Environmental Biology of Fishes

, Volume 93, Issue 4, pp 519–530 | Cite as

High intra-population genetic variability and inter-population differentiation in a plateau specialized fish, Triplophysa orientalis

  • Feixia Hou
  • Xiuyue Zhang
  • Xuefei Zhang
  • Bisong Yue
  • Zhaobin SongEmail author


Triplophysa orientalis (Herzenstein) is one of the Nemacheilinae (Cypriniformes: Balitoridae) fish species distributed in the Tibetan Plateau area. In order to understand the impact of plateau uplift on population history and the isolation effect of plateau lakes on T. orientalis, we examined its genetic structure and phylogenetic relationships. A total of 98 individuals from five wild populations, three from plateau lakes and two from branch rivers in upper reaches of the Yangtze River, in the eastern peripheral of the Tibetan Plateau were sampled. An 848 base pair fragment from the mitochondrial DNA (mtDNA) control region was sequenced for analyses. Overall, very high intra-population genetic variability was found in all populations except for one lake population (Rannicuo); nucleotide diversity ranged from 0.0025 to 0.0159 and haplotype diversity ranged from 0.641 to 0.879. Furthermore, the genetic distance between river populations (0.0326) was much higher than that among lake populations (Rannicuo and Barencuo 0.0035, Bannicuo and Yibicuo 0.0038, Rannicuo and Yibicuo 0.0049). Additionally, the analysis of molecular variance demonstrated that most of the observed genetic variability occurred among populations, accompanied with significant Fst values except for that between the Yibicuo and Barencuo populations. This evidence suggested a strong population structure of the species and a lack of inter-population connection. Lastly, the rate of migration indicated there were large historic gene flows among lake populations. Demographic analysis also indicated there were bottlenecks or expansions in three lake populations, suggesting a potential isolation effect of plateau lakes on population differentiation. Molecular dating of intra-specific divergence showed the plateau uplift has shaped the genetic structure of T. orientalis.


Genetic variability Population structure and differentiation Isolation effect Mitochondrial DNA control region Triplophysa orientalis Tibetan Plateau 



This work was supported by the National Natural Science Foundation of China (No. 30670290), Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry (No. 2008890-19-13), and Sichuan Youth Science and Technology Foundation (No. 08ZQ026-019). We would like to thank Chunlin He for his help in sample collection. We are grateful for Emily H. King, Jinzhong Fu and Cameron Hudson for their help in English corrections, three anonymous reviewers and David. L. G. Noakes for their comments on the manuscript.


