Mammalian Biology

, Volume 81, Issue 1, pp 31–39 | Cite as

Comparative phylogeography of Meriones meridianus, Dipus sagitta, and Allactaga sibirica: Potential indicators of the impact of the Qinghai-Tibetan Plateau uplift

  • Jicheng Liao
  • Dongdong Jing
  • Guangjie Luo
  • Ying Wang
  • Liming Zhao
  • Naifa LiuEmail author
Original Investigation


We conducted a comparative phylogeographic analysis of three rodent species (Meriones meridianus, Dipus sagitta, and Allactaga sibirica) on the northeast margin of the Qinghai-Tibetan Plateau, Qaidam Basin, the Hexi Corridor and Tengger-Badain Jaran Desert based on sequences of the mitochondrial cytochrome b gene of 264 individuals from 22 sampling sites. Our analyses indicated that the intraspecific genetic structures of the three rodents did not arise through the same historical events and that they did not show parallel geological and climatic histories. M. meridianus and D. sagitta, which showed low-altitude distributions, experienced less isolation because they stayed in stable favorable habitats. On the other hand, A. sibirica was strongly isolated due to fragmented habitats caused by the complex topography of the high-altitude regions in the Qaidam Basin. The two desert-dwelling rodent species, M. meridianus (0.023-0.014 Mya) and D. sagitta (0.013-0.009 Mya), showed sudden demographic expansion during the Last Glacial Maximum, with the disappearance of the ancient lakes and the maximum extent of desert expansion. A. sibirica is mostly distributed in the grassland mountain regions. Thus, steppe expansion and a sharp decrease in the ancient lake size significantly affected the species’ distribution during the Middle Pleistocene (0.525 Mya). No clear signal of population expansion was observed for this species, which might be attributable to successive phases of population bottlenecks obscuring the indicators of expansion. Our data reflect the continual interaction of extrinsic and intrinsic factors in generating intraspecific phylogeographic patterns and faunal diversity.


