Abstract
The "out of Tibet" hypothesis that suggests an important role of Tibetan highlands in the evolution of Central Asian cold-adapted fauna is a matter of debate. The long-tailed hamster Cricetulus longicaudatus is an important member of both steppe/semidesert Mongolian and high altitude Tibetan faunas. In this study, we analyze the mitochondrial variation in C. longicaudatus throughout a major part of its distribution range, perform molecular dating of the main divergence events, and model its historical range. The data reveal six genetic lineages, which are estimated to have diverged 100–200 kya. Four of the lineages are distributed in the northeastern part of the Qinghai-Tibetan Plateau. The northern part of the distribution range (Mongolia and southern Siberia) is almost entirely populated by another single lineage; its sister haplogroup is restricted to a small isolate in the Xingan Mountains. Species distribution modeling shows that the southern (Chinese) part of the geographic range of C. longicaudatus was relatively stable over the last 200 kya, while the northern (Mongolian) part demonstrated a high level of temporal variation, contracting considerably during cold glacials. The results suggest that the main center of origin of the long-tailed hamster was located in Tibet and that the northern part of the recent range was colonized through a single dispersal event at the Middle–Late Pleistocene boundary. At the same time, the comparative analysis of the fauna of Tibet and Mongolia indicates that the "out of Tibet" model is not the predominant pattern of geographic range evolution for small mammals.
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All sequences obtained for this study are now being deposited into GenBank.
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References
Anderson RP, Raza A (2010) The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. J Biogeogr 37(7):1378–1393. https://doi.org/10.1111/j.1365-2699.2010.02290.x
Bannikov AG (1954) Mammals of the Mongolian People’s Republic. Publishing House of the Academy of Sciences of USSR, Moscow ([in Russian])
Bannikova AA, Chernetskaya D, Raspopova A, Alexandrov D, Fang Y, Dokuchaev N, Sheftel B, Lebedev V (2018) Evolutionary history of the genus Sorex (Soricidae, Eulipotyphla) as inferred from multigene data. Zool Scr 47(5):518–538. https://doi.org/10.1111/zsc.12302
Bannikova AA, Lebedev VS, Poplavskaya NS, Simanovsky SA, Undrakhbayar E, Adiya Y, Surov AV (2019) Phylogeny and phylogeography of arvicoline and lagurine voles of Mongolia. J Vertebr Biol 68(2):100–113. https://doi.org/10.25225/fozo.002.2019
Bodrov SY, Vasiljeva VK, Okhlopkov IM, Mamayev NV, Zakharov ES, Oleinikov AY, Genelt-Yanovskiy EA, Abramson NI (2020) Evolutionary history of mountain voles of the subgenus Aschizomys (Cricetidae, Rodentia), inferred from mitochondrial and nuclear markers. Integr Zool 15(3):187–201. https://doi.org/10.1111/1749-4877.12415
Brandler OV, Lyapunova EA (2009) Molecular phylogenies of the genus Marmota (Rodentia Sciuridae): comparative analysis. Ethol Ecol Evol 21(3–4):289–298. https://doi.org/10.1080/08927014.2009.9522484
Chang Y, Hou J, Yang Q, Wen Z, Xia L, Lv X, Cheng J, Ge D, Lissovsky AA (2016) Population genetic structure and demographic history of Ochotona cansus (Lagomorpha, Ochotonidae). Acta Theriol Sin 36(4):373–387
Cheng J, Lv X, Xia L, Ge D, Zhang Q, Lu L, Yang Q (2019) Impact of orogeny and environmental change on genetic divergence and demographic history of Dipus sagitta (Dipodoidea, Dipodinae) since the Pliocene in inland East Asia. J Mamm Evol 26(2):253–266. https://doi.org/10.1007/s10914-017-9397-6
