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Variation at Nuclear Loci in the Japanese Sea Cucumber Apostichopus japonicus (Selenka, 1867) (Echinodermata: Holothuroidea) in Samples from Peter the Great Bay, Sea of Japan

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Abstract

The genetic diversity of the sea cucumber Apostichopus japonicus was assessed using five microsatellite markers. A total of 122 specimens of sea cucumber from five samples collected in Peter the Great Bay (Sea of Japan) were examined. All loci were polymorphic. For all samples and loci, the average value of the observed heterozygosity was 0.461 ± 0.027 and the expected heterozygosity was 0.575 ± 0.031. The values of the inbreeding coefficient were, on average, greater than zero due to the deficiency of heterozygotes. Null alleles were identified for some microsatellite loci. After their detection, genotyping errors and statistical data were corrected. The presence of null alleles caused a 1.5–2-fold decrease in the value of observed heterozygosity and led to deviations from the Hardy–Weinberg equilibrium.

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REFERENCES

  1. Gavrilova, G.S., Tovarnoe vyrashchivaniye dal’nevostochnogo trepanga (Commercial Culture of Japanese Sea Cucumber), Vladivostok: TINRO-Center, 2013.

  2. Galinskaya, T.V., Schepetov, D.M., and Lysenkov, S.N., Prejudices about microsatellite research and how to resist them, Russ. J. Genet., 2019, vol. 55, no. 6, pp. 657–671. https://doi.org/10.1134/S1022795419060048

    Article  CAS  Google Scholar 

  3. Lysenko, V.N., Zharikov, V.V., and Lebedev, A.M., The abundance and distribution of the Japanese sea cucumber, Apostichopus japonicus (Selenka, 1867) (Echinodermata: Stichopodidae), in nearshore waters of the southern part of the Far Eastern State Marine Reserve, Russ. J. Mar. Biol., 2015, vol. 41, no. 2, pp. 140–144. https://doi.org/10.1134/S1063074015020078

    Article  Google Scholar 

  4. Lysenko, V.N., Zharikov, V.V., and Lebedev, A.M., The current status of populations of the sea cucumber Apostichopus japonicus (Selenka, 1867) in the Far Eastern Marine Reserve, Russ. J. Mar. Biol., 2018, vol. 44, pp. 164–171. https://doi.org/10.1134/S1063074018020074

    Article  Google Scholar 

  5. Selin, N.I., Vertical distribution of the Far East trepang Apostichopus japonicus in Vostok Bay, Sea of Japan, Russ. J. Mar. Biol., 2001, vol. 27, no. 4, pp. 256–258. https://doi.org/10.1023/A:1011971504890

    Article  Google Scholar 

  6. Abdul-Muneer, P.M., Application of microsatellite markers in conservation and fisheries management: Recent advances in population structure analysis and conservation strategies, Genet. Res. Int., 2014, vol. 2014, 691759. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3997932. https://doi.org/10.1155/2014/691759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. An, H.S., Lee, J.W., Hong, S.W., et al., Genetic differences between wild and hatchery populations of red sea cucumber (Stichopus japonicus) inferred from microsatellite markers: Implications for production and stocking programs design, Genes Genomics, 2013, vol. 35, pp. 709–717. https://doi.org/10.1007/s13258-013-0139-8

    Article  Google Scholar 

  8. Arthofer, W., Heussler, C., Krapf, P., et al., Identifying the minimum number of microsatellite loci needed to assess population genetic structure: A case study in fly culturing, Fly, 2018, vol. 12, no. 1, pp. 13–22. https://doi.org/10.1080/19336934.2017.1396400

    Article  PubMed  Google Scholar 

  9. Brookfield, J.F.Y., A simple new method for estimating null allele frequency from heterozygote deficiency, Mol. Ecol., 1996, vol. 5, no. 3, pp. 453−455. https://doi.org/10.1111/j.1365-294X.1996.tb00336.x

    Article  CAS  PubMed  Google Scholar 

  10. Carlsson, J., Effects of microsatellite null alleles on assignment testing, J. Hered., 2008, vol. 99, no. 6, pp. 616–623. https://doi.org/10.1093/jhered/esn048

    Article  CAS  PubMed  Google Scholar 

  11. Chakraborty, R., de Andrade, M., Daiger, S.P., and Budowle, B., Apparent heterozygote deficiencies observed in DNA typing data and their implications in forensic applications, Ann. Hum. Genet., 1992, vol. 56, no. 1, pp. 45–57. https://doi.org/10.1111/j.1469-1809.1992.tb01128.x

    Article  CAS  PubMed  Google Scholar 

  12. Chang, Y., Feng, Z., Yu, J., and Ding, J., Genetic variability analysis in five populations of the sea cucumber Stichopus (Apostichopus) japonicus from China, Russia, South Korea and Japan as revealed by microsatellite markers, Mar. Ecol., 2009, vol. 30, no. 4, pp. 455–461. https://doi.org/10.1111/j.1439-0485.2009.00292.x

