Genetic Diversity of mtDNA of the Far Eastern Sea Cucumber Apostichopus japonicus (Selenka, 1867) (Echinodermata: Holothuroidea) in Peter the Great Gulf, Sea of Japan

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Abstract

The genetic diversity of the Far Eastern sea cucumber Apostichopus japonicus (Selenka, 1867), which lives in Peter the Great Gulf, Sea of Japan has been studied. Five samples were analyzed using the mitochondrial DNA’s COI gene fragment. A total of 16 haplotypes were identified, with high haplotype diversity (0.86767 ± 0.01800) and low nucleotide diversity (0.00759 ± 0.00025). The results using AMOVA and pairwise Fst did not reveal significant genetic differences between the samples from Peter the Great Gulf. Based on the data obtained and the structure of the haplotype network, it was suggested that the Far Eastern sea cucumber lives in non-equilibrium conditions. This relates to the uneven distribution of juveniles, depending on the hydrological regime, the type of soil and the development of mariculture in the water area, as well as a significant illegal catch.

About the authors

V. D. Yagodina

A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences

Author for correspondence.
Email: iagodinavd@gmail.com
Russia, 690041, Vladivostok

V. A. Brykov

A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences

Email: iagodinavd@gmail.com
Russia, 690041, Vladivostok

References

  1. Левин В.С. Дальневосточный трепанг: биология, промысел, воспроизводство. СПб.: Голанд. 2000. 200 с.
  2. Лысенко В.Н., Жариков В.В., Лебедев А.М. Современное состояние поселений дальневосточного трепанга Apostichopus japonicus (Selenka, 1867) в Дальневосточном морском заповеднике // Биол. моря. 2018. Т. 44. № 2. С. 134–140.
  3. Селин Н.И. Вертикальное распределение дальневосточного трепанга Apostichopus japonicus в заливе Восток Японского моря // Биол. моря. 2001. Т. 27. № 4. С. 297–299.
  4. Терехова В.Е., Белькова Н.Л. Идентификация оппортунистических патогенов трепанга (Apostichopus japonicus), культивируемого в Приморском крае // Вода: химия и экология. 2016. № 1. С. 36–42.
  5. Adachi K., Okumura S., Moriyama S. Genetic structure of Japanese sea cucumbers (Apostichopus japonicus) along the Sanriku coast supports the effect of earthquakes and related tsunamis // Genetica. 2018. V. 146. № 6. P. 497–503. https://doi.org/10.1007/s10709-018-0041-z
  6. Avise J.C. Phylogeography: The History and Formation of Species. Harvard: Harvard Univ. Press. 2000. 464 p.
  7. Bandelt H.-J., Forster P., Röhl A. Median-joining networks for inferring intraspecific phylogenies // Mol. Biol. Evol. 1999. V. 16. № 1. P. 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
  8. Chang Y., Feng Z., Yu J., 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. V. 30. P. 455–461. https://doi.org/10.1111/j.1439-0485.2009.00292.x
  9. Chen L., Yang J. Microsatellite genetic variation in wild and hatchery populations of the sea cucumber (Apostichopus japonicus Selenka) from northern China // Aqua. Res. 2008. V. 39. P. 1541–1549. https://doi.org/10.1111/j.1365-2109.2008.02027.x
  10. Dong Y., Li Q., Zhong X., 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 Aqua. Soc. 2016. V. 47. № 6. P. 873–888. https://doi.org/10.1007/s12686-013-9858-z
  11. 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. V. 13. P. 7080–7097. https://doi.org/10.3390/ijms13067080
  12. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity // BMC Bioinform. 2004. V. 5. P. 113. https://doi.org/10.1186/1471-2105-5-113
  13. Excoffier L., 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. V. 10. P. 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
  14. Excoffier L., Smouse P., Quattro J. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data // Genetics. 1992. V. 131. P. 479–491. https://doi.org/10.1093/genetics/131.2.479