Comparative phylogeography Cytochrome b gene Meriones meridianus Allactaga sibirica Dipus sagitta 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arbogast, B.S., Kenagy, G., 2001. Comparative phylogeography as an integrative approachto historical biogeography.J. Biogeogr. 28, 819–825.CrossRefGoogle Scholar
  2. Arbogast, B.S., Browne, R.A., Weigl, P.D., 2001. Evolutionary genetics and Pleistocene biogeography of North American tree squirrels (Tamiasciurus). J. Mammal. 82, 302–319.CrossRefGoogle Scholar
  3. Avise, J.C., Arnold, J., Ball, R.M., Bermingham, E., Lamb, T., Neigel, J.E., Reeb, C.A., Saunders, N.C., 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18, 489–522.CrossRefGoogle Scholar
  4. Bandelt, H.J., Forster, P., Rohl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bermingham, E., Moritz, C, 1998. Comparative phylogeography: concepts and applications. Mol. Ecol. 7, 367–369.CrossRefGoogle Scholar
  6. Brouat, C, Tatard, C, Bâ, K., Cosson, J.F., Dobigny, G., Fichet-Calvet, E., Granjon, L, Lecompte, E., Loiseau,A., Mouline, K., Piry, S., Duplantier,J.-M., 2009. Phylogeography of the Guinea multimammate mouse (Mastomys erythroleucus): a case study for Sahelian species in West Africa. J. Biogeogr. 36, 2237–2250.CrossRefGoogle Scholar
  7. Brylski, P., Hall, B., 1988. Epithelial behaviors and threshold effects in the development and evolution of internal and external cheek pouches in rodents. J. Zool. Syst. Evol. Res. 26, 144–154.CrossRefGoogle Scholar
  8. Cai, B., Li, Q., Zheng, S., 2008. Fossil mammals from Majuangou section of Nihewan Basin. China and their age. Acta Anthropol. Sin. 27, 129–142.Google Scholar
  9. Chen, T., Ren, J., Wang, H.S., Ma, S.Z., Li, X.F., 1992. he effect of the environmental change on the fauna evolution in Qinghai lake region. J. Lake Sci. 4, 41–47.CrossRefGoogle Scholar
  10. Cui, Z., Chen, Y., Zhang, W., 2011. Research history, clacial chronology and origins of Quaternary glaciations in China. Quat. Sci. 31, 749–764.Google Scholar
  11. Deng, T., 2008. Response of mammalian evolution to the Neogene climatic and environmental changes in China. Chin. J. Nat. 6, 334–339, 372–373.Google Scholar
  12. Dong, G., Gao, Q., Zou, X., Li, B., Yan, M., 1995. Climatic changes since the late pleistocene in deserts of Badain Jaran Desert. Chin. Sci. Bull. 13, 1214–1218.CrossRefGoogle Scholar
  13. Drummond, A.J., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.PubMedPubMedCentralGoogle Scholar
  14. Drummond, A.J., Ho, S.Y.W., Phillips, M.J., Rambaut, A., 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Drummond, A.J., Ho, S.Y.W., Rawlence, N., Rambaut, A., 2007. A Rough Guide to BEAST 1.4. University of Auckland, Auckland, New Zealand.Google Scholar
  16. Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47–50.Google Scholar
  17. Fang, X., Shi, Z., Yang, S., Li, J., Jiang, P., 2002. The development of Tianshan loess and Gurbantunggut Desert and aridification in North Xinjiang. Chin. Sci. Bull. 7, 540–545.Google Scholar
  18. Fedorov, V.B., Goropashnaya, A.V., Boeskorov, G.G., Cook, J.A., 2008. Comparative phylogeography and demographic history of the wood lemming (Myopus schis-ticolor): implications for late Quaternary history of the taiga species in Eurasia. Mol. Ecol. 17, 598–610.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Fu, Y., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.PubMedPubMedCentralGoogle Scholar
  20. Gaubert, P., Machordom, A., Morales, A., López-Bao, J.V., Veron, G., Amin, M., Bar-ros, T., Basuony, M., Djagoun, C.A.M.S., Do Linh San, E., Fonseca, C, Geffen, E., OnderOzkurt, S., Cruaud, C, Couloux, A., Palomares, F., 2011. Comparative phylogeography of two African carnivorans presumably introduced into Europe: disentangling natural versus human-mediated dispersal across the Strait of Gibraltar. J. Biogeogr. 38, 341–358.CrossRefGoogle Scholar
  21. Girman, D.J., Vilà, C, Geffen, E., Creel, S., Mills, M.G., McNutt, J.W., Ginsberg, J., Kat, P.W., Mamiya, K.H., Wayne, R.K., 2001. Patterns of population subdivision, gene flow and genetic variability in the African wild dog (Lycaonpictus). Mol. Ecol. 10, 1703–1723.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Gu, Z., Wang, R., Hong, D., 1985. Hipparion were found on north-eastern fringes of the Qinghai-Tibet Plateau. Vertebr. Palasiat. 23, 246.Google Scholar