    Article  CAS  Google Scholar 

  13. Chapuis, M.-P. and Estoup, A., Microsatellite null alleles and estimation of population differentiation, Mol. Biol. Evol., 2007, vol. 24, no. 3, pp. 621–631. https://doi.org/10.1093/molbev/msl191

    Article  CAS  PubMed  Google Scholar 

  14. Chen, L., Li, Q., and Yang, J., Microsatellite genetic variation in wild and hatchery populations of the sea cucumber (Apostichopus japonicus Selenka) from northern China, Aquacult. Res., 2008, vol. 39, no. 14, pp. 1541–1549. https://doi.org/10.1111/j.1365-2109.2008.02027.x

    Article  Google Scholar 

  15. Chen, M., Gao, L., Zhang, W., et al., Identification of forty-five gene-derived polymorphic microsatellite loci for the sea cucumber, Apostichopus japonicus, J. Genet., 2013, vol. 92, no. 2, p. e31–35. http://www.ias.as.in/jgenet/OnlineResources/92/e31.pdf. https://doi.org/10.1007/s12041-013-0234-2

    Article  CAS  PubMed  Google Scholar 

  16. Chybicki, I. and Burczyk, J., Simultaneous estimation of null alleles and inbreeding coefficients, J. Hered., 2009, vol. 100, no. 1, pp. 106–113. https://doi.org/10.1093/jhered/esn088

    Article  CAS  PubMed  Google Scholar 

  17. Dąbrowski, M.J., Bornelöv, S., Kruczyk, M., et al. ‘True’ null allele detection in microsatellite loci: A comparison of methods, assessment of difficulties and survey of possible improvements, Mol. Ecol. Resour., 2015, vol. 15, no. 3, pp. 477–488.https://doi.org/10.1111/1755-0998.12326

    Article  PubMed  Google Scholar 

  18. Dakin, E.E. and Avise, J.C., Microsatellite null alleles in parentage analysis, Heredity, 2004, vol. 93, no. 5, pp. 504–509. https://doi.org/10.1038/sj.hdy.6800545

    Article  CAS  PubMed  Google Scholar 

  19. De Meeûs, T., Revisiting FIS, FST, Wahlund effects, and null alleles, J. Hered., 2018, vol. 109, no. 4, pp. 446–456. https://doi.org/10.1093/jhered/esx106

    Article  PubMed  Google Scholar 

  20. Dempster, A.P., Laird, N.M., and Rubin, D.B., Maximum likelihood from incomplete data via the EM algorithm, J. R. Stat. Soc., Ser. B, 1977, vol. 39, no. 1, pp. 1–38. https://doi.org/10.1111/j.2517-6161.1977.tb01600.x

    Article  Google Scholar 

  21. Dong, Y., Li, Q., Zhong, X., and Kong, L., Development of gene-derived SNP markers and their application for the assessment of genetic diversity in wild and cultured populations in sea cucumber, Apostichopus japonicus, J. World Aquacult. Soc., 2016, vol. 47, no. 6, pp. 873–888. https://doi.org/10.1007/s12686-013-9858-z

    Article  CAS  Google Scholar 

  22. Du, H., Bao, Z., Yan, J., et al., Development of 101 gene-based single nucleotide polymorphism markers in sea cucumber, Apostichopus japonicus, Int. J. Mol. Sci., 2012, vol. 13, no. 6, pp. 7080–7097. https://doi.org/10.3390/ijms13067080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ellegren, H., Microsatellites: Simple sequences with complex evolution, Nat. Rev. Genet., 2004, vol. 5, pp. 435–445. https://doi.org/10.1038/nrg1348

    Article  CAS  PubMed  Google Scholar 

  24. Excoffier, L. and Lischer, H.E.L., Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, no. 3, pp. 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  25. Girard, P., A robust statistical method to detect null alleles in microsatellite and SNP datasets in both panmictic and inbred populations, Stat. Appl. Genet. Mol. Biol., 2011, vol. 10, p. 9. https://pubmed.ncbi.nlm.nih.gov/21381434/. https://doi.org/10.2202/1544-6115.1620

    Article  Google Scholar 

  26. Girard, P. and Angers, B., Assessment of power and accuracy of methods for detection and frequency-estimation of null alleles, Genetica, 2008, vol. 134, no. 2, pp. 187–197. https://doi.org/10.1007/s10709-007-9224-8

    Article  PubMed  Google Scholar 

  27. Grimaldi, M.-C. and Crouau-Roy, B., Microsatellite allelic homoplasy due to variable flanking sequences, J. Mol. Evol., 1997, vol. 44, pp. 336–340. https://doi.org/10.1007/PL00006151

