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Cyprininae phylogeny revealed independent origins of the Tibetan Plateau endemic polyploid cyprinids and their diversifications related to the Neogene uplift of the plateau

Science China Life Sciences volume 59, pages 1149–1165 (2016)Cite this article

Abstract

Origin and diversification of the Tibetan polyploid cyprinids (schizothoracins) may help us to explore relationships between diversification of the cyprinids and the Tibetan Plateau uplift. Cyprininae phylogeny was analyzed using mitochondrial and nuclear DNA sequences to trace origins of polyploidy and diversifications of schizothoracins. Ancestral states reconstruction for ploidy levels indicated that the Cyprininae was diploid origin and the schizothoracin clades tetraploid origins. There were two diversification rate shifts along with diversification of the cyprinine fishes in response to the Tibetan uplift. The unusual diversification shifts were located to branches subtending the clades of Tibetan polyploid cyprinids. Our analyses suggested that (i) phylogeny of Cyprininae recovered two independent origins of the Tibetan polyploidy schizothoracins; (ii) diversifications of the schizothoracins were closely related to the Neogene uplift of the Tibetan plateau in the following ways: the relatively ancient Late Oligocene-Middle Miocene adaptive radiation may be associated with the uplift of the southern Tibet and Himalaya; the Middle Miocene-Early Pleistocene lineage-specific diversification broadly coincident with major phase of the Neogene Tibetan uplift; and the most recent Pleistocene diversification shift in Schizothorax closely coincident with the successive Kunlun-Huanghe and Gonghe movements of the Tibetan uplift and the glaciation-induced climate oscillations on the plateau.

References

  • An, Z., Kutzbach, J.E., Prell, W.L., and Porter, S.C. (2001). Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature 411, 62–6.

    CAS  Article  Google Scholar 

  • Arai, R. (2011). Fish Karyotypes: A Check List. (Tokyo: Springer).

    Book  Google Scholar 

  • Becak, W., Becak, M.L., and Ohno, S. (1966). Intraindividual chromosomal polymorphism in green sunfish (Lepomis cyanellus) as evidence of somatic segregation. Cytogenetics 5, 313–18.

    CAS  Article  PubMed  Google Scholar 

  • Brysting, A.K., Oxelman, B., Huber, K.T., Moulton, V., and Brochmann, C. (2007). Untangling complex histories of genome mergings in high polyploids. Syst Biol 56, 467–76.

    CAS  Article  PubMed  Google Scholar 

  • Buth, D.G., Dowling, T.E., and Gold, J.R. (1991). Molecular and cytological investigations. In Cyprinid Fishes: Systematics, Biology and Exploitation, I.J. Winfield, and J.S. Nelson, eds. (London: Chapman and Hall), pp. 83–26.

  • Cao, W.X., Chen, Y.Y., Wu, Y.F., and Zhu, S.Q. (1981). Origin and evolution of schizothoracine fishes in relation to the upheaval of the Xizang Plateau. In Collection in Studies on the Period, Amplitude and Type of the Uplift of the Qinghai-Xizang Plateau, C.A.o.S (in Chinese). The Team of the Comprehensive Scientific Expedition to the Qinghai-Xizang Plateau, ed. (Beijing: Science Press), pp. 118–30.

    Google Scholar 

  • Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G., Quade, J., Eisenmann, V., and Ehleringer, J.R. (1997). Global vegetation change through the Miocene/Pliocene boundary. Nature 389, 153–58.

    CAS  Article  Google Scholar 

  • Chan, K.M., and Moore, B.R. (2002). Whole-tree methods for detecting differential diversification rates. Syst Biol 51, 855–65.

    Article  PubMed  Google Scholar 

  • Chan, K.M., and Moore, B.R. (2005). SYMMETREE: whole-tree analysis of differential diversification rates. Bioinformatics 21, 1709–710.

    CAS  Article  PubMed  Google Scholar 

  • Chen, W., Du, K., and He, S. (2015). Genetic structure and historical demography of Schizothorax nukiangensis (Cyprinidae) in continuous habitat. Ecol Evol 5, 984–95.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, X.L., Yue, P.Q., and Lin, R.D. (1984). Major groups within the family Cyprinidae and their phylogenetic relationships. Acta Zootaxon Sin 9, 424–40.

