Xianguang GUO,Li LIU and Yuezhao WANG.Phylogeography of the Phrynocephalus vlangalii Species Complex in the Upper Reaches of the Yellow River Inferred from mtDNA ND4-tRNALEU Segments[J].Asian Herpetological Research(AHR),2012,3(1):52-68.[doi:10.3724/SP.J.1245.2012.00052]
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Phylogeography of the Phrynocephalus vlangalii Species Complex in the Upper Reaches of the Yellow River Inferred from mtDNA ND4-tRNALEU Segments
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2012 VoI.3 No.1
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Phylogeography of the Phrynocephalus vlangalii Species Complex in the Upper Reaches of the Yellow River Inferred from mtDNA ND4-tRNALEU Segments
Xianguang GUO Li LIU and Yuezhao WANG*
Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, Sichuan, China
agamid diversification historical demography lineage mtDNA Pleistocene glaciations Tibetan Plateau
The Ching Hai Toad-headed Agama (Phrynocephalus vlangalii) complex is a small toad-headed viviparous lizard that is endemic to the Qinghai-Tibetan Plateau. A fragment of mtDNA ND4-tRNALEU from 189 samples in 26 populations was used to infer the phylogeographic history of this species complex in the upper reaches of the Yellow River. Phylogenetic analyses revealed that P. vlangalii and another proposed species (P. putjatia) do not form a monophyletic mtDNA clade, which in contrast with a previous study, includes P. theobaldi and P. forsythii. Lineage diversification occurred in the Middle Pleistocene for P. vlangali (ca. 0.95 Ma) and in the Early Pleistocene for P. putjatia (ca. 1.78 Ma). The uplift of the A’nyemaqen Mountains and glaciations since the mid-late Pleistocene, especially during the Kunlun Glaciation, are considered to have promoted the allopartric divergence of P. vlangalii. The diversification of P. putjatia may be triggered by the tectonic movement in the Huangshui River valley during the C phase of Qingzang Movement. Subsequently, the glacial climate throughout the Pleistocene may have continued to impede the gene flow of P. putjatia, eventually resulting in the genetic divergence of P. putjatia in the allopatric regions. Demographic estimates revealed weak population expansion in one lineage of P. vlangalii (A2, the Qaidam Basin lineage) and one lineage of P. putjatia (B2, the north Qinghai Lake lineage) after approximately 42 000 years before present. However, constant population size through time was inferred for two lineages (A1 and B1), the source of Yellow River lineage of P. vlangalii and the southeast of Qinghai Lake lineage of P. putjatia, possibly due to stable populations persisting in areas unaffected by glacial advances. Our results also suggest: 1) at least four differentiated lineages of P. vlangalii complex may have evolved allopatrically in different regions during the Pleistocene glaciation events; 2) in support of several recent studies, P. putjatia is a valid species, having a more wide distribution than previously considered; and 3) a hypothesis referring to P. v. hongyuanensis, inhabiting in the source region of the Yellow River, being synonymous with P. v. pylozwi is supported.


Ababneh F., Jermiin L. S., Ma C., Robinson J. 2006. Matched-pairs tests of homogeneity with applications to homologous nucleotide sequences. Bioinformatics, 22: 1225–1231
Akaike H. 1974. A new look at the statistical model identification. IEEE Trans Automat Contr, 19: 716–723
Aljanabi S. M., Martinez I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucl Acids Res, 25: 4692–4693
Arèvalo E., Davis S. K., Sites Jr J. W. 1994. Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst Biol, 43: 387–418
Avise J. C. 2000. Phylogeography: The History and Formation of Species. Cambridge: Harvard University Press, 447 pp
Barabanov A. V., Ananjeva N. B. 2007. Catalogue of the available scientific species-group names for lizards of the genus Phrynocephalus Kaup, 1825 (Reptilia, Sauria, Agamidae). Zootaxa, 1399: 1–56
