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Genetic diversity and genetic structure of the endangered Manchurian trout, Brachymystax lenok tsinlingensis, at its southern range margin: conservation implications for future restoration

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Abstract

The Manchurian trout, Brachymystax lenok tsinlingensis (family: Salmonidae), is a cold freshwater fish endemic to Northeast Asia. South Korean populations of this species, which comprise its southern range limit, have recently decreased markedly in size and are now becoming critically endangered. We assessed the current population status of this species in South Korea by estimating the levels of genetic diversity and genetic structure of five natural and four restored populations using mitochondrial DNA (mtDNA) control region sequences and eight nuclear microsatellite loci. Levels of within-population genetic diversity were low, suggesting that past effective population sizes (N e) have been small. Each population had one or a maximum of two mtDNA haplotypes. Microsatellite allelic richness (AR) was significantly higher for natural populations (mean AR = 3.51; 95% confidence interval, 3.00–4.03) than for restored populations (mean AR = 2.61; 2.38–2.98). South Korean populations were significantly genetically isolated from one another, with private mtDNA haplotypes and microsatellite alleles, suggesting that limited gene flow has been occurring among populations. A mtDNA phylogeny revealed that South Korean lineages were more closely related to those of China than to those of North Korea and Russia. Overall, we suggest that future restoration efforts aimed at South Korean populations should consider the genetic characteristics reported here, which should help to fulfil effective conservation strategies for this highly cherished species. Our results will inform other conservation efforts, including assisted migration of freshwater fish populations at the equatorial end of the geographical range limit of the species.

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References

  • Adams JM, Faure H (1997) Preliminary vegetation maps of the world since the last glacial maximum: an aid to archaeological understanding. J Archaeol Sci 24:623–647

    Article  Google Scholar 

  • Aizawa M, Kim ZS, Yoshimaru H (2012) Phylogeography of the Korean pine (Pinus koraiensis) in northeast Asia: inferences from organelle gene sequences. J Plant Res 125:713–723

    Article  PubMed  Google Scholar 

  • Antognazza CM, Andreou D, Zaccara S, Britton RJ (2016) Loss of genetic integrity and biological invasions result from stocking and introductions of Barbus barbus: insights from rivers in England. Ecol Evol 6:1280–1292

    Article  PubMed  PubMed Central  Google Scholar 

  • Bae HG, Suk HY (2015) Population genetic structure and colonization history of short ninespine sticklebacks (Pungitius kaibarae). Ecol Evol 5:3075–3089

    Article  PubMed  PubMed Central  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996/2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171. Université de Montpellier II, Montpellier

  • Boulding EG (2008) Genetic diversity, adaptive potential, and population viability in changing environments. In: Carroll S, Fox C (eds) Conservation biology: evolution in action. Oxford University Press, Oxford, pp 199–219

    Google Scholar 

  • Byeon HK, Kim KS, Song HY, Bang IC (2009) Morphological variations and genetic variations inferred from AFLP (amplified fragment length polymorphism) analysis of Cottus populations (Scorpaeniformes: Cottidae) in Korea. Korean J Ichthyol 21:67–75

    Google Scholar 

  • Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205

    Article  CAS  PubMed  Google Scholar 

  • Choi KC, Jeon SR, Kim IS, Son YM (2002) Coloured illustrations of the freshwater fishes of Korea. Hyangmunsa Press, Seoul, pp 154–156

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawnay N, Dawnay L, Hughes RN, Cove R, Taylor MI (2011) Substantial genetic structure among stocked and native populations of the European grayling (Thymallus thymallus, Salmonidae) in the United Kingdom. Conserv Genet 12:731–744

    Article  Google Scholar 

  • Dionne M, Caron F, Dodson JJ, Bernatchez L (2008) Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation. Mol Ecol 17:2382–2396

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46:185–208

    Article  CAS  PubMed  Google Scholar 

  • Froufe E, Alekseyev S, Knizhin I, Alexandrino P, Weiss S (2003) Comparative phylogeography of salmonid fishes (Salmonidae) reveals late to post-Pleistocene exchange between three now-disjunct river basins in Siberia. Divers Distrib 9:269–282

