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Mitochondrial DNA sequence variation, demographic history, and population structure of Amur sturgeon Acipenser schrenckii Brandt, 1869

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Abstract

The variability of the mtDNA control region (D-loop) was examined in Amur sturgeon endemic to the Amur River. This species is also classified as critically endangered by the IUCN Red List of Threatened species. Sequencing of 796- to 812-bp fragments of the D-loop in 112 sturgeon collected in the Lower Amur revealed 73 different genotypes. The sample was characterized by a high level of haplotypic (0.976) and nucleotide (0.0194) diversity. The identified haplotypes split into two well-defined monophyletic groups, BG (n = 39) and SM (n = 34), differing (HKY distance) on average by 3.41% of nucleotide positions with an average level of intragroup differences of 0.54 and 1.23%, respectively. Moreover, the haplotypes of the SM groups differed by the presence of a 13–14 bp deletion. Most of the specimens (66 out of 112) carried BG haplotypes. Overall, the pattern of pairwise nucleotide differences and the results of neutrality tests, as well as the results of tests for compliance with the model of sudden demographic expansion or with the model of exponential growth pointed to a past significant increase in the number of Amur sturgeon, which was most clearly manifested in the analysis of data on the BG haplogroup. The constructed Bayesian skyline plots showed that this growth began about 18-16 thousand years ago. At present, the effective size of the strongly reduced (due to overfishing) population of Amur sturgeon may be equal to or even lower than it was before the beginning of this growth during the Last Glacial Maximum. The presence in the mitochondrial gene pool of Amur sturgeon of two haplogroups, their unequal evolutionary dynamics, and, judging by scanty data, their unequal representation in the Russian and Chinese parts of the Amur River basin point to the possible existence of at least two distinct populations of Amur sturgeon in the past.

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References

  1. Bemis, W.E., Findeis, E.K., and Grande, L., An overview of Acipenseriformes, Environ. Biol. Fishes, 1997, vol. 48, pp. 25–71.

    Article  Google Scholar 

  2. Ludwig, A., Belfiore, N., and Pitra, C., Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus), Genetics, 2001, vol. 158, pp. 1203–1215.

    PubMed Central  CAS  PubMed  Google Scholar 

  3. Krieger, J., Hett, A.K., Fuerst, P.A., et al., The molecular phylogeny of the order Acipenseriformes revisited, J. Appl. Ichthyol., 2008, vol. 24, suppl. 1, pp. 36–45.

    Article  Google Scholar 

  4. Soldatov, V.K., The study of acipenserids of Amur River, Mater. Poznaniyu Russ. Rybolov., 1915, vol. 3, no. 12, pp. 96–415.

    Google Scholar 

  5. Nikol’skii, G.V., Ryby basseina Amura (Itogi Amurskoi ikhtiologicheskoi ekspeditsii, 1945–1949 gg.) (Fishes of Amur Basin (Results of the Amur Ichthyological Expedition)), Moscow: Akad. Nauk SSSR, 1956.

    Google Scholar 

  6. Omoto, N., Maebayashi, M., Hara, A., et al., Gonadal maturity in wild sturgeons, Huso dauricus, Acipenser mikadoi and A. schrenckii caught near Hokkaido, Japan, Environ. Biol. Fishes, 2004, vol. 70, no. 4, pp. 381–391.

    Article  Google Scholar 

  7. Krykhtin, M.L. and Svirskii, V.G., Endemic sturgeons of the Amur River: kaluga, Huso dauricus, and Amur sturgeon, Acipenser schrenckii, Environ. Biol. Fishes, 1997, vol. 48, pp. 231–239.

    Article  Google Scholar 

  8. Wang, Y. and Chang, J., Status and conservation of sturgeons in Amur River, China: a review based on surveys since the year 2000, J. Appl. Ichthyol., 2006, vol. 22, suppl. 1, pp. 44–52.

    Article  Google Scholar 

  9. Ruban, G. and Qiwei, W., Acipenser schrenckii, in IUCN 2013: IUCN Red List of Threatened Species. Version 2013.2, 2013. http://www.iucnredlist.org. Accessed June 3, 2014.

