Conservation Genetics

, Volume 19, Issue 2, pp 467–480 | Cite as

Genetic diversity and population structure of the northern snakehead (Channa argus Channidae: Teleostei) in central China: implications for conservation and management

  • Ruo-Jin Yan
  • Gui-Rong Zhang
  • Xiang-Zhao Guo
  • Wei Ji
  • Kun-Ci Chen
  • Gui-Wei Zou
  • Kai-Jian Wei
  • Jonathan P. A. Gardner
Research Article


Major threats to freshwater fish diversity now include loss of native genetic diversity as a consequence of translocations of fishes between sites and from hatcheries to sites, and small effective population sizes resulting from overfishing and/or habitat loss. Ten polymorphic microsatellite markers were employed to evaluate genetic diversity, population genetic structure and gene flow amongst nine populations of the ecologically and economically important fish, the northern snakehead (Channa argus), in three river systems in central China. Multiple analyses revealed evidence of high genetic diversity and pronounced subdivision based on both regional separation and on river systems. A lack of evidence of genetic bottleneck over recent generations was consistent with the long-term stability of population size and contemporary distribution. The effective population sizes for most C. argus populations were small, suggesting the need for future conservation efforts focusing on these populations. Different lines of evidence point to the local enhancement of stocks by both aquaculture-reared fish and the transfer of wild fish. This study illustrates how human activities may affect genetic diversity and population genetic structure of C. argus populations, and highlights the need for new management regimes to protect native freshwater fish genetic diversity.


Genetic diversity Microsatellites Channa argus Human-mediated transport Yangtze-Huai-Huang river system 



We thank Tian-Xi Fu and Hai-Ping Chen for assistance with sample collection. This work was supported by the Scientific Research Foundation for the Introduction of High-level Talents, Huazhong Agricultural University (Grant No. 2012RC012) and by the National Key Technology R&D Program (Grant No. 2012BAD26B03).

Compliance with ethical standards

Ethical approval

No specific permits were required for the field studies described here. We confirm that the study locations were not privately owned or protected, and the field sampling activities did not involve endangered or protected species beyond the focal species. All animal research protocols were approved by the Animal Research Oversight Committee of Huazhong Agricultural University (HZAU) and the Institutional Animal Care and Use Committee of HZAU, the methods were carried out in accordance with the approved guidelines.

Supplementary material

10592_2017_1023_MOESM1_ESM.doc (82 kb)
Supplementary material 1 (DOC 82 KB)