Bedriaga J. V. 1909. Amphibian und reptilien. In Wissenschaftliche Resultate der von NM Prezewalski nach Central-Asien unternomenen Reisen (Zoologischer Theil) St. Petersburg: Band 3 Abt. 1 Annual Reports of the Zoological Museum of Emperor Acad Sci
Brandley M. C., Schmitz A., Reeder T. W. 2005. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol, 54: 373–390
Clement M., Posada D., Crandall K. A. 2000. TCS: A computer program to estimate gene genealogies. Mol Ecol, 9: 1657–1660
Cui Z., Wu Y., Liu G., Ge D., Pang Q., Xu Q. 1998. On Kunlun-Yellow River tectonic movement. Sci Chin Ser D Earth Sci, 41: 592–600
Degnan J. H., Rosenberg N. A. 2009. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol, 24: 332–340
Deng X., Liu S., Ding Y., Shen Y., Zhao L., Xie C. 2004. Quaternary glaciations and environment change in the A’nymaqen Mountains. J Glaciol Geocryol, 26: 305–311 (In Chinese with English abstract)
Drummond A. J., Rambaut A., Shapiro B., Pybus O. G. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol, 22: 1185–1192
Drummond A. J., Ho, S. Y. W., Pillips M. J., Ranbaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol, 4: e88
Drummond A. J., Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol, 7: 214
Engstrom T. N., Shaffer H. B., McCord W. P. 2004. Multiple data sets, high homoplasy, and the phylogeny of softshell turtles (Testudines: Trionychidae). Syst Biol, 53: 693–710
Excoffier L., Lischer H. E. L. 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
Fan Y., Wu R., Chen M.-H., Kuo L., Lewis P. O. 2011. Choosing among partition models in Bayesian phylogenetics. Mol Biol Evol, 28: 523–532
Felsenstein J. P. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39: 783–791
Fu Y. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147: 915–925
Gelman A., Rubin D. B. 1992. Inference from iterative simulation using multiple sequences. Stat Sci, 7: 457–511
Guo X., Wang Y. 2007. Partitioned Bayesian analyses, dispersal-vicariance analysis, and the biogeography of Chinese toad-headed lizards (Agamidae: Phrynocephalus): A re-evaluation. Mol Phylogenet Evol, 45: 643–662
Harpending H. 1994. Signature of ancient population growth in a low-resolution mitochondrial mismatch distribution. Human Biol, 66: 131–137
Hewitt G. M. 2001. Speciation, hybrid zones and phylogeography–or seeing genes in space and time. Mol Ecol, 10: 537–549
Ho J. W. K., Adams C. E., Lew J. B., Matthews T. J., Ng C. C., Shahabi-Sirjan A., Tan L. H., Zhao Y., Easteal S., Wilson S. R., Jermin L. S. 2006. SeqVis: Visualization of compositional heterogeneity in large alignments of nucleotides. Bioinformatics, 22: 2162–2163
Huelsenbeck J. P., Larget B., Miller R. E., Ronquist F. 2002. Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol, 51: 673–688
Jermiin L. S., Ho J. W. K., Lau K. W., Jayaswal V. 2009. SeqVis: A tool for detecting compositional heterogeneity among aligned nucleotide sequences. In Posada D. A. (Ed.), Bioinformatics for DNA Sequence Analysis. Totowa, NJ: Humana Press, 65–91
Jermiin L. S., Jayaswal V., Ababneh F., Robinson J. 2008. Phylogenetic model evaluation. In Keith J. (Ed), Methods in Molecular Biology: Bioinformatics, Vol. I, Data, Sequence Analysis and Evolution. Totowa, NJ: Humana Press, 331–364
Jiang F., Fu J., Wang S., Sun D., Zhao Z. 2007. Formation of the Yellow River, inferred from loess-palaeosol sequence in Mangshan and lacustrine sediments in Sanmen Gorge, China. Quatern Int, 175: 62–70
Jin Y. 2008. Evolutionary studies of Phrynocephalus (Agamidae) on Qinghai-Tibetan Plateau. Ph. D. Thesis. Lanzhou University, Lanzhou, 174 pp (In Chinese with English abstract)
Jin Y., Brown R. P., Liu N. 2008. Cladogenesis and phylogeography of the lizard Phrynocephalus vlangalii (Agamidae) on the Tibetan plateau. Mol Ecol, 17: 1971–1982
Kass R. E., Raftery A. E. 1995. Bayes factors. J Am Statist Assoc, 90: 773–795