    Article  CAS  PubMed  Google Scholar 

  28. Huang, K., Ritland, K., Dunn, D.W., et al., Estimating relatedness in the presence of null alleles, Genetics, 2016, vol. 202, no. 1, pp. 247–260. https://doi.org/10.1534/genetics.114.163956

    Article  CAS  PubMed  Google Scholar 

  29. Kalinowski, S.T. and Taper, M.L., Maximum likelihood estimation of the frequency of null alleles at microsatellite loci, Conserv. Genet., 2006, vol. 7, pp. 991–995. https://doi.org/10.1007/s10592-006-9134-9

    Article  CAS  Google Scholar 

  30. Kanno, M., Suyama, Y., Li Q., and Kijima, A., Microsatellite analysis of Japanese sea cucumber, Stichopus (Apostichopus) japonicus, supports reproductive isolation in color variants, Mar. Biotechnol., 2006, vol. 8, pp. 672–685. https://doi.org/10.1007/s10126-006-6014-8

    Article  CAS  Google Scholar 

  31. Kim, M., Choi, T., and An, H.S., Population genetic structure of sea cucumber, Stichopus japonicus in Korea using microsatellite markers, Aquacult. Res., 2008, vol. 39, no. 10, pp. 1038–1045. https://doi.org/10.1111/j.1365-2109.2008.01962.x

    Article  CAS  Google Scholar 

  32. Kolodziej, K., Theissinger, K., Brün, J., et al., Determination of the minimum number of microsatellite markers for individual genotyping in wild boar (Sus scrofa) using a test with close relatives, Eur. J. Wildl. Res., 2012, vol. 58, pp. 621–628. https://doi.org/10.1007/s10344-011-0588-9

    Article  Google Scholar 

  33. Lemer, S., Rochel, E., and Planes, S., Correction method for null alleles in species with variable microsatellite flanking regions, a case study of the black-lipped pearl oyster Pinctada margaritifera, J. Hered., 2011, vol. 102, no. 2, pp. 243–246. https://doi.org/10.1093/jhered/esq123

    Article  CAS  PubMed  Google Scholar 

  34. Oh, G.-W., Ko, S.-C., Lee, D.H., et al., Biological activities and biomedical potential of sea cucumber (Stichopus japonicus): A review, Fish. Aquat. Sci., 2017, vol. 20, p. 28. https://doi.org/10.1186/s41240-017-0071-y

    Article  CAS  Google Scholar 

  35. Peakall, R. and Smouse, P.E., GenAlEx 6.5: Genetic analysis in Exel. Population genetic software for teaching and research—an update, Bioinformatics, 2012, vol. 28, no. 19, pp. 2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Rico, C., Cuesta, J.A., Drake, P., et al., Null alleles are ubiquitous at microsatellite loci in the Wedge Clam (Donax trunculus), PeerJ., 2017, vol. 5, e3188. https://peerj.com/articles/3188/. https://doi.org/10.7717/peerj.3188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Selenka, E., Beiträge zur Anatomie und Systematik der Holothurien, Z. Wiss. Zool., 1867, vol. 17, pp. 291–374.

    Google Scholar 

  38. Soliman, T., Kanno, M., Kijima, A., and Yamazaki, Y., Population genetic structure and gene flow in the Japanese sea cucumber Apostichopus japonicus across Toyama Bay, Japan, Fish. Sci., 2012, vol. 78, pp. 775–783. https://doi.org/10.1007/s12562-012-0509-1

    Article  CAS  Google Scholar 

  39. Truett, G.E., Preparation of genomic DNA from animal tissues, in DNA Sequencing II: Optimizing Preparation and Cleanup, Boston: Jones and Bartlett, 2006, chapter 3, pp. 33–46.

    Google Scholar 

  40. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., and Shipley, P., MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data, Mol. Ecol. Notes, 2004, vol. 4, no. 3, pp. 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

The authors are grateful to E.I. Bondar (Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences), I. Chybicki (Casimir the Great University, Poland), and M.J. Dąbrowski (Museum and Institute of Zoology of the Polish Academy of Sciences) for help in research.

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Correspondence to V. D. Yagodina.

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Translated by T. Koznova

APPENDIX

APPENDIX

Таблица 6. Null allele frequency for 5 loci of the sea cucumber samples according to statistical programs

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Yagodina, V.D., Batishcheva, N.M. & Brykov, V.A. Variation at Nuclear Loci in the Japanese Sea Cucumber Apostichopus japonicus (Selenka, 1867) (Echinodermata: Holothuroidea) in Samples from Peter the Great Bay, Sea of Japan. Russ J Mar Biol 48, 380–388 (2022). https://doi.org/10.1134/S1063074022050212

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