    Google Scholar 

  • Chen, Y.Y. (1998). Fauna Sinica, Osteichthys: Cypriniformes (Part II) (Beijing: Science Press).

    Google Scholar 

  • Coleman, M., and Hodges, K. (1995). Evidence for Tibetan Plateau uplift before 14-Myr ago from a new minimum age for east-west extension. Nature 374, 49–2.

    CAS  Article  Google Scholar 

  • Copeland, P., Harrison, T.M., Kidd, W.S.F., Xu, R.H., and Zhang, Y.Q. (1987). Rapid early Miocene acceleration of uplift in the Gangdese Belt, Xizang (southern Tibet), and its bearing on accommodation mechanisms of the India-Asia collision. Earth Planet Sci Lett 86, 240–52.

    CAS  Article  Google Scholar 

  • De Rijk, P., Wuyts, J., Van de Peer, Y., Winkelmans, T., and De Wachter, R. (2000). The European large subunit ribosomal RNA database. Nucleic Acids Res 28, 177–78.

    Article  PubMed  PubMed Central  Google Scholar 

  • Don, J., and Avtalion, R.R. (1988). Production of viable tetraploid tilapias using the cold shock technique. Isr J Aquacult-Bamid 40, 17–1.

    Google Scholar 

  • Eriksson, T. (2001). AutoDecay ver. 5.0 (program distributed by the author) (Stockholm, Bergius Foundation, Royal Swedish Academy of Sciences).

  • Evans, B.J., Kelley, D.B., Melnick, D.J., and Cannatella, D.C. (2005). Evolution of RAG-1 in polyploid clawed frogs. Mol Biol Evol 22, 1193–207.

    CAS  Article  PubMed  Google Scholar 

  • Evans, B.J., Kelley, D.B., Tinsley, R.C., Melnick, D.J., and Cannatella, D.C. (2004). A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol Phylogenet Evol 33, 197–13.

    CAS  Article  PubMed  Google Scholar 

  • Fan, M., Dettman, D.L., Song, C., Fang, X., and Garzione, C.N. (2007). Climatic variation in the Linxia basin, NE Tibetan Plateau, from 13.1 to 4.3 Ma: the stable isotope record. Palaeogeography, Palaeoclimatology, Palaeoecology 247, 313–28.

    Article  Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–91.

    Article  Google Scholar 

  • Felsenstein, J. (1993). PHYLIP (Phylogeny Inference Package) version 3.5 c (Department of Genetics, University of Washington, Seattle).

  • Fortune, P.M., Schierenbeck, K.A., Ainouche, A.K., Jacquemin, J., Wendel, J.F., and Ainouche, M.L. (2007). Evolutionary dynamics of Waxy and the origin of hexaploid Spartina species (Poaceae). Mol Phylogenet Evol 43, 1040–055.

    CAS  Article  PubMed  Google Scholar 

  • Guo, X., He, S., and Zhang, Y. (2005). Phylogeny and biogeography of Chinese sisorid catfishes re-examined using mitochondrial cytochrome b and 16S rRNA gene sequences. Mol Phylogenet Evol 35, 344–62.

    CAS  Article  PubMed  Google Scholar 

  • Guo, X., and 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, 643–62.

    CAS  Article  PubMed  Google Scholar 

  • Guo, Z.T., Ruddiman, W.F., Hao, Q.Z., Wu, H.B., Qiao, Y.S., Zhu, R.X., Peng, S.Z., Wei, J.J., Yuan, B.Y., and Liu, T.S. (2002). Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature 416, 159–63.

    CAS  Article  PubMed  Google Scholar 

  • Gutell, R.R., and Fox, G.E. (1988). A compilation of large subunit RNA sequences presented in a structural format. Nucleic Acids Res 16 Suppl, r175–69.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Gutell, R.R., Gray, M.W., and Schnare, M.N. (1993). A compilation of large subunit (23S and 23S-like) ribosomal RNA structures. Nucleic Acids Res 21, 3055–074.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Harris, N. (2006). The elevation history of the Tibetan Plateau and its implications for the Asian monsoon. Palaeogeography Palaeoclimatology Palaeoecology 241, 4–5.