Knowles L. L. 2009. Estimating species trees: Methods of phylogenetic analysis when there is incongruence across genes. Syst Biol, 58: 463–467
Knowles L. L., Kubatko L. S. 2010. Estimating Species Trees: Practical and Theoretical Aspects. New Jersey, USA: Wiley-Blackwell Press, 232 pp
Lewis P. O., Holder M. T., Swofford D. L. 2008. Phycas: Software for phylogenetic analysis. Storrs (CT): University of Connecticut. Available from http://www.phycas.org/
Li B., Li J., Cui Z., Zheng B., Zhang Q., Wang F., Zhou S., Shi Z., Jiao K., Kang J. 1991. Quaternary Glacial Distribution Map of Qinghai-Xizang (Tibet) Plateau. Beijing, China: Science Press (In Chinese)
Li J., Fang X., Ma H., Zhu J., Pan B., Chen H. 1996. Geomorphological and environmental evolution in the upper reaches of the Yellow River during the late Cenozoic. Sci Chin Ser D Earth Sci, 39: 380–390
Li R. 1993. The formation and evolution of Yellow River. In Yang J. (Ed.), Features and Evolution of Landforms in China. Beijing: China Ocean Press
Librado P., Rozas J. 2009. DnaSP v5: Software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25: 1451–1452
Liu Z., Sun Y. 2007. Uplift of the Qinghai-Tibet Plateau and formation, evolution of the Yellow River. Geogr Geo-Inform Sci, 23: 79–83 (In Chinese with English abstract)
Lu H., Wang X., An Z., Miao X., Zhu R., Ma H., Li Z., Tan H., Wang X. 2004. Geomorphologic evidence of phased uplift of the northeastern Qinghai-Tibet Plateau since 14 million years ago. Sci Chin Ser D Earth Sci, 47: 822–5833
Luikart G., Gielly L., Excoffier L., Vigne J. D., Bouvet J., Taberlet P. 2001. Multiple maternal origins and weak phylogeographic structure in domestic goats. Proc Natl Acad Sci USA, 98: 5927–5932
Macey J. R., Verma A. 1997. Homology in phylogenetic analysis: Alignment of transfer RNA genes and the phylogenetic position of snakes. Mol Phylogenet Evol, 7: 272–279
Maddison W. P. 1997. Gene trees in species trees. Syst Biol, 46: 523–536
Madsen D. B., Ma H., Rhodes D., Brantigham P. J. , Forman S. L. 2008. Age constraints on the late Quaternary evolution of Qinghai Lake, Tibetan Plateau. Quat Res, 69: 316–325
Muelle R. L. 2006. Evolutionary rates, divergence dates, and the performance of mitochondrial genes in Bayesian phylogenetic analysis. Syst Biol, 55: 289–300
Noble D., Qi Y., Fu. J. 2010. Species delineation using Bayesian model-based assignment tests: A case study using Chinese toad-headed agamas (genus Phrynocephalus). BMC Evol Biol, 10: 197
Nylander J. A. A. 2008. MrModeltest 2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
Owen L. A., Caffee M. W., Bovard K. R., Finkel R. C., Sharma M. C. 2006. Terrestrial cosmogenic nuclide surface exposure dating of the oldest glacial successions in the Himalayan orogen: Ladakh range, northern India. Geol Soc Am Bull, 118: 383–392
Pan B. 1994. Research upon the geomorphologic evolution of the Guide Basin and the development of the Yellow River. Arid Land Geog, 7: 43–50 (In Chinese with English abstract)
Pang J., Wang Y., Zhong Y., Hoelzel A. R., Papenfuss T. J., Zeng X., Ananjeva N. B., Zhang Y. 2003. A phylogeny of Chinese species in the genus Phrynocephalus (Agamidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol, 27: 398–409
Posada D., Crandal K. A. 2001. Intraspecific gene genealogies: Trees grafting into networks. Trends Ecol Evol, 16: 37–45
Qu Y., Lei F., Zhang R., Lu X. 2010. Comparative phylogeography of five avian species: Implications for Pleistocene evolutionary history in the Qinghai-Tibetan plateau. Mol Ecol, 19: 338–351
Raftery A. E. 1996. Hypothesis testing and model selection. In Gilks W. R., Spiegelhalter D. J., Richardson S. (Eds.), Markov Chain Monte Carlo in Practice. London, UK: Chapman and Hall, 163–188
Rambaut A., Drummond A. J. 2009. Tracer v. 1.5. Available from http://beast.bio.ed.ac.uk/Tracer
Ramos-Onsins R., Rozas R. 2002. Statistical properties of new neutrality tests against population growth. Mol Biol Evol, 19: 2092–2100