    Article  Google Scholar 

  • Froufe E, Sefc KM, Alexandrino P, Weiss S (2004) Isolation and characterization of Brachymystax lenok microsatellite loci and cross-species amplification in Hucho spp. and Parahucho perryi. Mol Ecol Notes 4:150–152

    Article  CAS  Google Scholar 

  • Froufe E, Alekseyev S, Alexandrino P, Weiss S (2008) The evolutionary history of sharp- and blunt-snouted lenok (Brachymystax lenok (Pallas, 1773) and its implications for the paleo-hydrological history of Siberia. BMC Evol Biol 8:40

    Article  PubMed  PubMed Central  Google Scholar 

  • Gjerde B, Refstie T (1988) The effect of fin-clipping on growth rate, survival and sexual maturity of rainbow trout. Aquaculture 73:383–389

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm.

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hartl DL, Clark AG (2007) Principles of population genetics. Sinauer Associates, Sunderland

  • IUCN Red List of Threatened Species (2008) http://www.iucnredlist.org/. Accessed 26 Sept 2008

  • Jia ZY, Zhang YY, Shi LY, Bai QL, Jin SB, Mou ZB (2008) Amplification of rainbow trout microsatellites in Brachymystax lenok. Mol Ecol Resour 8:1520–1521

    Article  CAS  PubMed  Google Scholar 

  • Kirchhofer A, Hefti D (1996) Conservation of endangered freshwater fish in Europe. Birkhäuser Verlag, Basel

    Book  Google Scholar 

  • Kwon T-S, Bae M-J, Hwang S-J, Kim S-H, Park Y-S (2015) Predicting potential impacts of climate change on freshwater fish in Korea. Ecol Inform 29:156–165

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Maceda-Veiga A (2012) Towards the conservation of freshwater fish: Iberian Rivers as an example of threats and management practices. Rev Fish Biol Fish 23:1–22

    Article  Google Scholar 

  • Malaj E, Peter C, Grote M, Kühne R, Mondy CP, Usseglio-Polatera P, Brack W, Schäfer RB (2014) Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale. Proc Natl Acad Sci USA 111:9549–9554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mclntyre PB, Jones LE, Flecker SA, Vanni MJ (2007) Fish extinctions alter nutrient cycling in tropical freshwaters. Proc Natl Acad Sci USA 104:4461–4466

    Article  Google Scholar 

  • Mills EL, Leach JH, Carlton JT, Secor CL (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. J Great Lakes Res 19:1–54

    Article  Google Scholar 

  • Morlon H, Kefi S, Martinez ND (2014) Effects of trophic similarity on community composition. Ecol Lett 17:1495–1506

    Article  PubMed  Google Scholar 

  • National Institute of Biological Resources (NIBR) (2011) Red Data Book of Endangered Fishes in Korea. NIBR, Incheon, pp 74–459

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  PubMed  Google Scholar 

  • Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Petit RJ, Mousadik AE, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Report of Natural Heritage Centre in Korea (2004) Research for habitat and management plan of Brachymystax lenok. The National Heritage Centre, Daejeon, pp 31–32

    Google Scholar 

  • Ricciardi A, Simberloff D (2009) Assisted colonization is not a viable conservation strategy. Trend Ecol Evol 24:248–253

    Article  Google Scholar 

  • Ronquist F, Teslenko M, Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Rourke ML, Gilligan DM (2015) Complex biogeography and historic translocations lead to complicated phylogeographic structure of freshwater eel-tailed catfish (Tandanus spp.) in south-eastern Australia. Conserv Genet 16:777–790

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Teacher AGF, Griffiths DJ (2011) HapStar: automated haplotype network layout and visualization. Mol Ecol Resour 11:151–153

    Article  CAS  PubMed  Google Scholar 

  • Uiblein F, Jagsch A, Honsig-Erlenburg W, Weiss S (2001) Status, habitat use, and vulnerability of the European grayling in Austrian waters. J Fish Biol 59:223–247

    Google Scholar 

  • Vrijenhoek RC (1998) Conservation genetics of freshwater fish. J Fish Biol 53:394–412