    Article  Google Scholar 

  • Harrison, T.M., Copeland, P., Kidd, W.S.F., and Yin, A.N. (1992). Raising Tibet. Science 255, 1663–670.

    CAS  Article  PubMed  Google Scholar 

  • Howes, G.J. (1991). Systematics and biogeography: an overview. In Cyprinid Fishes: Systematics, Biology and Exploitation, I.J. Winfield, and J.S. Nelson, eds. (London: Chapman and Hall), pp. 1–3.

  • Leggatt, R.A., and Iwama, G.K. (2003). Occurrence of polyploidy in the fishes. Rev Fish Biol Fish 13, 237–46.

    Article  Google Scholar 

  • Li, G.G., Peng, Z.G., Zhang, R.Y., Tang, Y.T., Tong, C., Feng, C.G., Zhang, C.F., and Zhao, K. (2016). Mito-nuclear phylogeography of the cyprinid fish Gymnodiptychus dybowskii in the arid Tien Shan region of Central Asia. Biol J Linn Soc 118, 304–14.

    Article  Google Scholar 

  • Li, J., Wang, X., Kong, X., Zhao, K., He, S., and Mayden, R.L. (2008). Variation patterns of the mitochondrial 16S rRNA gene with secondary structure constraints and their application to phylogeny of cyprinine fishes (Teleostei: Cypriniformes). Mol Phylogenet Evol 47, 472–87.

    CAS  Article  PubMed  Google Scholar 

  • Li, J.J., and Fang, X.M. (1999). Uplift of the Tibetan Plateau and environmental changes. Chin Sci Bull 44, 2117–124.

    Article  Google Scholar 

  • Li, T. (1996). The process and mechanism of the rise of the Qinghai-Tibet Plateau. Tectonophysics 260, 45–3.

    Article  Google Scholar 

  • Liu, J.Q. (2004). Uniformity of karyotypes in Ligularia (Asteraceae: Senecioneae), a highly diversified genus of the eastern Qinghai-Tibet Plateau highlands and adjacent areas. Bot J Linn Soc 144, 329–42.

    Article  Google Scholar 

  • Liu, J.Q., Wang, Y.J., Wang, A.L., Hideaki, O., and Abbott, R.J. (2006). Radiation and diversification within the Ligularia-Cremanthodium-Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Mol Phylogenet Evol 38, 31–9.

    CAS  Article  PubMed  Google Scholar 

  • Lu, H.Y., Wang, X.Y., An, Z.S., Miao, X.D., Zhu, R.X., Ma, H.Z., Li, Z., Tan, H.B., and Wang, X.Y. (2004). Geomorphologic evidence of phased uplift of the northeastern Qinghai-Tibet Plateau since 14 million years ago. Sci China Ser D 47, 822–33.

    Article  Google Scholar 

  • Luo, J., Yang, D., Suzuki, H., Wang, Y., Chen, W.J., Campbell, K.L., and Zhang, Y.P. (2004). Molecular phylogeny and biogeography of Oriental voles: genus Eothenomys (Muridae, Mammalia). Mol Phylogenet Evol 33, 349–62.

    CAS  Article  PubMed  Google Scholar 

  • Ma, Y.Z., Li, J.J., and Fang, X.M. (1998). Pollen assemblage in 30.6–.0 Ma redbeds of Linxia region and climate evolution. Chin Sci Bull 43, 301–04.

    Google Scholar 

  • Machordom, A., and Doadrio, I. (2001). Evolutionary history and speciation modes in the cyprinid genus Barbus. P Roy Soc B-Biol Sci 268, 1297–306.

    CAS  Article  Google Scholar 

  • Maddison, D.R., and Maddison, W.P. (2000). MacClade 4 (Sunderland, Massachusetts, Sinauer Associates).

  • Maddison, W.P., and Maddison, D.R. (2015). Mesquite: a modular system for evolutionary analysis (http://mesquiteproject.org).

