Skip to main content

Advertisement

SpringerLink
Log in

How Quaternary geologic and climatic events in the southeastern margin of the Tibetan Plateau influence the genetic structure of small mammals: inferences from phylogeography of two rodents, Neodon irene and Apodemus latronum

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Phylogeographical studies that focus on the southeastern margin of the Tibetan Plateau are limited. The complex terrain and unique geological history make it a particularly unusual region of the Tibetan Plateau. We carried out a phylogeographical study of two rodent species Neodon irene and Apodemus latronum using the mitochondrial cytochrome b gene sequences. High genetic diversities and deep phylogenetic splits were detected in both rodents. Some haplotypes from one sampling region fell into different evolutionary clades, but most haplotypes from the same sampling regions were clustered together with each other. The results of isolation by distance analysis further substantiated that their genetic diversities were structured along geography. Thus, there were high levels of geographical structure for both rodents. Demographic analyses implied a relatively constant population size for all samples of N. irene and A. latronum in history. However, clade B of N. irene and clade 3 of A. latronum experienced population expansions at 105–32 and 156–47 Kya, respectively. Through comparison with previous studies, we suggest the high mitochondrial DNA diversities in them are probably not a species-specific feature, but a common pattern for small mammals in this unique area. Details of the historical demography of these rodents revealed in this study could provide new insights into how rodents and possibly other small mammals in this region responded to the geological and climatic events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • An Z, John EK, Warren LP, Stephen CP (2001) Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature 411:62–66

    Article  CAS  Google Scholar 

  • Arbogast BS, Browne RA, Weigl PD (2001) Evolutionary genetics and Pleistocene biogeography of North American tree squirrels (Tamiasciurus). J Mammal 82:302–319

    Article  Google Scholar 

  • Avise JC (1998) The history and purview of phylogeography: a personal reflection. Mol Ecol 7:371–379

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  CAS  Google Scholar 

  • Brunhoff C, Galbreath KE, Fedorov VB, Cook JA, Jaarola M (2003) Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes. Mol Ecol 12:957–968

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Liu S, Liu Y, Hao H, Zeng B, Chen S, Peng H, Yue B, Zhang X (2010) Phylogeography of the large white-bellied rat Niviventer excelsior suggests the influence of Pleistocene Glaciations in the Hengduan Mountains. Zoolog Sci 27:487–493

    Article  PubMed  Google Scholar 

  • Ci H, Lin G, Cai Z, Tang L, Su J, Liu J (2009) Population history of the plateau pika endemic to the Qinghai-Tibetan Plateau based on mtDNA sequence data. J Zool 279:396–403

    Article  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver.3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  CAS  Google Scholar 

  • Fan Z, Liu S, Liu Y, Zeng B, Zhang X, Cuo C, Yue B (2009) Molecular phylogeny and taxonomic reconsideration of the subfamily Zapodiane (Rodentia: Dipodidae), with an emphasis on Chinese species. Mol Phylogenet Evol 51:447–453

    Article  PubMed  CAS  Google Scholar 

  • Fedorov VB, Goropashnaya AV, Boeskorov GG, Cook JA (2008) Comparative phylogeography and demographic history of the wood lemming (Myopus schisticolor): implications for late Quaternary history of the taiga species in Eurasia. Mol Ecol 17:598–610

    Article  PubMed  CAS  Google Scholar 

  • Fu YX (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Galbreath KE, Cook JA (2004) Genetic consequences of Pleistocene glaciations for the tundra vole (Microtus oeconomus) in Beringia. Mol Ecol 13:135–148

    Article  PubMed  CAS  Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    PubMed  CAS  Google Scholar 

  • Harrison TM, Copeland P, Kidd WSF, Yin A (1992) Raising Tibet. Science 255:1663–1670

    Article  PubMed  CAS  Google Scholar 

  • Haynes S, Jaarola M, Searle JB (2003) Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago. Mol Ecol 12:951–956

    Article  PubMed  CAS  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Proc R Soc Lond B 359:183–195

    CAS  Google Scholar 

  • Hu J, Wang Y, Cheng H, Cheng E, Deng Q, Deng Z, He G, Shi C, Song Y, Yu Z (1984) Sichuan Fauna Economica Volume 2. Sichuan Publishing House of Science & Technology, Chengdu

    Google Scholar 

  • Huang Z, Liu N, Liang W, Zhang Y, Liao X, Ruan L, Yang Z (2010) Phylogeography of Chinese bamboo partridge, Bambusicola thoracica thoracica (Aves: Galliformes) in south China: inference from mitochondrial DNA control-region sequences. Mol Phylogenet Evol 56:273–280

    Article  PubMed  Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144

    Article  PubMed  CAS  Google Scholar 

  • Jaarola M, Searle JB (2002) Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Mol Ecol 11:2613–2621