  1. Aboim MA, Menezes GM, Schlitt T, Rogers AD (2005) Genetic structure and history of populations of the deep-sea fish Helicolenus dactylopterus (Delaroche, 1809) inferred from mtDNA sequence analysis. Mol Ecol 14:1343–1354PubMedCrossRefGoogle Scholar
  2. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723CrossRefGoogle Scholar
  3. An ZS, Kutzbach JE, Prell WL, Porter SC (2001) Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan Plateau since Late Miocene times. Nature 411:62–66CrossRefGoogle Scholar
  4. Arbogast BS, Kenagy GJ (2001) Comparative phylogeography as an integrative approach to historical biogeography. J Biogeogr 28:819–825CrossRefGoogle Scholar
  5. Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol 13:494–504PubMedGoogle Scholar
  6. Aurelle D, Berrebi P (2001) Genetic structure of brown trout (Salmo trutta, L.) populations from south-western France: data from mitochondrial control region variability. Mol Ecol 10:1551–1561PubMedCrossRefGoogle Scholar
  7. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  8. Beerli P (2008) Migrate version 3.0 − a maximum likelihood and Bayesian estimator of gene flow using the coalescent. Distributed over the internet at
  9. Beerli P, Felsentein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773PubMedGoogle Scholar
  10. Bowen BW, Grant WS (1997) Phylogeography of the sardines (Sardinops spp.): assessing biogeographic models and population histories in temperate upwelling zones. Evolution 51:1601–1610CrossRefGoogle Scholar
  11. Brown GG, Gadaleta G, Pepe G, Saccone C, Sbisà E (1986) Structural conservation and variation in the D-loop-containing region of vertebrate mitochondrial DNA. J Mol Biol 192:503–511PubMedCrossRefGoogle Scholar
  12. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  13. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  14. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  15. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  16. Fu YX, Li WH (1993) Maximum likelihood estimation of population parameters. Genetics 134:1261–1270PubMedGoogle Scholar
  17. Grant WAS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426CrossRefGoogle Scholar
  18. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  19. Harrison TM, Copeland P, Kidd WSF, Yin A (1992) Raising Tibet. Science 255:1663–1670PubMedCrossRefGoogle Scholar
  20. He CL (2008) Taxonomic revision of Triplophysa species in Sichuan Province, MS Dissertation. Sichuan University, ChinaGoogle Scholar
  21. He DK, Chen YF (2006) Biogeography and molecular phylogeny of the genus Schizothorax (Teleostei: Cyprinidae) in China inferred from cytochrome b sequences. J Biogeogr 33:1448–1460CrossRefGoogle Scholar
  22. He DK, Chen YF (2007) Molecular phylogeny and biogeography of the highly specialized grade schizothoracine fishes (Teleostei: Cyprinidae) inferred from cytochrome b sequences. Chin Sci Bull 52:777–788CrossRefGoogle Scholar
  23. He SP, Cao WX, Chen YY (2001) The uplift of Qinghai-Xizang (Tibet) Plateau and the vicariance speciation of glyptosternoid fishes (Siluriformes: Sisoridae). Sci China Ser C 44:644–651CrossRefGoogle Scholar
  24. He DK, Chen YF, Chen YY, Chen ZM (2004) Molecular phylogeny of the specialized schizothoracine fishes (Teleostei: Cyprinidae), with their implications for the uplift of the Qinghai-Tibetan Plateau. Chin Sci Bull 49:39–48Google Scholar
  25. He DK, Chen YX, Chen YF (2006) Molecular phylogeny and biogeography of the genus Triplophysa (Osteichthyes: Nemacheilinae) in the Tibetan Plateau inferred from cytochrome b DNA sequences. Prog Nat Sci 16:1395–1404Google Scholar
  26. Herzenstein SM (1888) Fische. In: Wissenschaftliche Resultate der von N. M. Przewalski nach Central-Asien unternommenen Reisen. Zool Theil 3(2):1−90Google Scholar
  27. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  28. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589PubMedGoogle Scholar
  29. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  30. Liu HZ, Tzeng CS, Teng HY (2002a) Sequence variations in the mitochondrial DNA control region and their implications for the phylogeny of the Cypriniformes. Can J Zool 80:569–581CrossRefGoogle Scholar
  31. Liu JQ, Gao TG, Chen ZD, Lu AM (2002b) Molecular phylogeny and biogeography of the Qinghai-Tibet Plateau endemic Nannoglottis (Asteraceae). Mol Phylogenet Evol 23:307–325PubMedCrossRefGoogle Scholar
  32. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  33. Pang JF, Wang YZ, Zhong Y, Hoelzel AR, Papenfuss TJ, Zeng XM, Ananjeva NB, Zhang YP (2003) A phylogeny of Chinese species in the genus Phrynocephalus (Agamidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 27:398–409PubMedCrossRefGoogle Scholar