  • Marhold, K., and Lihová, J. (2006). Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Syst Evol 259, 143–74.

    Article  Google Scholar 

  • Molnar, P. (2005). Mio-pliocene growth of the Tibetan Plateau and evolution of East Asian climate. Palaeontol Electron 8, 131–42.

    Google Scholar 

  • Molnar, P., England, P., and Martinod, J. (1993). Mantle dynamics, uplift of the Tibetan Plateau, and the Indian monsoon. Rev Geophys 31, 357–96.

    Article  Google Scholar 

  • Moore, B.R., Chan, K.M.A., and Donoghue, M.J. (2004). Detecting diversification rate variation in supertrees. In Phylogenetic supertrees: combining Information to reveal the tree of life, O.R.P. Bininda-Emonds, ed. (Dordrecht: Kluwer Academic), pp. 487–33.

  • Nee, S., Mooers, A.O., and Harvey, P.H. (1992). Tempo and mode of evolution revealed from molecular phylogenies. Proc Natl Acad Sci USA 89, 8322–326.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Nelson, J.S. (2006). Fishes of the world, 4th ed. (New York: John Wiley and Sons Inc.).

    Google Scholar 

  • Nie, Z.L., Wen, J., Gu, Z.J., Boufford, D.E., and Sun, H. (2005). Polyploidy in the flora of the Hengduan Mountains hotspot, southwestern China. Ann Mo Bot Gard 92, 275–06.

    Google Scholar 

  • Oellermann, L.K., and Skelton, P.H. (1990). Hexaploidy in yellowfish species (Barbus, Pisces, Cyprinidae) from southern Africa. J Fish Biol 37, 105–15.

    Article  Google Scholar 

  • Otero, O. (2001). The oldest-known cyprinid fish of the Afro-Arabic Plate, and its paleobiogeographical implications. J Vertebr Paleontol 21, 386–88.

    Article  Google Scholar 

  • Posada, D., and Crandall, K.A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–18.

    CAS  Article  PubMed  Google Scholar 

  • Rabosky, D.L. (2006a). LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evol Bioinform Online 2, 273–76.

    Google Scholar 

  • Rabosky, D.L. (2006b). Likelihood methods for detecting temporal shifts in diversification rates. Evolution 60, 1152–164.

    Article  PubMed  Google Scholar 

  • Rainboth, W.J. (1991). Cyprinid fishes of Southeast Asia. In Cyprinid Fishes: Systematics, biology and exploitation, I.J. Winfield, and J.S. Nelson, eds. (London: Chapman and Hall), pp. 156–10.

  • Ritts, B.D., Yue, Y., Graham, S.A., Sobel, E.R., Abbink, O.A., and Stockli, D. (2008). From sea level to high elevation in 15 million years: uplift history of the northern Tibetan Plateau margin in the Altun Shan. Am J Sci 308, 657–78.

    Article  Google Scholar 

  • Ronquist, F., and Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–574.

    CAS  Article  PubMed  Google Scholar 

  • Rousseau-Gueutin, M., Gaston, A., Ainouche, A., Ainouche, M.L., Olbricht, K., Staudt, G., Richard, L., and Denoyes-Rothan, B. (2009). Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes. Mol Phylogenet Evol 51, 515–30.

    CAS  Article  PubMed  Google Scholar 

  • Royden, L.H., Burchfiel, B.C., and van der Hilst, R.D. (2008). The geological evolution of the Tibetan Plateau. Science 321, 1054–058.

    CAS  Article  PubMed  Google Scholar 

  • Sambrook, J., Fritsch, E., and Maniatis, T. (1989). Molecular cloning: a laboratory manual, Vol 2, 2nd edition edn. (New York: Cold Spring Harbor Laboratory Press).

    Google Scholar 

  • Sanderson, M.J. (1997). A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14, 1218–231.

    CAS  Article  Google Scholar 

  • Sanderson, M.J. (2002). Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 19, 101–09.

    CAS  Article  PubMed  Google Scholar 

  • Sanderson, M.J. (2003). r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–02.