    Google Scholar 

  10. Vasil’ev, V.P., Vasil’eva, E.D., Shedko, S.V., and Novomodny, G.V., How many times has polyploidization occurred during acipenserid evolution? New data on the karyotypes of sturgeons (Acipenseridae, Actinopterygii) from the Russian Far East, J. Ichthyol., 2010, vol. 50, no. 10, pp. 950–959.

    Article  Google Scholar 

  11. Mugue, N.S., Barmintseva, A.E., Rastorguev, S.M., et al., Polymorphism of the mitochondrial DNA control region in eight sturgeon species and development of a system for DNA-based species identification, Russ. J. Genet., 2008, vol. 44, no. 7, pp. 793–798.

    Article  CAS  Google Scholar 

  12. Staden, R., Beal, K.F., and Bonfield, J.K., The Staden package, 1998, Methods Mol. Biol., 2000, vol. 132, pp. 115–130.

    CAS  PubMed  Google Scholar 

  13. Katoh, K., Misawa, K., Kuma, K., and Miyata, T., MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 2002, vol. 30, pp. 3059–3066.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Villesen, P., FaBox: an online toolbox for fasta sequences, Mol. Ecol. Notes, 2007, vol. 7, no. 6, pp. 965–968.

    Article  CAS  Google Scholar 

  15. 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. Res., 2010, vol. 10, no. 3, pp. 564–567.

    Article  Google Scholar 

  16. Swofford, D.L., PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods): Version 4, Sunderland: Sinauer Associates, 2002.

    Google Scholar 

  17. Ewens, W.J., The sampling theory of selectively neutral alleles, Theor. Popul. Biol., 1972, vol. 3, no. 1, pp. 87–112.

    Article  CAS  PubMed  Google Scholar 

  18. Watterson, G.A., The homozygosity test of neutrality, Genetics, 1978, vol. 88, no. 2, pp. 405–417.

    PubMed Central  CAS  PubMed  Google Scholar 

  19. Tajima, F., Statistical method for testing the neutral mutation hypothesis by DNA polymorphism, Genetics, 1989, vol. 123, no. 3, pp. 585–595.

    PubMed Central  CAS  PubMed  Google Scholar 

  20. Fay, J.C. and Wu, C.I., Hitchhiking under positive Darwinian selection, Genetics, 2000, vol. 155, no. 3, pp. 1405–1413.

    PubMed Central  CAS  PubMed  Google Scholar 

  21. Fu, Y.X., Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection, Genetics, 1997, vol. 147, no. 2, pp. 915–925.

    PubMed Central  CAS  PubMed  Google Scholar 

  22. Kelly, J.K., A test of neutrality based on interlocus associations, Genetics, 1997, vol. 146, no. 3, pp. 1197–1206.

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Eckert, A.J., Liechty, J.D., Tearse, B.R., et al., DnaSAM: software to perform neutrality testing for large datasets with complex null models, Mol. Ecol. Res., 2010, vol. 10, pp. 542–545.

    Article  CAS  Google Scholar 

  24. Watterson, G.A., The homozygosity test after a change in population size, Genetics, 1986, vol. 112, no. 4, pp. 899–907.

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Zeng, K., Fu, Y.-X., Shi, S., and Wu, C.-I., Statistical tests for detecting positive selection by utilizing high-frequency variants, Genetics, 2006, vol. 174, no. 3, pp. 1431–1439.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Rogers, A. and Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences, Mol. Biol. Evol., 1992, vol. 9, no. 3, pp. 552–569.

    CAS  PubMed  Google Scholar 

  27. Schneider, S. and 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, vol. 152, no. 3, pp. 1079–1089.

    PubMed Central  CAS  PubMed  Google Scholar 

  28. Kuhner, M.K., Yamato, J., and Felsenstein, J., Maximum likelihood estimation of population growth rates based on the coalescent, Genetics, 1998, vol. 149, no. 1, pp. 429–434.

    PubMed Central  CAS  PubMed  Google Scholar 

  29. Drummond, A., Nicholls, G., Rodrigo, A., and Solomon, W., Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data, Genetics, 2002, vol. 161, pp. 1307–1320.