  23. Hickerson, M., Carstens, B., Cavender-Bares, J., Crandall, K., Graham, C, Johnson, J., Rissler, L., Victoriano, P., Yoder, A., 2010. Phylogeography’s past, present, and future: 10 years after Avise, 2000. Mol. Phylogenet. Evol. 54, 291–301.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Huelsenbeck, J., Ronquist, F., 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
  25. Huhndorf, M.H., Kerbis Peterhans, J.C., Loew, S.S., 2007. Comparative phylogeography of three endemic rodents from the Albertine Rift, east central Africa. Mol. Ecol. 16, 663–674.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Irwin, D., Kocher, T., Wilson, A., 1991. Evolution of the cytochrome bgene of mammals. J. Mol. Evol. 32, 123–144.CrossRefGoogle Scholar
  27. Jin, Y., Brown, R., Liu, N., 2008. Cladogenesisand phylogeography of the lizard Phrynocephalus vlangalii (Agamidae) on the Tibetan plateau. Mol. Ecol. 17, 1971–1982.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Li, C.,1981. Pontiansand-rat from Yushe basin, Shansi. Vertebr. Palasiat. 19, 321–326.Google Scholar
  29. Li, J., Fang, X., Pan, B., Zhao, Z., Song, Y., 2001. Late Cenozoic intensive uplift of Qinghai-Xizang plateau and its impacts on environments in surrounding area. Quat. Sci. 21, 381–391.Google Scholar
  30. Liu, H., Feng, J., Li, C, Shi, Y., Yang, G., Chen, Z., Wang, G., 1984. The ecological studies and investigations of Meriones meridianus. Chin. J. Zool. 4, 21–25.Google Scholar
  31. Lu, B., Zheng, Y., Murphy, R.W., Zeng, X., 2012. Coalescence patterns of endemic Tibetan species of stream salamanders (Hynobiidae: Batrachuperus). Mol. Ecol. 12, 3308–3324.CrossRefGoogle Scholar
  32. Luo, Z., Chen, W., Gao, W., 2000. Fauna sinica, Mammalia-Rodentia part III: Criceti-dae. Science Press, Beijing.Google Scholar
  33. Moussalli, A., Moritz, C, Williams, S.E., Carnaval, A.C., 2009. Variable responses of skinks to a common history of rainforest fluctuation: concordance between phylogeography and palaeo-distribution models. Mol. Ecol. 18, 483–499.PubMedCrossRefPubMedCentralGoogle Scholar
  34. Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A.B., Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Nicolas, V., Mboumba,J.F., Verheyen, E., Denys, C, Lecompte, E., Olayemi, A., Missoup, A.D., Katuala, P., Colyn, M., 2008. Phylogeographic structure and regional history of Lemniscomys striatus (Rodentia: Muridae) in tropical Africa. J. Biogeogr. 35, 2074–2089.CrossRefGoogle Scholar
  36. Nylander, J.A.A., 2004. MrModeltest v2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University.Google Scholar
  37. Perdices, A., Coelho, M., 2006. Comparative phylogeography of Zacco platypus and Opsariichthys bidens (Teleostei, Cyprinidae) in China based on cytochrome b sequences. J. Zool. Syst. Evol. Res. 44, 330–338.CrossRefGoogle Scholar
  38. Polzin, T., Daneshmand, S.V., 2003. On Steiner trees and minimum spanning trees in hypergraphs. Oper. Res. Lett. 31, 12–20.CrossRefGoogle Scholar
  39. Pybus, O., Rambaut, A., 2002. GENIE: estimating demographic history from molecular phylogenies. Bioinformatics 18, 1404–1405.PubMedCrossRefGoogle Scholar
  40. Qiu, Z., Li, C, 2004. Evolution of cenozoic mammalian faunal regions of China and the Qinghai-Tibet uplift. Sci. China Ser. D: Earth Sci. 9, 845–854.Google Scholar
  41. Qu, Y., Lei, F., 2009. Comparative phylogeography of two endemic birds of the Tibetan plateau, the white-rumped snow finch (Onychostruthus taczanowskii) and the Hume’s ground tit (Pseudopodoces humilis). Mol. Phylogenet. Evol. 51, 312–326.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Rambaut, A., 2009. Computer program and documentation distributed by the author, beastbioedacuk.Google Scholar
  44. Rambaut, A., Drummond, A., 2007. Tracer, version 1.4 Computer program and documentation distributed by the author,
  45. Renaud, S., Auffray, J., 2009. Adaptation and plasticity in insular evolution of the house mouse mandible. J. Zool. Syst. Evol. Res. 48, 138–150.CrossRefGoogle Scholar
  46. Rogers, A.R., Harpending, H., 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9, 552.Google Scholar
  47. Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X., Rozas, R., 2003. DnaSP DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496.CrossRefGoogle Scholar