    CAS  Article  PubMed  Google Scholar 

  • Sang, T. (2002). Utility of low-copy nuclear gene sequences in plant phylogenetics. Crit Rev Biochem Mol 37, 121–47.

    CAS  Article  Google Scholar 

  • Schultz, R.J. (1980). Role of polyploidy in the evolution of fishes. In Polyploidy: Biological Relevance, W.H. Lewis, ed. (Boston: Springer US), pp. 313–40.

  • Shi, Y., Li, J., Li, B., Yao, T., Wang, S., Li, S., Cui, Z., Wang, F., Pan, B., Fang, X., and Zhang, Q. (1999). Uplift of the Qinghai-Xizang (Tibetan) Plateau and East Asia environmental change during late Cenozoic. Acta Geograph Sin 54, 10–1.

    Google Scholar 

  • Skelton, P.H., Tweddle, D., and Jackson, P.B.N. (1991). Cyprinids of Africa. In Cyprinid Fishes: Systematics, Biology and Exploitation, I.J. Winfield, and J.S. Nelson, eds. (London: Chapman and Hall), pp. 211–39.

  • Slowinski, J.B., and Guyer, C. (1993). Testing whether certain traits have caused amplified diversification: an improved method based on a model of random speciation and extinction. Am Nat 142, 1019–024.

    CAS  Article  PubMed  Google Scholar 

  • Spicer, R.A., Harris, N.B.W., Widdowson, M., Herman, A.B., Guo, S., Valdes, P.J., Wolfe, J.A., and Kelley, S.P. (2003). Constant elevation of southern Tibet over the past 15 million years. Nature 421, 622–24.

    CAS  Article  PubMed  Google Scholar 

  • Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–690.

    CAS  Article  PubMed  Google Scholar 

  • Stewart, K.M. (2001). The freshwater fish of Neogene Africa (Miocene-Pleistocene): systematics and biogeography. Fish Fish 2, 177–30.

    Article  Google Scholar 

  • Stewart, K.M. (2009). Fossil fish from the Nile River and its southern basins. Monograph Biol 89, 677–04.

    Article  Google Scholar 

  • Tang, H., Meng, L., Shiqimg, A., and Jianquaan, L. (2005). Origin of the Qinghai-Tibetan Plateau endemic Milula (Liliaceae): further insights from karyological comparisons with Allium. Caryologia 58, 320–31.

    Article  Google Scholar 

  • Tapponnier, P., Zhiqin, X., Roger, F., Meyer, B., Arnaud, N., Wittlinger, G., and Jingsui, Y. (2001). Oblique stepwise rise and growth of the Tibet Plateau. Science 294, 1671–677.

    CAS  Article  PubMed  Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–882.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Tsigenopoulos, C.S., Rab, P., Naran, D., and Berrebi, P. (2002). Multiple origins of polyploidy in the phylogeny of southern African barbs (Cyprinidae) as inferred from mtDNA markers. Heredity 88, 466–73.

    CAS  Article  PubMed  Google Scholar 

  • Uyeno, T., and Smith, G.R. (1972). Tetraploid origin of the karyotype of catostomid fishes. Science 175, 644–46.

    CAS  Article  PubMed  Google Scholar 

  • Van Couvering, J.A.H. (1977). Early records of freshwater fishes in Africa. Copeia 1977, 163–66.

    Article  Google Scholar 

  • Wang, M., Yang, J.X., and Chen, X.Y. (2013). Molecular phylogeny and biogeography of Percocypris (Cyprinidae, Teleostei). PLoS One 8, e61827.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Willett, C.E., Cherry, J.J., and Steiner, L.A. (1997). Characterization and expression of the recombination activating genes (rag1 and rag2) of zebrafish. Immunogenetics 45, 394–04.

    CAS  Article  PubMed  Google Scholar 

  • Wolf, U., Ritter, H., Atkin, N.B., and Ohno, S. (1969). Polyploidization in the fish family Cyprinidae, order Cypriniformes. I. DNA-content and chromosome sets in various species of Cyprinidae. Humangenetik 7, 240–44.