  34. Peng ZG, Ho SYW, Zhang YG, He SP (2006) Uplift of the Tibetan Plateau: Evidence from divergence times of glyptosternoid catfishes. Mol Phylogenet Evol 39:568–572PubMedCrossRefGoogle Scholar
  35. Posada D (2008) jModelTest: Phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  36. Qi DL, Guo SC, Zhao XQ, Yang J, Tang WJ (2007) Genetic diversity and historical population structure of Schizopygopsis pylzovi (Teleostei: Cyprinidae) in the Qinghai–Tibetan Plateau. Freshw Biol 52:1090–1104CrossRefGoogle Scholar
  37. Qu YH, Ericson PGP, Lei FM, Li SH (2005) Postglacial colonization of the Tibetan Plateau inferred from the matrilineal genetic structure of the endemic red-necked snow finch, Pyrgilauda ruficollis. Mol Ecol 14:1767–1781PubMedCrossRefGoogle Scholar
  38. Qu JY, Liu NF, Bao XK, Wang XL (2009) Phylogeography of the ring-necked pheasant (Phasianus colchicus) in China. Mol Phylogenet Evol 52:125–132PubMedCrossRefGoogle Scholar
  39. Rambaut A, Drummond AJ (2007) Tracer v 1.4
  40. Recuero E, Martínez SÍ, Parra OG, García PM (2006) Phylogeography of Pseudacris regilla (Anura: Hylidae) in western North America, with a proposal for a new taxonomic rearrangement. Mol Phylogenet Evol 39:293–304PubMedCrossRefGoogle Scholar
  41. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  42. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioniformatics 19:1572–1574CrossRefGoogle Scholar
  43. Rozas J, Sánchez DJC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  44. Saccone C, Attimonelli M, Sbisà E (1987) Structural elements highly preserved during the evolution of the D-loop-containing region in vertebrate mitochondrial DNA. J Mol Biol 26:205–211Google Scholar
  45. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Press, Cold Spring HarborGoogle Scholar
  46. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedGoogle Scholar
  47. Shi YF, Li JJ, Li BY (1998) Uplift and environmental changes of Qinghai-Xizang (Tibetan) Plateau in the Late Cenozoic. Guangdong Science and Technology Press, GuangzhouGoogle Scholar
  48. Song ZB, Song J, Yue BS (2008) Population genetic diversity of Prenant’s schizothoracin, Schizothorax prenanti, inferred from the mitochondrial DNA control region. Environ Biol Fish 81:247–252CrossRefGoogle Scholar
  49. Stepien CA (1995) Population genetic divergence and geographic patterns from DNA sequences: Examples from marine and freshwater fishes. Am Fish Soc Symp 17:263–287Google Scholar
  50. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  51. Tang QY, Liu HZ, Mayden R, Xiong BX (2006) Comparison of evolutionary rates in the mitochondrial DNA cytochrome b gene and control region and their implications for phylogeny of the Cobitoidea (Teleostei: Cypriniformes). Mol Phylogenet Evol 39:347–357PubMedCrossRefGoogle Scholar
  52. Wu YF, Wu CZ (1992) The fishes of the Qinghai-Xizang Plateau. Sichuan Publishing House of Science and Technology, ChengduGoogle Scholar
  53. Yang SJ, Lei FM, Qu YH, Yin ZH (2006a) Intraspecific phylogeography of the white-rumped snowfinch (Onychostruthus taczanowskii) endemic to the Tibetan Plateau based on mtDNA sequences. J Zool 268:187–192CrossRefGoogle Scholar
  54. Yang SJ, Yin ZH, Ma XM, Lei FM (2006b) Phylogeography of ground tit (Pseudopodoces humilis) based on mtDNA: Evidence of past fragmentation on the Tibetan Plateau. Mol Phylogenet Evol 41:257–265PubMedCrossRefGoogle Scholar
  55. Yang SJ, Dong HL, Lei FM (2009) Phylogeography of regional fauna on the Tibetan Plateau: A review. Prog Nat Sci 19:789–799CrossRefGoogle Scholar
  56. Yu N, Zheng CL, Zhang YP, Li WH (2000) Molecular systematics of pikas (Genus Ochotona) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 16:85–95PubMedCrossRefGoogle Scholar
  57. Zhang JB, Cai ZP, Huang LM (2006) Population genetic structure of crimson snapper Lutjanus erythropterus in East Asia, revealed by analysis of the mitochondrial control region. ICES J Mar Sci 63:693–704CrossRefGoogle Scholar
  58. Zhu SQ (1989) The loaches of the subfamily Nemacheilinae in China (Cypriniformes: Cobitidae). Jiangsu Science and Technology Publishing House, NanjingGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Feixia Hou
    • 1
  • Xiuyue Zhang
    • 1
  • Xuefei Zhang
    • 1
  • Bisong Yue
    • 1
  • Zhaobin Song
    • 1
    Email author
  1. 1.Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life SciencesSichuan UniversityChengduPeople’s Republic of China

Personalised recommendations