Cheng J, Xia L, Feijó A, Shenbrot GI, Wen Z, Ge D, Lu L, Yang Q (2020) Phylogeny, taxonomic reassessment and ‘ecomorph’ relationship of the Orientallactaga sibirica complex (Rodentia: Dipodidae: Allactaginae). Zool J Linnean Soc. https://doi.org/10.1093/zoolinnean/zlaa102
Dawson MR (1967) Lagomorph history and the stratigraphic record. Essays in paleontology and stratigraphy. Raymond C. Moore commemorative volume. Univ Kansas Dept Geol Spec Publ 2:287–316
Deng T, Wang X, Fortelius M, Li Q, Wang Y, Tseng ZJ, Takeuchi GT, Saylor JE, Saila LK, Xie G (2011) Out of Tibet: Pliocene woolly rhino suggests high-plateau origin of Ice Age megaherbivores. Science 333(6047):1285–1288. https://doi.org/10.1126/science.1206594
Ding L, Liao J (2019) Phylogeography of the Tibetan hamster Cricetulus kamensis in response to uplift and environmental change in the Qinghai– Tibet Plateau. Ecol Evol 9:7291–7306. https://doi.org/10.1002/ece3.5301
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1. 7. Mol Biol Evol 29(8):1969–1973. https://doi.org/10.1093/molbev/mss075
Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17(1):43–57. https://doi.org/10.1111/j.1472-4642.2010.00725.x
Erbajeva MA, Montuire S, Chaline J (2001) New ochotonids (Lagomorpha) from the Pleistocene of France. Geodiversitas 23(3):395–409
Erbajeva M, Flynn LJ, Alexeeva N (2015) Late Cenozoic Asian Ochotonidae: taxonomic diversity, chronological distribution and biostratigraphy. Quat Int 355:18–23. https://doi.org/10.1016/j.quaint.2014.10.064
Excoffier L, Lischer HE (2010) Arlequin suite ver 3. 5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fan Z, Liu S, Liu Y, Zhang X, Yue B (2011) 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(3):339–351. https://doi.org/10.1007/s10709-011-9553-5
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37(12):4302–4315. https://doi.org/10.1002/joc.5086
Flint VE, Golovkin AN (1961) Essay on comparative ecology of hamsters of Tuva. Bull Mosk O-Va Ispyt Prir Otd Biol 66(5):57–75
Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol 62(5):707–724. https://doi.org/10.1093/sysbio/syt033
Gamisch A (2019) Oscillayers: a dataset for the study of climatic oscillations over Plio-Pleistocene time-scales at high spatial-temporal resolution. Glob Ecol Biogeogr 28(11):1552–1560. https://doi.org/10.1111/geb.12979
Ge DY, Zhang Z, Xia L, Zhang Q, Ma Y, Yang QS (2012) Did the expansion of C4 plants drive extinction and massive range contraction of micromammals? Inferences from food preference and historical biogeography of pikas. Palaeogeogr Palaeoclimatol Palaeoecol 326:160–171. https://doi.org/10.1016/j.palaeo.2012.02.016
Giraudoux P, Quéré JP, Delattre P, Bao G, Wang X, Shi D, Vuitton D, Craig PS (1998) Distribution of small mammals along a deforestation gradient in southern Gansu, central China. Acta Theriol 43(4):349–362
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Proceedings of the Conference Held in Nucleic Acids Symposium 41:95–98
Herron MD, Castoe TA, Parkinson CL (2004) Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus). Mol Phyl Evol 31(3):1015–1030. https://doi.org/10.1016/j.ympev.2003.09.015
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25(15):1965–1978. https://doi.org/10.1002/joc.1276
Ho SY, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22(7):1561–1568. https://doi.org/10.1093/molbev/msi145
Hoffmann R (2008) Cricetinae. In: Smith AT, Xie Y (eds) A guide to the mammals of China. Princeton University Press, Princeton, pp 129–1382
Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285
Kapli P, Lutteropp S, Zhang J, Kobert K, Pavlidis P, Stamatakis A, Flouri T (2017) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33(11):1630–1638. https://doi.org/10.1093/bioinformatics/btx025
Lebedev VS (2012) Cricetinae. In: Pavlinov IY, Lisovskii AA (eds) The mammals of Russia: a taxonomic and geographic reference. KMK, Moscow, pp 210–276
Lebedev VS, Bannikova AA, Lu L, Snytnikov EA, Adiya Y, Solovyeva EN, Abramov AV, Surov AV, Shenbrot GI (2018a) Phylogeographical study reveals high genetic diversity in a widespread desert rodent, Dipus sagitta (Dipodidae: Rodentia). Biol J Linn Soc 123(2):445–462. https://doi.org/10.1093/biolinnean/blx090
Lebedev VS, Bannikova AA, Neumann K, Ushakova MV, Ivanova NV, Surov AV (2018b) Molecular phylogenetics and taxonomy of dwarf hamsters Cricetulus Milne-Edwards, 1867 (Cricetidae, Rodentia): description of a new genus and reinstatement of another. Zootaxa 4387(2):331–349. https://doi.org/10.11646/zootaxa.4387.2.5
Lebedev V, Bogdanov A, Brandler O, Melnikova M, Enkhbat U, Tukhbatullin A, Abramov A, Surov A, Baklushinskaya I, Bannikova A (2020) Cryptic variation in mole voles Ellobius (Arvicolinae, Rodentia) of Mongolia. Zool Scr 49(5):535–548. https://doi.org/10.1111/zsc.12440
Li Q, Wang X (2015) Into Tibet: an Early Pliocene dispersal of fossil zokor (Rodentia: Spalacidae) from Mongolian Plateau to the hinterland of Tibetan Plateau. PLoS ONE 10(12):e0144993. https://doi.org/10.1371/journal.pone.0144993
Li JS, Song YL, Zeng ZG (2003) Elevational gradients of small mammal diversity on the northern slopes of Mt. Qilian China. Glob Ecol Biogeogr 12(6):449–460
Liao J, Jing D, Luo G, Wang Y, Zhao L, Liu N (2016) Comparative phylogeography of Meriones meridianus, Dipus sagitta, and Allactaga sibirica: potential indicators of the impact of the Qinghai-Tibetan Plateau uplift. Mamm Biol 81(1):31–39. https://doi.org/10.1016/j.mambio.2015.05.002
Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40(4):778–789. https://doi.org/10.1111/jbi.12058
Lv X, Xia L, Ge D, Wen Z, Qu Y, Lu L, Yang Q (2016) Continental refugium in the Mongolian Plateau during Quaternary glacial oscillations: phylogeography and niche modelling of the endemic desert hamster Phodopus Roborovskii. Plos ONE 11(2):e0148182. https://doi.org/10.1371/journal.pone.0148182
Lv X, Cheng J, Meng Y, Chang Y, Xia L, Wen Z, Ge D, Liu S, Yang Q (2018) Disjunct distribution and distinct intraspecific diversification of Eothenomys melanogaster in South China. BMC Evol Biol 50:1–14. https://doi.org/10.1186/s12862-018-1168-3
Markova AK (2007) Pleistocene mammal faunas of Eastern Europe. Quat Int 160(1):100–111. https://doi.org/10.1016/j.quaint.2006.09.011
Minh BQ, Nguyen MAT, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30(5):1188–1195. https://doi.org/10.1093/molbev/mst024
Musser GG Carleton MD (1993) Family Muridae. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 2nd ed. Smithsonian Institution Press, Washington, DC, and London, pp. 501–755
Nanova OG, Lebedev VS, Matrosova VA, Adiya Y, Undrakhbayar E, Surov AV, Shenbrot GI (2020) Phylogeography, phylogeny, and taxonomical revision of the Midday jird (Meriones meridianus) species complex from Dzungaria. J Zool Syst Evol Res 58(4):1335–1358. https://doi.org/10.1111/jzs.12372