  15. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap // Evolution. 1985. V. 39. P. 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb004
  16. Fu Y.X. Statistical test of neutrality of mutation against population growth, hitchhiking and background selection // Genetics. 1997. V. 147. № 2. P. 915–925. https://doi.org/10.1093/genetics/147.2.915
  17. Hamamoto K., Soliman T., Poliseno A., Iria Fernandez-Silva I., Reimer J.D. Higher genetic diversity of the common sea cucumber Holothuria (Halodeima) atra in marine protected areas of the Central and Southern Ryukyu Islands // Front. Conserv. Sci. 2021. V. 2. P. 736633. https://doi.org/10.3389/fcosc.2021.736633
  18. Harpending R.C. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution // Hum. Biol. 1994. V. 66. P. 591–600.
  19. Hedgecock D., Pudovkin A.I. Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary // Bull. Mar. Sci. 2011. V. 87. № 4. P. 971–1002. https://doi.org/10.5343/bms.2010.1051
  20. Hoareau T.B., Boissin E. Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata // Mol. Ecol. Res. 2010. V. 10. P. 960–967. https://doi.org/10.1111/j.1755-0998.2010.02848.x
  21. Kanno M., Li Q., Kijima A. Microsatellite analysis of Japanese sea cucumber, Stichopus (Apostichopus) japonicus, supports reproductive isolation in color variants // Mar. Biotech. 2006. V. 8. P. 672–685. https://doi.org/10.1007/s10126-006-6014-8
  22. Karl S.A., Toonen R.J., Grant W.S., Bowen B.W. Common misconceptions in molecular ecology: echoes of the modern synthesis // Mol. Ecol. 2012. V. 21. P. 4171–4189. https://doi.org/10.1111/j.1365-294X.2012.05576.x
  23. Kim M., Choi T., An H.S. Population genetic structure of sea cucumber, Stichopus japonicus in Korea using microsa-tellite markers // Aqua. Res. 2008. V. 39. P. 1038–1045. https://doi.org/10.1111/j.1365-2109.2008.01962.x
  24. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences // J. Mol. Evol. 1980. V. 16. № 2. P. 111–120. https://doi.org/10.1007/BF01731581
  25. Marjoram P., Donnelly P. Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution // Gene-tics. 1994. V. 136. P. 673–683. https://doi.org/10.1093/genetics/136.2.673
  26. Nehemia A., Kochzius M. Reduced genetic diversity and alteration of gene flow in a fiddler crab due to mangrove degradation // PLoS One. 2017. V. 12. P.8. https://doi.org/10.1371/journal.pone.0182987
  27. Oh G.-W., Ko S.-C., Lee D.H. et al. Biological activities and biomedical potential of sea cucumber (Stichopus japo-nicus): a review // Fish. Aqua. Sci. 2017. V. 20. https://doi.org/10.1186/s41240-017-0071-y
  28. Palumbi S.R., Wilson A.C. Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and S. droebachiensis // Evolution. 1990. V. 44. P. 403–415. https://doi.org/10.1111/j.1558-5646.1990.tb05208.x
  29. Purcell S.W., Samyn Y., Conand C. Commercially important sea cucumbers of the world // FAO Species Catalogue for Fishery Purposes № 6 / Eds. N. De Angelis, A. Lovatelli. 2012. P. 223.
  30. Qiu T., Zhang T., Hamel J.-F., Mercier A. Development, settlement, and post-settlement growth // The Sea Cucumber Apostichopus japonicus History, Biology and Aquaculture / Eds. H. Yang, J.-F. Hamel, A. Mercier. Academic Press. 2015. P. 111–131. https://doi.org/10.1016/B978-0-12-799953-1.00008-8
  31. Ray N., Currat M., Excoffier L. Intra-deme molecular diversity in spatially expanding populations // Mol. Biol. Evol. 2003. V. 20. P. 76–86. https://doi.org/10.1093/molbev/msg009
  32. Rodrigues F., Valente S., González-Wanguemert M. Genetic diversity across geographical scales in marine coastal ecosystems: Holothuria arguinensis a model species // J. Exp. Mar. Biol. Ecol. 2015. V. 463. P. 158–167. https://doi.org/10.1016/j.jembe.2014.12.006