  1. Abraham RK, Kelkar N (2012) Do terrestrial protected areas conserve freshwater fish diversity? Results from the Western Ghats of India. Oryx 46:544–553CrossRefGoogle Scholar
  2. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323CrossRefGoogle Scholar
  3. Araki H, Schmid C (2010) Is hatchery stocking a help or harm?: evidence, limitations and future directions in ecological and genetic surveys. Aquaculture 308:S2–S11CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  5. Bogutskaya NG, Naseka AM (2002) An overview of nonindigenous fishes in inland waters of Russia. Proc Zool Inst Rus Acad Sci 296:21–30Google Scholar
  6. Bondad-Reantaso MG (2007) Assessment of freshwater fish seed resources for sustainable aquaculture. FAO, RomeGoogle Scholar
  7. Bromaghin JF (2008) BELS: backward elimination locus selection for studies of mixture composition or individual assignment. Mol Ecol Resour 8:568–571CrossRefPubMedGoogle Scholar
  8. Chen MM, Zheng Y, Hao YJ, Mei ZG, Wang KX, Zhao QZ, Zheng JS, Wang D (2016) Parentage-based group composition and dispersal pattern studies of the Yangtze finless porpoise population in Poyang lake. Int J Mol Sci 17:1268CrossRefPubMedCentralGoogle Scholar
  9. Chessman BC (2013) Do protected areas benefit freshwater species? A broad-scale assessment for fish in Australia’s Murray-Darling Basin. J Appl Ecol 50:969–976CrossRefGoogle Scholar
  10. Courtenay WR, Williams JD (2004) Snakeheads (Pisces, Channidae): a biological synopsis and risk assessment. Department of Interior, United States Geological Survey, RestonGoogle Scholar
  11. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214CrossRefPubMedGoogle Scholar
  12. Dong XP, Mu SM, Zhou N, Kang XJ, Luo Q, Bai JJ (2014) Structure analysis of mtDNA D-loop region and the genetic diversity of Channa argus in different populations. J Fish China 38:1277–1285 (in Chinese with English abstract: available at—
  13. Dudgeon D, Arthington AH, Gessner MO, Kawabata ZI, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard AH, Soto D, Stiassny MLJ, Sullivan CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182CrossRefPubMedGoogle Scholar
  14. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  15. Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  16. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  17. 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 10:564–567CrossRefPubMedGoogle Scholar
  18. Faubet P, Waples RS, Gaggiotti OE (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol Ecol 16:1149–1166CrossRefPubMedGoogle Scholar
  19. Fisheries Bureau of China’s Ministry of Agriculture (2015) China fishery year books. China Agriculture Press, BeijingGoogle Scholar
  20. Gagnaire PA, Broquet T, Aurelle D, Viard F, Souissi A, Bonhomme F, Arnaud-Haond S, Bierne N (2015) Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evol Appl 8:769–786CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gao XY, Starmer JD (2008) AWclust: point-and-click software for non-parametric population structure analysis. BMC Bioinform 9:77CrossRefGoogle Scholar
  22. Guo XZ, Zhang GR, Wei KJ, Yan RJ, Ji W, Yang RB, Wei QW, Gardner JPA (2016) Phylogeography and population genetics of Schizothorax o’connori: strong subdivision in the Yarlung Tsangpo river inferred from mtDNA and microsatellite markers. Sci Rep 6:29821CrossRefPubMedPubMedCentralGoogle Scholar
  23. Herborg LM, Mandrak NE, Cudmore BC, MacIsaac HJ (2007) Comparative distribution and invasion risk of snakehead (Channidae) and Asian carp (Cyprinidae) species in North America. Can J Fish Aquat Sci 64:1723–1735CrossRefGoogle Scholar
  24. Ji W, Zhang GR, Ran W, Gardner JPA, Wei KJ, Wang WM, Zou GW (2014) Genetic diversity of and differentiation among five populations of blunt snout bream (Megalobrama amblycephala) revealed by SRAP markers: implications for conservation and management. PLoS One 9:e108967CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefPubMedGoogle Scholar
  26. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  28. Kang B, Deng JM, Wu YF, Chen LQ, Zhang J, Qiu HY, Lu Y, He DM (2014) Mapping China’s freshwater fishes: diversity and biogeography. Fish Fish 15:209–230CrossRefGoogle Scholar
  29. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lapointe NWR, Odenkirk JS, Angermeier PL (2013) Seasonal movement, dispersal, and home range of Northern Snakehead Channa argus (Actinopterygii, Perciformes) in the Potomac river catchment. Hydrobiologia 709:73–87CrossRefGoogle Scholar
  31. Lawrence DJ, Larson ER, Liermann CAR, Mims MC, Pool TK, Olden JD (2011) National parks as protected areas for US freshwater fish diversity. Conserv Lett 4:364–371CrossRefGoogle Scholar
  32. Li Y, Abbas K, Ma XF, Wang WM (2009) Isolation and characterization of polymorphic microsatellite loci from Yellowcheek (Elopichthys bambusa). Conserv Genet 10:1811CrossRefGoogle Scholar
  33. Liao XL, Yu XM, Tong JG (2006) Genetic diversity of common carp from two largest Chinese lakes and the Yangtze River revealed by microsatellite markers. Hydrobiologia 568:445–453CrossRefGoogle Scholar