Neumann K, Michaux J, Lebedev V, Yigit N, Colak E, Ivanova N, Poltoraus A, Surov A, Markov G, Maak S, Neumann S, Gattermann R (2006) Molecular phylogeny of the Cricetinae subfamily based on the mitochondrial cytochrome b and 12S rRNA genes and the nuclear vWF gene. Mol Phylogenetics Evol 39(1):135–148. https://doi.org/10.1016/j.ympev.2006.01.010
Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274. https://doi.org/10.1093/molbev/msu300
Päckert M, Favre A, Schnitzler J, Martens J, Sun YH, Tietze DT, Hailer F, Michalak I, Strutzenberger P (2020) “Into and out of” the Qinghai-Tibet Plateau and the Himalayas: centers of origin and diversification across five clades of Eurasian montane and alpine passerine birds. Ecol Evol 10(17):9283–9300. https://doi.org/10.1002/ece3.6615
Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31(2):161–175. https://doi.org/10.1111/j.0906-7590.2008.5203.x
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190(3–4):231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55(4):595–609. https://doi.org/10.1080/10635150600852011
Poplavskaya NS, Lebedev VS, Bannikova AA, Neumann K, Pavlenko MV, Kartavtseva IV, Bazhenov YA, Bogomolov PL, Abramov AV, Surov AV (2018a) Phylogeographic structure in the chromosomally polymorphic rodent Cricetulus barabensis sensu lato (Mammalia, Cricetidae). J Zool Syst Evol Res 57(3):679–694. https://doi.org/10.1111/jzs.12251
Poplavskaya NS, Bannikova AA, Fang Y, Sheftel BI, Ushakova MV, Surov AV, Lebedev VS (2018b) Is the center of origin of long-tailed hamster Cricetulus longicaudatus Milne-Edwards 1867 (Rodentia, Cricetidae) located in Tibet? Dokl Biol Sci 479(1):70–73. https://doi.org/10.1134/S0012496618020102
Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic barcode gap discovery for primary species delimitation. Mol Ecol 21(8):1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
Rambaut A, & Drummond, A. (2005). Tracer, version 1.2. 1. Computer program distributed by the authors. Department of Zoology, University of Oxford.
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3. 2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Lab Press, Cold Spring Harbor, NY
Smith AT, Xie Y (2008) A guide to the mammals of China. Princeton University Press, Princeton
Steppan SJ, Akhverdyan MR, Lyapunova EA, Fraser DG, Vorontsov NN, Hoffmann RS, Braun MJ (1999) Molecular phylogeny of the marmots (Rodentia: Sciuridae): tests of evolutionary and biogeographic hypotheses. Syst Biol 48(4):715–734. https://doi.org/10.1080/106351599259988
Steppan SJ, Kenagy GJ, Zawadzki C, Robles R, Lyapunova EA, Hoffmann RS (2011) Molecular data resolve placement of the Olympic marmot and estimate dates of trans-Beringian interchange. J Mammal 92(5):1028–1037. https://doi.org/10.1644/10-MAMM-A-272.1
Swofford DL (2003) PAUP* – phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland, MD
Tang LZ, Wang LY, Cai ZY, Zhang TZ, Ci HX, Lin GH, Su JP, Liu JQ (2010) Allopatric divergence and phylogeographic structure of the plateau zokor (Eospalax baileyi), a fossorial rodent endemic to the Qinghai-Tibetan Plateau. J Biogeogr 37(4):657–668. https://doi.org/10.1111/j.1365-2699.2009.02232.x
Tang MK, Jin W, Tang Y, Yan CC, Murphy RW, Sun ZY, Zhang XY, Zeng T, Liao R, Hou QF, Yue BS (2018) Reassessment of the taxonomic status of Craseomys and three controversial species of Myodes and Alticola (Rodentia: Arvicolinae). Zootaxa 4429(1):1–52. https://doi.org/10.11646/zootaxa.4429.1.1
Tseng ZJ, Wang X, Slater GJ, Takeuchi GT, Li Q, Liu J, Xie G (2014) Himalayan fossils of the oldest known pantherine establish ancient origin of big cats. Proc R Soc b: Biol Sci 281(1774):20132686. https://doi.org/10.1098/rspb.2013.2686