    CAS  PubMed  Google Scholar 

  • Wu, Z., Barosh, P.J., Wu, Z., Hu, D., Zhao, X., and Ye, P. (2008). Vast early Miocene lakes of the central Tibetan Plateau. Geol Soc Am Bull 120, 1326–337.

    Article  Google Scholar 

  • Yang, L., Sado, T., Vincent Hirt, M., Pasco-Viel, E., Arunachalam, M., Li, J., Wang, X., Freyhof, J., Saitoh, K., Simons, A.M., Miya, M., He, S., and Mayden, R.L. (2015a). Phylogeny and polyploidy: resolving the classification of cyprinine fishes (Teleostei: Cypriniformes). Mol Phylogenet Evol 85, 97–16.

    Article  PubMed  Google Scholar 

  • Yang, L.D., Wang, Y., Zhang, Z.L., and He, S.P. (2015b). Comprehensive transcriptome analysis reveals accelerated genic evolution in a Tibet fish, Gymnodiptychus pachycheilus. Genome Biol Evol 7, 251–61.

    Article  CAS  Google Scholar 

  • Yazdani Moghaddam, F., Aliabadian, M., Khalijah Daud, S., and Seifali, M. (2013). Molecular phylogeny of the Puntius (Hamilton, 1822) based on nuclear gene rag2. Prog Biol Sci 2, 66–5.

    Google Scholar 

  • Yonezawa, T., Hasegawa, M., and Zhong, Y. (2014). Polyphyletic origins of schizothoracine fish (Cyprinidae, Osteichthyes) and adaptive evolution in their mitochondrial genomes. Genes Genet Syst 89, 187–91.

    Article  PubMed  Google Scholar 

  • Yu, X., Zhou, T., Li, K., Li, Y., and Zhou, M. (1987). On the karyosystematics of cyprinid fishes and a summary of fish chromosome studies in China. Genetica 72, 225–36.

    Article  Google Scholar 

  • Yu, X., Zhou, T., Li, Y., Li, K., and Zhou, M. (1989). Chromosomes of Chinese Fresh-Water Fishes. (Beijing: Science Press).

    Google Scholar 

  • Yuan, W., Dong, J., Shicheng, W., and Carter, A. (2006). Apatite fission track evidence for Neogene uplift in the eastern Kunlun Mountains, northern Qinghai-Tibet Plateau, China. J Asian Earth Sci 27, 847–56.

    Article  Google Scholar 

  • Yue, P., ed. (2000). Fauna Sinica, Osteichthys: Cypriniformes (Part III). (Beijing: Science Press).

  • Zhang, J.W., Nie, Z.L., and Sun, H. (2009). Cytological study on the genus Syncalathium (Asteraceae-Lactuceae), an endemic taxon to alpine scree of the Sino-Himalayas. J Syst Evol 47, 226–30.

    Article  Google Scholar 

  • Zheng, H., Clift, P.D., Wang, P., Tada, R., Jia, J., He, M., and Jourdan, F. (2013). Pre-Miocene birth of the Yangtze River. Proc Natl Acad Sci USA 110, 7556–561.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Zheng, H.B., Powell, C.M., An, Z.S., Zhou, J., and Dong, G.R. (2000). Pliocene uplift of the northern Tibetan Plateau. Geology 28, 715–18.

    Article  Google Scholar 

  • Zhou, C., Wang, X., Gan, X., Zhang, Y., Irwin, D.M., Mayden, R.L., and He, S. (2016). Diversification of Sisorid catfishes (Teleostei: Siluriformes) in relation to the orogeny of the Himalayan Plateau. Sci Bull 61, 991–002.

    CAS  Article  Google Scholar 

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    Xuzhen Wang, Xiaoni Gan, Junbing Li, Yiyu Chen & Shunping He

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Wang, X., Gan, X., Li, J. et al. Cyprininae phylogeny revealed independent origins of the Tibetan Plateau endemic polyploid cyprinids and their diversifications related to the Neogene uplift of the plateau. Sci. China Life Sci. 59, 1149–1165 (2016). https://doi.org/10.1007/s11427-016-0007-7

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Keywords

  • Cyprininae
  • polyploid
  • schizothoracins
  • the Tibetan Plateau
  • diversifications