    PubMed Central  CAS  PubMed  Google Scholar 

  30. Drummond, A.J., Suchard, M.A., Xie, D., and Rambaut, A., Bayesian phylogenetics with BEAUti and the BEAST 1.7, Mol. Biol. Evol., 2012, vol. 29, no. 8, pp. 1969–1973.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Pybus, O.G., Rambaut, A., and Harvey, P.H., An integrated framework for the inference of viral population history from reconstructed genealogies, Genetics, 2000, vol. 155, no. 3, pp. 1429–1437.

    PubMed Central  CAS  PubMed  Google Scholar 

  32. Drummond, A.J., Rambaut, A., Shapiro, B., and Pybus, O.G., Bayesian coalescent inference of past population dynamics from molecular sequences, Mol. Biol. Evol., 2005, vol. 22, no. 5, pp. 1185–1192.

    Article  CAS  PubMed  Google Scholar 

  33. Brown, J.R., Beckenbach, A.T., and Smith, M.J., Intraspecific DNA sequence variation of the mitochondrial control region of white sturgeon (Acipenser transmontanus), Mol. Biol. Evol., 1993, vol. 10, no. 2, pp. 326–341.

    CAS  PubMed  Google Scholar 

  34. Wang, W., Hua, Z., Hu, H.-X., et al., Heteroplasmy in mtDNA control region and phylogenetics of five sturgeons, Zool. Res., 2009, vol. 30, no. 5, pp. 487–496.

    Article  CAS  Google Scholar 

  35. Raymond, M. and Rousset, F., An exact test for population differentiation, Evolution, 1995, vol. 49, no. 6, pp. 1280–1283.

    Article  Google Scholar 

  36. Excoffier, L., Smouse, P.E., and Quattro, J.M., Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data, Genetics, 1992, vol. 131, no. 2, pp. 479–491.

    PubMed Central  CAS  PubMed  Google Scholar 

  37. Niu, C.-J., Hu, H.-X., Luo, J., and Li, C., Genetic diversity in the reserved parent fish broodstocks of Asipenser schrenckii and Huso dauricus, J. Fish. China, 2010, vol. 34, no. 12, pp. 1795–1799.

    CAS  Google Scholar 

  38. Wang, W., Zhu, H., and Hu, H.-X., Genetic diversity of the reserved broodstocks in four species of sturgeon, Chin. J. Zool., 2012, vol. 47, no. 1, pp. 105–111.

    CAS  Google Scholar 

  39. Zhang, S.M., Wang, D.Q., and Zhang, Y.P., Mitochondrial DNA variation, effective female population size and population history of the endangered Chinese sturgeon, Acipenser sinensis, Conserv. Genet., 2003, vol. 4, no. 6, pp. 673–683.

    Article  CAS  Google Scholar 

  40. Qiwei, W., Acipenser sinensis, in IUCN 2013: IUCN Red List of Threatened Species. Version 2013.2, 2013. http://www.iucnredlist.org. Accessed June 3, 2014.

    Google Scholar 

  41. Duke, S., Down, T., Ptolemy, J., et al., Acipenser transmontanus, in IUCN 2013: IUCN Red List of Threatened Species. Version 2013.2, 2013. http://www.iucnredlist.org. Accessed June 3, 2014.

    Google Scholar 

  42. Weber, D.S., Stewart, B.S., and Lehman, N., Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi), J. Hered., 2004, vol. 95, no. 2, pp. 144–153.

    Article  CAS  PubMed  Google Scholar 

  43. Johnson, J.A., Dunn, P.O., and Bouzat, J.L., Effects of recent population bottlenecks on reconstructing the demographic history of prairie-chickens, Mol. Ecol., 2007, vol. 16, no. 11, pp. 2203–2222.

    Article  CAS  PubMed  Google Scholar 

  44. Wei, Q., Ke, F., Zhang, J., et al., Biology, fisheries and conservation of sturgeons and paddlefish in China, Environ. Biol. Fishes, 1997, vol. 48, pp. 241–255.

    Article  Google Scholar 

  45. Koshelev, V.N., Mikheev, P.B., Litovchenko, Zh.S., et al., Age and growth of the Amur sturgeon (Acipenser schrenckii) from Amur River, Izv. Tikhookean. Inst. Rybov. Okeanogr., 2009, vol. 159, pp. 136–147.