  34. Liu S, Zhu XP, Chen KC, Zhao J, Pan DB, Li KB (2011) Morphological variations of Channa maculata, Channa argus and their hybrid (C. maculate ♀ × C. argus ♂). J Huazhong Agricult Univ 30:488–493Google Scholar
  35. Magurran AE (2009) Threats to freshwater fish. Science 325:1215–1216CrossRefPubMedGoogle Scholar
  36. Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using “Monmonier’s algorithm”. Hum Biol 76:173–190CrossRefPubMedGoogle Scholar
  37. McCusker MR, Bentzen P (2010) Positive relationships between genetic diversity and abundance in fishes. Mol Ecol 19:4852–4862CrossRefPubMedGoogle Scholar
  38. Miller MP (2005) Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724CrossRefPubMedGoogle Scholar
  39. Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RF, Allendorf FW (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5:328–331CrossRefPubMedPubMedCentralGoogle Scholar
  40. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170CrossRefPubMedGoogle Scholar
  41. Nevill J (2006) Freshwater protected areas in Australia. OnlyOnePlanet Consulting. Accessed 28 June 2017
  42. Odenkirk J, Owens S (2005) Northern snakeheads in the tidal Potomac River system. Trans Am Fish Soc 134:1605–1609CrossRefGoogle Scholar
  43. Orrell TM, Weigt L (2005) The Northern Snakehead Channa argus (Anabantomorpha: Channidae), a non-indigenous fish species in the Potomac River, USA. Proc Biol Soc Wash 118:407–415CrossRefGoogle Scholar
  44. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  45. Piry S, Luikart G, Cornuet JM (1999) Bottleneck: a program for detecting recent effective population size reductions from allele data frequencies. J Hered 90:502–503CrossRefGoogle Scholar
  46. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539CrossRefPubMedGoogle Scholar
  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  48. Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627CrossRefPubMedGoogle Scholar
  49. R Development Core Team (2017) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna.
  50. Rousset F (2008) Genepop’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  51. Takezaki N, Nei M, Tamura K (2009) Poptree2: software for constructing population trees from allele frequency data and computing other population statistics with Windows interface. Mol Biol Evol 27:747–752CrossRefPubMedPubMedCentralGoogle Scholar
  52. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  53. Wang CY, Yu XM, Tong JG (2007) Microsatellite diversity and population genetic structure of redfin culter (Culter erythropterus) in fragmented lakes of the Yangtze River. Hydrobiologia 586:321–329CrossRefGoogle Scholar
  54. Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262CrossRefPubMedGoogle Scholar
  55. Wei K, Wood AR, Gardner JPA (2013) Population genetic variation in the New Zealand greenshell mussel: locus-dependent conflicting signals of weak structure and high gene flow balanced against pronounced structure and high self-recruitment. Mar Biol 160:931–949CrossRefGoogle Scholar
  56. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedPubMedCentralGoogle Scholar
  57. Xiao MS, Cui F, Kang J, Zhang XH (2013) Genetic structure and variation of wild Ophicephalus argus cantor from Huaihe River based on MtDNA D-loop sequences. J Huazhong Normal Univ (Nat Sci) 47:82–90Google Scholar
  58. Yan RJ, Wei KJ, Guo XZ, Zhang GR, Gardner JPA, Yang RB, Chen KC (2014) Isolation and characterization of nineteen novel polymorphic microsatellite loci for the northern snakehead Channa argus. Conserv Genet Resour 6:621–623CrossRefGoogle Scholar
  59. Yang DY (1986) The evolution of the Poyang Lake in Quaternary. Oceanol Limnol Sin 17:429–435Google Scholar
  60. Yeh FC, Yang RC, Boyle T, Ye Z (2000) Popgene 1.32: Population Genetic Analysis. Molecular Biology and Biotechnology Centre, University of Alberta, CanadaGoogle Scholar
  61. Zhang B, Li ZJ, Tong JG, Liao XL (2006) Isolation and characterization of 18 polymorphic microsatellite markers in Chinese mandarin fish Siniperca chuatsi (Basilewsky). Conserv Genet Resour 6:1216–1218Google Scholar
  62. Zhou AG, Zhuo XL, Zou Q, Chen JT, Zou JX (2015) Population genetic diversity of the northern snakehead (Channa argus) in China based on the mitochondrial DNA control region and adjacent regions sequences. Mitochondr DNA 26:341–349CrossRefGoogle Scholar
  63. Zhuo XL, Liang RS, Chen YF, Huang GJ, Yu DH, Zou JX (2012) Genetic characterization of northern snakehead (Channa argus) populations in China using microsatellite markers. Biochem Syst Ecol 43:25–31CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, College of FisheriesHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.Pearl River Fisheries Research InstituteChinese Academy of Fishery SciencesGuangzhouPeople’s Republic of China
  3. 3.Yangtze River Fisheries Research InstituteChinese Academy of Fishery SciencesWuhanPeople’s Republic of China
  4. 4.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand

Personalised recommendations