  33. Rogers A.R. Genetic evidence for a Pleistocene population expansion // Evolution. 1995. V. 49. P. 608–615. https://doi.org/10.1111/j.1558-5646.1995.tb02297.x
  34. Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J.C. et al. DnaSP 6: DNA sequence polymorphism analysis of large datasets // Mol. Biol. Evol. 2017. V. 34. № 12. P. 3299–3302.https://doi.org/10.1093/molbe v/msx248
  35. Schneider S., Excoffier L. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA // Genetics. 1999. V. 152. P. 1079–1089. https://doi.org/10.1093/genetics/152.3.1079
  36. Selenka E. Beiträge zur Anatomie und Systematik der Holothurien // Zoology. 1867. V. 17. P. 291–374.
  37. Simões T.D., Azevedo E., Silva F.H. et al. Ecological traits of sea cucumbers with commercial relevance from the north-eastern Atlantic coast // Front. Mar. Sci. Conference Abstract: IMMR'18. 2019. https://doi.org/10.3389/conf.FMARS.2018.06.00147
  38. So J., Uthicke S., Hamel J.-F., Mercier A. Genetic population structure in a commercial marine invertebrate with long-lived lecithotrophic larvae: Cucumaria frondosa (Echinodermata: Holothuroidea) // Mar. Biol. 2011. V. 158. P. 859–870. https://doi.org/10.1007/s00227-010-1613-3
  39. Soliman T., Kanno M., Kijima A., Yamazaki Y. Population genetic structure and gene flow in the Japanese sea cucumber Apostichopus japonicus across Toyama Bay, Japan // Fish. Sci. 2012. V. 78. P. 775–783. https://doi.org/10.1007/s12562-012-0509-1
  40. Soliman T., Fernandez-Silva I., Reimer J.D. Genetic population structure and low genetic diversity in the over-exploited sea cucumber Holothuria edulis Lesson, 1830 (Echinodermata: Holothuroidea) in Okinawa Island // Conserv. Genetics. 2016. V. 17. P. 811–821. https://doi.org/10.1007/s10592-016-0823-8
  41. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism // Genetics. 1989. V. 123. P. 585–595. https://doi.org/10.1093/genetics/123.3.585
  42. Tamura K., Stecher G., Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11 // Mol. Biol. Evol. 2021. V. 38. P. 3022–3027. https://doi.org/10.1093/molbev/msab120
  43. Truett G.E. Preparation of Genomic DNA from Animal Tissues // DNA Sequencing II: Optimizing Preparation and Cleanup / Ed. J. Kieleczawa. Sudbury: Jones and Bartlett Publishers. 2006. P. 33–46.
  44. Tyler P.A., Young C.M.D., Billett S.M., Giles L.A. Pairing behaviour, reproduction and diet in the deep-sea holothurian genus Paroriza (Holothurioidea: Synallactidae) // J. Mar. Biol. Assoc. U. K. 1992. V. 72.2. P. 447–462. https://doi.org/10.1017/S0025315400037814
  45. Uthicke S., Benzie J.A.H. Gene flow and population history in high dispersal marine invertebrates: Mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-pacific // Mol. Ecol. 2003. V. 12. P. 2635–2648. https://doi.org/10.1046/j.1365-294X.2003.01954.x
  46. Valente S., Serrão E.A., González-Wangüemert M. West versus East Mediterranean Sea: origin and genetic diffe-rentiation of the sea cucumber Holothuria polii // Mar. Ecol. 2014. V. 36. № 3. P. 485–495. https://doi.org/10.1111/maec.12156
  47. Watts R.J., Johnson M.S., Black R. Effects of recruitment on genetic patchiness in the urchin Echinometra mathaei in Western Australia // Mar. Biol. 1990. V. 105. P. 145–151.
  48. Yagodina V.D., Bondar E.I., Brykov V.A. Genetic variability and population structure of the Japanese sea cucumber, Apostichopus japonicus Selenka, 1867 revealed by microsatellites in Peter the Great Gulf, Sea of Japan // Mar. Biodivers. 2022. V. 52. P. 40. https://doi.org/10.1007/s12526-022-01278-0
  49. Yan J., Jing J., Mu X. et al. A genetic linkage map of the sea cucumber (Apostichopus japonicus) based on microsa-tellites and SNPs // Aquaculture. 2013. V. 404–405. P. 1–7. https://doi.org/10.1016/j.aquaculture.2013.04.011

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