    Google Scholar 

  46. Slatkin, M. and Hudson, R.R., Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations, Genetics, 1991, vol. 129, no. 2, pp. 555–562.

    PubMed Central  CAS  PubMed  Google Scholar 

  47. Marjoram, P. and Donnelly, P., Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution, Genetics, 1994, vol. 136, no. 2, pp. 673–683.

    PubMed Central  CAS  PubMed  Google Scholar 

  48. Hein, J., Schierup, M.H., and Wiuf, C., Gene Genealogies, Variation and Evolution: A Primer in Coalescent Theory, Oxford Univ. Press, 2005.

    Google Scholar 

  49. Koshelev, V.N., Amur sturgeon, Acipenser schrenckii Brandt, 1869 (distribution, biology, artificial reproduction), Extended Abstract of Cand. Sci. Dissertation, Vseross. Nauchno-Issled. Inst. Rybov. Okeanogr., Moscow, 2010.

    Google Scholar 

  50. Allendorf, F.W., Isolation, gene flow and genetic differentiation among populations, in Genetics and Conservation: A Reference for Managing Wild Plant and Animal Populations, Schonewald, C.M., Chambers, S.M., MacBryde, B., and Thomas, W.L., Eds., New York: Blackburn, 1983, pp. 51–66.

    Google Scholar 

  51. Doukakis, P., Birstein, V.J., Ruban, G.I., and DeSalle, R., Molecular genetic analysis among subspecies of two Eurasian sturgeon species, Acipenser baerii and A. stellatus, Mol. Ecol., 1999, vol. 8, pp. 117–127.

    Article  Google Scholar 

  52. Grunwald, C., Stabile, J., Waldman, J., et al., Population genetics of shortnose sturgeon Acipenser brevirostrum based on mitochondrial DNA control region sequences, Mol. Ecol., 2002, vol. 11, pp. 1885–1898.

    Article  CAS  PubMed  Google Scholar 

  53. Waldman, B.J.R., Grunwald, C., Stabile, J., and Wirgin, I., Impacts of life history and biogeography on the genetic stock structure of Atlantic sturgeon Acipenser oxyrinchus oxyrinchus, gulf sturgeon A. oxyrinchus desotoi, and shortnose sturgeon A. brevirostrum, J. Appl. Ichthyol., 2002, vol. 18, pp. 509–518.

    Article  Google Scholar 

  54. Doukakis, P., Birstein, V.J., and DeSalle, R., Intraspecific structure within three caviar-producing sturgeons (Acipenser gueldenstaedtii, A. stellatus, and Huso huso) based on mitochondrial DNA analysis, J. Appl. Ichthyol., 2005, vol. 21, pp. 457–460.

    Article  CAS  Google Scholar 

  55. Bemis, W.E. and Kynard, B., Sturgeon rivers: an introduction to acipenseriform biogeography and life history, Environ. Biol. Fishes, 1997, vol. 48, pp. 167–183.

    Article  Google Scholar 

  56. Lindberg, G.U., Krupnye kolebaniya urovnya okeana v chetvertichnyi period: biogeograficheskie obosnovaniya gipotezy (Large-Scale Fluctuations of Sea Level in the Quaternary Period: Hypothesis Based on Biogeographical Evidence), Leningrad: Nauka, 1972.

    Google Scholar 

  57. Frankham, R., Effective population size/adult population size ratios in wildlife: a review, Genet. Res., 1995, vol. 66, no. 2, pp. 95–107.

    Article  Google Scholar 

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Correspondence to S. V. Shedko.

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Original Russian Text © S.V. Shedko, I.L. Miroshnichenko, G.A. Nemkova, V.N. Koshelev, M.B. Shedko, 2015, published in Genetika, 2015, Vol. 51, No. 2, pp. 200–216.

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Shedko, S.V., Miroshnichenko, I.L., Nemkova, G.A. et al. Mitochondrial DNA sequence variation, demographic history, and population structure of Amur sturgeon Acipenser schrenckii Brandt, 1869. Russ J Genet 51, 169–184 (2015). https://doi.org/10.1134/S102279541502012X

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