    Article  Google Scholar 

  • Vrijenhoek RC, Douglas ME, Meffe GK (1985) Conservation genetics of endangered fish populations in Arizona. Science 229:400–402

    Article  CAS  PubMed  Google Scholar 

  • Wang K, Zhang S, Wang D, Xin M, Wu J, Sun Q, Du H, Wang C, Huang J, Wei Q (2015) Development of 27 novel cross-species microsatellite markers for the endangered Hucho bleekeri using next-generation sequencing technology. Conserv Genet Resour 7:263–267

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J org Evol 38:1358–1370

    CAS  Google Scholar 

  • Winemiller KO, McIntyre PB, Castello L et al (2016) Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science 351:128–129

    Article  CAS  PubMed  Google Scholar 

  • Wonju Regional Environmental Office (2012) Brachymystax lenok tsinlingensis stocked in Pyeongchang Ohdaecheon. Publishing Ministry of Environment in Korea Web. http://mobile.me.go.kr/home/web/board/read.do?boardMasterId=1&boardId=183062. Accessed 19 Oct 2015 (in Korean)

  • Xia YZ, Chen YY, Sheng Y (2006) Phylogeographic structure of lenok (Brachymystax lenok Pallas) (Salmoninae, Salmonidae) populations in water systems of eastern China, inferred from mitochondrial DNA sequences. Zool Stud 45:190–200

    CAS  Google Scholar 

  • Xing Y, Zhang C, Fan E, Zhao Y (2016) Freshwater fishes of China: species richness, endemism, threatened species and conservation. Divers Distrib 22:358–370

    Article  Google Scholar 

  • Xu G, Wang F, Liu Y, Li Y, Mou Z (2009) Threatened fishes of the world: Brachymystax lenok (Pallas 1773). Environ Biol Fish 85:299–300

    Article  Google Scholar 

  • Yu JN, Kwak M (2015) The complete mitochondrial genome of Brachymystax lenok tsinlingensis (Salmoninae, Salmonidae) and its intraspecific variation. Gene 573:246–253

    Article  CAS  PubMed  Google Scholar 

  • Yu JN, Kim S, Lim CE (2014) Development of 21 novel microsatellite markers for conservation genetic studies of Brachymystax lenok tsinlingensis, an endangered species in Korea, using next generation sequencing. Conserv Genet Resour 6:213–216

    Article  Google Scholar 

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Acknowledgements

This study was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MEST; NRF-2014R1A1A2059401) to HJL, the Ministry of Oceans and Fisheries, Korea (Project title: Long-term changes in structure and function in the marine ecosystems of Korea) to HJL and the Sangji University Research Fund, 2014 to HJL. We thank members of the Molecular Ecology and Evolution Laboratory and Animal Ecology Laboratory (especially Seung-Hyun Lee) of Sangji University for helping to collect samples in the field. We also thank Elizabeth G. Boulding and Angela Tie for English editing and instructive comments on an earlier version of this manuscript.

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Authors and Affiliations

  1. Molecular Ecology and Evolution Laboratory, Department of Biological Science, College of Science and Engineering, Sangji University, Wonju, 26339, South Korea

    Ji Eun Jang, Jae Hwan Kim, Song Yi Baek & Hyuk Je Lee

  2. Korean Entomological Institute, Korea University, Seoul, 02841, South Korea

    Ji Hyoun Kang

  3. Animal Ecology Laboratory, Department of Biological Science, College of Science and Engineering, Sangji University, Wonju, 26339, South Korea

    Ju-hyoun Wang, Hwang-Goo Lee & Jun-Kil Choi

  4. Institute of Environmental Research, Kangwon National University, Chuncheon, 24341, South Korea

    Jae-Seok Choi

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  1. Ji Eun Jang
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Jang, J.E., Kim, J.H., Kang, J.H. et al. Genetic diversity and genetic structure of the endangered Manchurian trout, Brachymystax lenok tsinlingensis, at its southern range margin: conservation implications for future restoration. Conserv Genet 18, 1023–1036 (2017). https://doi.org/10.1007/s10592-017-0953-7

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