp (Ctenopharyngodon idella) based on microsatellites and SNPs. BMC Genetics, 11: 135.CrossRefGoogle Scholar
  54. Xie, Z. M., 2003. Aquaculture Technology of Marine Economic Shellfishes. China Agriculture Press, Beijing, 23–27.Google Scholar
  55. Xu, F. S., and Zhang, S. P., 2008. Illustrated Bivalvia Mollusca Fauna of China Seas. Science Press, Beijing, 211–213 (in Chinese).Google Scholar
  56. Ye, H., Liu, Y., Liu, X. D., Wang, X. Q., and Wang, Z. Y., 2014. Genetic mapping and QTL analysis of growth traits in the large yellow croaker Larimichthys crocea. Marine Biotechnology, 16: 729–738.CrossRefGoogle Scholar
  57. Yu, Z. N., and Guo, X. M., 2003. Genetic linkage map of the eastern oyster Crassostrea virginica Gmelin. The Biological Bulletin, 204: 327–338.CrossRefGoogle Scholar
  58. Zhan, A., Hu, J., Hu, X., Hui, M., Wang, M., Peng, W., Huang, X., Wang, S., Lu, W., Sun, C., and Bao, Z., 2009. Construction of microsatellite-based linkage maps and identification of size-related quantitative trait loci for Zhikong scallop (Chlamys farreri). Animal Genetics, 40: 821–831.CrossRefGoogle Scholar
  59. Zhan, X., Fan, F. L., You, W. W., Yu, J. J., and Ke, C. H., 2012. Construction of an integrated map of Haliotis diversicolor using microsatellite markers. Marine Biotechnology, 14: 79–86.CrossRefGoogle Scholar
  60. Zhong, X. X., Li, Q., Guo, X., Yu, Y., and Kong, L. F., 2014. QTL mapping for glycogen content and shell pigmentation in the Pacific oyster Crassostrea gigas using microsatellites and SNPs. Aquaculture International, 22: 1877–1889.CrossRefGoogle Scholar

Copyright information

© Science Press, Ocean University of China and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Marine Ecological RestorationShandong Marine Resource and Environment Research InstituteYantaiChina
  2. 2.College of Animal Science and TechnologyGuangxi UniversityNanningChina
  3. 3.Key Laboratory of Protection and Utilization of Marine ResourcesGuangxi University of NationalitiesNanningChina

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