Wang XM, Li Q, Qiu ZD, Xie GP, Wang BY, Qiu ZX, Tseng ZJ, Takeuchi GT, Deng T (2013) Neogene mammalian biostratigraphy and geochronology of the Tibetan Plateau. In: Wang X, Flynn LJ, Fortelius M (eds) Fossil mammals of Asia: Neogene biostratigraphy and chronology. Columbia University Press, New York, pp 274–292
Wang X, Tseng ZJ, Li Q, Takeuchi GT, Xie G (2014) From ‘third pole’ to north pole: a Himalayan origin for the arctic fox. Proc R Soc b: Biol Sci 281(1787):20140893. https://doi.org/10.1098/rspb.2014.0893
Wang X, Wang Y, Li Q, Tseng ZJ, Takeuchi GT, Deng T, Xie G, Chang MM, Wang N (2015) Cenozoic vertebrate evolution and paleoenvironment in Tibetan Plateau: Progress and prospects. Gondwana Res 27(4):1335–1354. https://doi.org/10.1016/j.gr.2014.10.014
Wang X, Liang D, Jin W, Tang M, Liu S, Zhang P (2020) Out of Tibet: genomic perspectives on the evolutionary history of extant pikas. Molec Biol Evol 37(6):1577–1592. https://doi.org/10.1093/molbev/msaa026
Wu X, Fu H (2005) Rodent communities of in desert and semi–desert regions in Inner Mongolia. Dong Wu Xue Bao [acta Zoologica Sinica] 51(6):961–972
Xing Y, Ree RH (2017) Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. PNAS 114(17):E3444–E3451. https://doi.org/10.1073/pnas.1616063114
Yan J, Chen H, Lin G, Li Q, Chen J, Qin W, Su J, Zhang T (2017) Genetic evidence for subspecies differentiation of the Himalayan marmot, Marmota himalayana, in the Qinghai-Tibet Plateau. PloS one 12(8):e0183375. https://doi.org/10.1371/journal.pone.0183375
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591. https://doi.org/10.1093/molbev/msm088
Yu F, Li S, Kilpatrick WC, McGuire PM, Wei He K, W, (2012) Biogeographical study of plateau pikas Ochotona curzoniae (Lagomorpha, Ochotonidae). Zool Sci 29(8):518–526. https://doi.org/10.2108/zsj.29.518
Zhang Y, Jin S, Quan G, Li S, Ye Z, Wang F, Zhang M (1997) Distribution of mammalian species in China. China Forestry Publishing House, Beijing
Acknowledgements
The present study was funded by RFBR, projects № 16–34–60086 mol_a_dk, 20-54-53003_GFEN_a and by the Joint Russian-Mongolian Biological expedition of IEE RAS. We thank Eduard Galoyan for the specimen of the long-tailed hamster kindly presented to our work.
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Russian Foundation for Basic Research, projects № 16–34–60086mol_a_dk, 20–54–53003_GFEN_a and the Joint Russian-Mongolian Biological expedition of Institute of Ecology and Evolution Russian Academy of Sciences.
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V.S.L, N.S.M, A.V.S, Y.S, and G.I.S conceived and designed the study. V.S.L, A.A.B, B.I.S, N.Yu.F, J.Q, Y.Z, and Y.F provided samples of long-tailed hamsters. N.S.M and A.A.B obtained the sequences for recent samples. A.A.L performed the DNA analysis of the material from the museum collections. V.S.L, N.S.M, and A.A.B examined the relevant literature sources. V.S.L, N.S.M, and A.A.B analyzed the molecular data. G.I.S performed the geographic range modeling. All authors discussed the obtained results, made conclusions, and participated in the writing of the manuscript.
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Lebedev, V.S., Maslova (Poplavskaya), N.S., Lisenkova, A.A. et al. Phylogeographic pattern and Pleistocene range reconstruction in the long-tailed hamster Cricetulus longicaudatus (Rodentia, Cricetidae) support its Tibetan origin. Mamm Res 66, 635–648 (2021). https://doi.org/10.1007/s13364-021-00585-4
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DOI: https://doi.org/10.1007/s13364-021-00585-4