  48. Rozihan, M., Ismail, E., 2011. Impact of Malaysian continental drift on the genetic diversity of horseshoe crab inferred through mt DNA sequence analysis. Int. J. Biol. 4, 104–110.CrossRefGoogle Scholar
  49. Sakka, H., QuÉRÉ, J.P., Kartavtseva, I., Pavlenko, M., Chelomina, G., Atopkin, D., Bog-danov, A., Michaux, J., 2010. Comparative phylogeography of four Apodemus species (Mammalia: Rodentia) in the Asian Far East: evidence of quaternary climatic changes in their genetic structure. Biol. J. Linn. Soc. 100, 797–821.CrossRefGoogle Scholar
  50. Schneider, S., Roessli, D., Excoffier, L., 2000. Arlequin: a software for population genetics data analysis. User manual ver 2., pp. 2496–2497.Google Scholar
  51. Shi, Z., Fang, X., Song, Y., An, Z., Yang, S., 2006. Loess sediments in the north slope of Tianshan mountains and its indication of desertification since middle pleistocene. Mar. Geol. Quat. Geol. 3, 109–114.Google Scholar
  52. Steel, M., McKenzie, A., 2001. Properties of phylogenetic trees generated by Yule-type speciation models. Math. Biosci. 170, 91–112.PubMedCrossRefPubMedCentralGoogle Scholar
  53. Swofford, D.L., 2003. PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  54. Tajima, F., 1989. The effect of change in population size on DNA polymorphism. Genetics 123, 597.Google Scholar
  55. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Tang, L., Wang, L., Cai, Z., Zhang, T., Ci, H., Lin, G., Su, J., Liu, J., 2010. Allopatric divergence and phylogeographic structure of the plateau zokor (Eospalax baileyi), a fossorial rodent endemic to the Qinghai-Tibetan Plateau. J. Biogeogr. 37, 657–668.CrossRefGoogle Scholar
  57. 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. Nucleic Acids Res. 25, 4876.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Wang, X., Xie, G., Li, Q., Qiu, Z., Tseng, Z.J., Takeuchi, G.T., Wang, B., Fortelius, M., Rosenstr(O)M-Fortelius, A., Wahlquist, H., Downs, W.R., Zhang, C, Wang, Y., 2011. Early explorations of Qaidam basin (Tibetan plateau) by Birger Bohlin-reconciling classic vertebrate fossil localities with modern biostratigraphy. Vertebr. Palasiat. 49, 285–310.Google Scholar
  59. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Zhang, R., 1979. Chinese Nature Geoscience. Science Press, Beijing.Google Scholar
  61. Zhang, L., Song, Y., 2001. The effect of the Qinghai-Tibet Plateau uplift on the space-time distributing pattern of Chinese desert and desertification. China Popul. Resour. Environ. 3, 367–372.Google Scholar
  62. Zhang, J., Wang, Z., 1963. Faunistic studies of mammals of the Chinghai province. Acta Zool. Sin. 15, 125–127.Google Scholar
  63. Zhang, R., Zheng, C, 1985. The geographical distribution of mammals and the evolution of mammalian fauna in Qinghai-Xizang Plateau. Acta Geogr. Sin. 40, 225–230.Google Scholar
  64. Zhang, Q., Chiang, T., George, M., Liu, J., Abbott, R., 2005. Phylogeography of the Qinghai-Tibetan Plateau endemic Juniperus przewalskii (Cupressaceae) inferred from chloroplast DNA sequence variation. Mol. Ecol. 14, 3513–3524.PubMedCrossRefPubMedCentralGoogle Scholar
  65. Zhao, K., 1991. China’s Jerboas. J. Suzhou Railw. Normal Coll. 8, 29–36.Google Scholar
  66. Zhao, Q., Liu, H., Luo, L.,Ji,X., 2011. Comparative population genetics and phylogeography of two lacertid lizards (Eremias argus and E. brenchleyi) from China. Mol. Phylogenet. Evol. 58, 478–491.PubMedCrossRefPubMedCentralGoogle Scholar
  67. Zheng, S., Cai, B., Li, Q., 2006. The Plio-Pleistocen small mammals from Donggou section of Nihewan Basin, Hebei, China. Vertebr. Palasiat. 44, 320–331.Google Scholar
  68. Zhou, L, Ma, Y., Li, D., 2001. Spatial distribution patterns of Chinese gerbils (gerbilline) in relation to environmental factors. Acta Zool. Sin. 47, 616–624.Google Scholar
  69. Zhu, X., Kang, A., Han, D., Wang, Y., Kang, Q., 2003. Relation among Quaternary environmental evolution, tectonic deformation in the Qaidam Basin and uplifting of the Qinghai-Tibet Plateau. Chin. J. Geol. 38, 367–376.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2015

Authors and Affiliations

  • Jicheng Liao
    • 1
  • Dongdong Jing
    • 1
  • Guangjie Luo
    • 1
  • Ying Wang
    • 1
  • Liming Zhao
    • 1
  • Naifa Liu
    • 1
    Email author
  1. 1.Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental PollutionSchool of Life Sciences, Lanzhou UniversityLanzhouChina

Personalised recommendations