Rogers A. R., Harpending H. C. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol, 9: 552–569
Ronquist F., Huelsenbeck J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572–1574
Shi Y., Li J., Li B. 1998. Uplift and Environmental Changes of Qinghai-Tibetan Plateau in the Late Cenozoic. Guangzhou: Guangdong Science and Technology Press, 463 pp (In Chinese)
Shi Y., Zhao J., Wang J. 2011. New Understanding of Quaternary Glaciations in China. Shanghai: Shanghai Popular Science Press, 213 pp (In Chinese)
Swofford D. L. 2003. PAUP*. Phylogenetic analysis using parsimony (* and other methods), Version 4. Sunderland, MA: Sinauer
Tamura K., Dudley J., Nei M., Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol, 24: 1596–1599
Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res, 25: 4876–4882
Wang Y., Zeng X., Fang Z., Wu G., Liu Z., Papenfuss T. J., Macey J. R. 2002. A valid species of the genus Phrynocephalus: P. putjatia and a discussion on taxonomy of Phrynocephalus hongyuanensis (Sauria: Agamidae). Acta Zootaxon Sin, 27: 372–383
Wang Y., Zhan A., Fu J. 2009. Testing historical phylogeographic inferences with contemporary gene flow data: Population genetic structure of the Qinghai toad-headed lizard. J Zool, 278: 149–156
Xie W., Lewis P. O., Fan Y., Kuo L., Chen M. H. 2011. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol, 60: 150–160
Xu T., Abbott R. J., Milne R. I., Mao K., Du F. K., Wu G., Ciren Z., Miehe G., Liu J. 2010. Phylogeography and allopatric divergence of cypress species (Cupressus L.) in the Qinghai-Tibetan Plateau and adjacent regions. BMC Evol Biol, 10: 194
Yang S., Dong H., Lei F. 2009. Phylogeogrpahy of regional fauna on the Tibetan Plateau: A review. Prog Nat Sci, 19: 789–799
Yuan B., Chen K., Ye S. 1990. Origin and evolution of Lake Qinghai. Quatern Sci, 3: 233–243 (In Chinese with English abstract)
Zardoya R., Meyer A. 1996. Phylogenetic performance of mitochondrial protein-coding genes in resolving relationships among vertebrates. Mol Biol Evol, 13: 966–942
Zerova G. A., Chkhikvadze V. M. 1984. The review of Cenozoic lizards and snakes of the USSR. Review of Cenozoic lizards and snakes in USSR. Proc Acad Sci Georgian SSR. Series: Biology, 10: 319–325 (In Russian)
Zhan X., Zheng Y., Wei F., Bruford M. W., Jia C. 2011. Molecular evidence for Pleistocene refugia at the eastern edge of the Tibetan Plateau. Mol Ecol, 20: 3014–3026
Zhang Z., Wang S., Yang X., Jiang F., Shen J., Li X. 2004. Evidence of a geological event and environmental change in the catchment area of the Yellow River at 0.15 Ma. Quatern Int, 117: 3–40
Zhao J., Shi Y., Wang J. 2011. Comparison between Quaternary Glaciations in China and the marine oxygen isotope stage (MIS): An improved schema. Acta Geogr Sin, 66: 867–884 (In Chinese with English abstract)
Zhao K. 1997. Notes on the Chinese toad-headed agamids and its diagnostic characters. J Suzhou Railway Teachers Coll, 14: 27–32
Zhao K. 1999. Phrynocephalus Kaup, 1825. In Zhao E., Zhao K., Zhou K. (Eds.), Fauna Sinica Reptilia, Vol. 2. Beijing: Science Press, 153–193 (In Chinese)
Zheng B., Rutter N. 1998. On the problem of Quaternary glaciations, and the extent and patterns of Pleistocene ice cover in the Qinghai-Xizang (Tibet) Plateau. Quatern Int, 45/46: 109–122
Zheng B., Wang S. 1996. A study on the Paleo-glaciation and paleoenvironment in the source area of the Yellow River. J Glaciol Geocryol, 18: 210–218 (In Chinese with English abstract)
Zheng B., Xu Q., Shen Y. 2002. The relationship between climate change and Quaternary glacial cycles on the Qinghai-Tibetan Plateau: Review and speculation. Quatern Int, 97/98: 93–101
Zhou S., Li J., Zhao J., Wang J., Zheng J. 2011.Quaternary Glaciations: Extent and Chronology in China. In Ehlers J., Gibbard P. L., Hughes P. D. (Eds), Developments in Quaternary Science, Vol. 15, Amsterdam, The Netherlands: Elsevier Press, 981–1002


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