    Article  PubMed  CAS  Google Scholar 

  • Jensen J, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13

    Article  PubMed  Google Scholar 

  • Jin Y, Brown RP, Liu N (2008) Cladogenesis and phylogeography of the lizard Phrynocephalus vlangalii (Agamidae) on the Tibetan plateau. Mol Ecol 17:1971–1982

    Article  PubMed  CAS  Google Scholar 

  • Jing M, Yu H, Wu S, Wang W, Zheng X (2007) Phylogenetic relationships in genus Niviventer (Rodentia: Muridae) in China inferred from complete mitochondrial cytochrome b gene. Mol Phylogenet Evol 44:521–529

    Article  PubMed  CAS  Google Scholar 

  • Lehmkuhl F, Haselein F (2000) Quaternary palaeoenvironmental change on the Tibetan Plateau and adjacent areas (Western China and Western Mongolia). Quatern Int 65(66):121–145

    Article  Google Scholar 

  • Li J, Li B, Wang F (1981) The process of uplift of the Qinghai-Xizang Plateau. Geological and ecological studies of Qinghai-Xizang Plateau, Science Press, Beijing

    Google Scholar 

  • Li M, Wei FW, Goossens B, Feng ZJ, Tamate HB, Bruford MW, Funk SM (2005) Mitochondrial phylogeography and subspecific variation in the red panda (Ailurus fulgens): implications for conservation. Mol Phylogenet Evol 36:78–89

    Article  PubMed  CAS  Google Scholar 

  • Li S, Yeung CKL, Feinstein J, Han L, Le M, Wang C, Ding P (2009) Sailing through the Late Pleistocene: unusual historical demography of an East Asian endemic, the Chinese Hwamei (Leucodioptron canorum canorum), during the last glacial period. Mol Ecol 18:622–633

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Wei F, Li M, Jiang X, Feng Z, Hu J (2004) Molecular phylogeny and taxonomy of wood mice (genus Apodemus Kaup, 1829) based on complete mtDNA cytochrome b sequences, with emphasis on Chinese species. Mol Phylogenet Evol 33:1–15

    Article  PubMed  Google Scholar 

  • Luo Z, Chen W, Gao W (2000) Fauna Sinica (Mammalia Vol. 6 Rodentia II Cricetidae). Science Press, Beijing

    Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Michaux JR, Libois R, Filippucci M-G (2005) So close and so different: comparative phylogeography of two small mammal species, the Yellow-necked fieldmouse (Apodemus flavicollis) and the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Heredity 94:52–63

    Article  PubMed  CAS  Google Scholar 

  • Moeller DA, Tiffin P (2005) Genetic diversity and the evolutionary history of plant immunity genes in two species of Zea. Mol Biol Evol 22:2480–2490

    Article  PubMed  CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) Mrmodeltest V2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Norbyv

    Google Scholar 

  • Oshida T, Abramov A, Yanagawa H, Masuda R (2005) Phylogeography of the Russian flying squirrel (Pteromys volans): implication of refugia theory in arboreal small mammal of Eurasia. Mol Ecol 14:1191–1196

    Article  PubMed  CAS  Google Scholar 

  • Pilkington MM, Wilder JA, Mendez FL, Cox MP, Woerner A, Angui T, Kingan S, Mobasher Z, Batini C, Destro-Bisol G, Soodyall H, Strassmann BI, Hammer MF (2008) Contrasting signatures of population growth for mitochondrial DNA and Y chromosomes among human populations in Africa. Mol Biol Evol 25:517–525

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Qu Y, Ericson PGP, Lei F, Li S (2005) Postglacial colonization of the Tibetan plateau inferred from the matrilineal genetic structure of the endemic red-necked snow finch, Pyrgilauda ruficollis. Mol Ecol 14:1767–1781

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rogers A, Harpending HM (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Ronquist FR, Huelsenbeck JP (2003) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Sakka H, Quéré JP, Kartavtseva I, Pavlenko M, Chelomina G, Atopkin D, Bogdanov 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

    Article  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Press, New York

    Google Scholar 

  • Serizawa K, Suzuki H, Tsuchiya K (2000) A phylogenetic view on species radiation in Apodemus inferred from variation of nuclear and mitochondiral genes. Biochem Genet 38:27–40

    Article  PubMed  CAS  Google Scholar 

  • Shi Y (2002) Characteristics of late Quaternary monsoonal glaciation on the Tibetan plateau and in East Asia. Quatern Int 97–98:79–91

    Article  Google Scholar 

  • Shi Y, Zheng B, Li S (1990) Last glaciation and maximum glaciation in Qinghai-Xizang (Tibet) plateau. J Glaciol Geocryol 12:1–15

    Google Scholar 

  • Shi Y, Li J, Li B (1998) Uplift and Environmental Changes of Qinghai-Tibetan Plateau in the Late Cenozoic. Guangdong Science and Technology Press, Guangzhou

    Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    PubMed  CAS  Google Scholar 

  • Song G, Qu Y, Yin Z, Li S, Liu N, Lei F (2009) Phylogeography of the Alcippe morrisonia (Aves: Timaliidae): long population history beyond late Pleistocene glaciations. BMC Evol Biol 9:143

    Article  PubMed  Google Scholar 

  • Su B, Fu Y, Wang Y, Jin L, Chakraborty R (2001) Genetic diversity and population history of the red panda (Ailurus fulgens) as inferred from Mitochondrial DNA sequence variations. Mol Biol Evol 18:1070–1076

    PubMed  CAS  Google Scholar 

  • Su Z, Shi Y, Zheng B (2002) Quaternary glacial remains on the Gongga Mountain and the division of glacial period. Adv Earth Sci 17:639–647

    Google Scholar 

  • Suzuki H, Sato JJ, Tsuchiya K, Luo J, Zhang Y, Wang Y, Jiang X (2003) Molecular phylogeny of wood mice (Apodemus, Muridae) in East Asia. Biol J Linn Soc 80:469–481

    Article  Google Scholar 

  • Suzuki H, Filippucci MG, Chelomina GN, Sato JJ, Serizawa K, Nevo E (2008) A biogeographic view of Apodemus in Asia and Europe inferred from Nuclear and Mitochondrial gene sequences. Biochem Genet 46:329–346

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Cui Z, Liu G, Ge D, Yin J, Xu Q, Pang Q (2001) Quaternary geomorphological evolution of the Kunlun Pass areas and uplift of the Qinghai-Xizang (Tibet) plateau. Geomorphology 36:203–216

    Article  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Heredity 92:371–373

    Article  CAS  Google Scholar 

  • Xu L, Zhou S, Cui J, Wang J, Mickelson D (2004) Dating of the Pleistocene Glaciations around the Daocheng Ice Cap. J Glaciol Geocryol 26:528–534

    Google Scholar 

  • Yang S, Yin Z, Ma X, Lei F (2006) Phylogeography of ground tit (Pseudopodoces humilis) based on mtDNA: Evidence of past fragmentation on the Tibetan Plateau. Mol Phylogenet Evol 41:257–265

    Article  PubMed  CAS  Google Scholar 

  • Zeng B, Xu L, Yue B, Li Z, Zou F (2008) Molecular phylogeography and genetic differentiation of blue sheep Pseudois nayaur szechuanensis and Pseudois schaeferi in China. Mol Phylogenet Evol 48:387–395

    Article  PubMed  CAS  Google Scholar 

  • Zhang F, Jiang Z (2006) Mitochondrial phylogeography and genetic diversity of Tibetan gazelle (Procapra picticaudata): Implications for conservation. Mol Phylogenet Evol 41:313–321

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Feng Q, Jian M (2000) Eco-environmental effects of the Qinghai-Tibet plateau uplift during the Quaternary in China. EnvironmGeol 39:1352–1358

    Google Scholar 

  • Zheng BX (1990) The glacier, environment and its changes since the last glaciation in West China. Quatern Sci 2:101–110

    Google Scholar 

  • Zheng D (1996) The system of physico-geographical regions of the Qinghai-Tibet (Xizang) Plateau. Sci in China (Series D) 39:410–417

    Google Scholar 

  • Zheng H, Powell CM, An ZS, Dong G (2000) Pliocene uplift of the northern Tibet Plateau. Geology 8:715–718

    Article  Google Scholar 

  • Zheng B, Xu Q, Shen Y (2002) The relatonship between climate change and Quaternary glacial cycles on the Qinghai-Tibetan plateau: review and speculation. Quatern Int 97–98:93–101

    Article  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge Rui Liao at Sichuan Academy of Forestry for collecting samples and Emily King at Sichuan University for English revisions. We also thank Dr. Greta Binford at Lewis & Clark College for her valuale comments and suggestions. This research was funded by the National Basic Research Program of China (973 Project: 2007 CB109106 and 2007 CB411605).

Author information

Authors and Affiliations

  1. Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu, 610064, People’s Republic of China

    Zhenxin Fan, Xiuyue Zhang & Bisong Yue

  2. Sichuan Academy of Forestry, Chengdu, 610081, People’s Republic of China

    Shaoying Liu & Yang Liu

Authors
  1. Zhenxin Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaoying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiuyue Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bisong Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bisong Yue.

Additional information

Z. Fan and S. Liu authors are contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fan, Z., Liu, S., Liu, Y. et al. How Quaternary geologic and climatic events in the southeastern margin of the Tibetan Plateau influence the genetic structure of small mammals: inferences from phylogeography of two rodents, Neodon irene and Apodemus latronum . Genetica 139, 339–351 (2011). https://doi.org/10.1007/s10709-011-9553-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-011-9553-5

Keywords

Search

Navigation