Abstract
Diversification patterns and demography of montane species are affected by Pleistocene climate fluctuations. Empirical cases from the Qinling Mountains (QM) region, which is a major biogeographic divider of East Asia, are few. We used DNA sequence data of the complete mitochondrial ND2 gene to detect effects of the Pleistocene glaciations on phylogeographic profiles of a frog species, Feirana taihangnica, which is endemic to the QM. Four distinct lineages consisting of seven sublineages were revealed. The strongest signal of biogeographical structure (F ct = 0.971, P < 0.01) was found when populations were grouped according to these seven sublineages. One narrow secondary contact zone was detected in the middle QM between the lineage from middle QM and the lineage from eastern QM. Coalescent simulations indicated that this species colonized the QM region by a stepping-stone model. Divergences among lineages had likely been influenced by the uplift of the Tibetan Plateau during the late Miocene-to-late Pleistocene, as well as by the Pleistocene climatic cycles. Coalescent simulations also suggested that F. taihangnica populations have persisted through the Pleistocene glacial periods in multiple refugia across the QM region. Demographic analyses indicated that all lineages, except the lineage in the Funiu Mountains, have been experienced postglacial expansion of population size and distribution range. In conclusion, Pleistocene climate fluctuations and tectonic changes during the late Miocene-late Pleistocene have profoundly influenced the phylogeography and historical demography of F. taihangnica.
Similar content being viewed by others
References
An ZS, Kutzbach JE, Prell WL, Porter SC (2001) Evolution of Asian monsoons and phased uplift of the Himalaya–Tibetan plateau since Late Miocene times. Nature 411:62–66
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Avise JC, Walker D (1998) Pleistocene phylogeographic effects on avian populations and the speciation process. Proceedings of the Royal Society B: Biological Sciences 265(1395):457–463
Avise JC, Walker D, Johns GC (1998) Speciation durations and Pleistocene effects on vertebrate phylogeography. Proceedings of the Royal Society B: Biological Sciences 265(1407):1707–1712
Beerli P (2008) MIGRATE version 2.4.1. http://popgen.csit.fsu.edu/Migrate-n.html
Bermingham E, McCafferty SS, Martin AP (1997) Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. In: Kocher TD, Stepien CA (eds) Molecular systematics of fishes. Academic Press, San Diego, pp 113–118
Bertorelle G, Slatkin M (1995) The number of segregating sites in expanding human populations, with implications for estimates of demographic parameters. Mol Biol Evol 12:887–892
Burg T, Gaston AJ, Winker K, Friesen VL (2005) Rapid divergence and postglacial colonization in western North American Steller’s jays (Cyanocitta stelleri). Mol Ecol 14:3745–3755
Carstens BC, Richards CL (2007) Integrating coalescent and ecological niche modelling in comparative phylogeography. Evolution 61:1439–1454
Carstens BC, Sullivan J, Davalos LM, Larsen PA, Pedersen SC (2004) Exploring population genetic structure in three species of Lesser Antillean bats. Mol Ecol 13:2557–2566
Castoe TA, Spencer CL, Parkinson CL (2007) Phylogeographic structure and historical demography of the western diamondback rattlesnake (Crotalus atrox): a perspective on North American desert biogeography. Mol Phylogenet Evol 42:193–212
Che J, Hu JS, Zhou WW, Murphy RW, Papenfuss TJ, Chen MY, Rao DQ, Li PP, Zhang YP (2009) Phylogeny of the Asian spiny frog tribe Paini (Family Dicroglossidae) sensu Dubois. Mol Phylogenet Evol 50:59–73
Che J, Zhou WW, Hua JS et al (2010) Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc Natl Acad Sci USA 107(31):13765–13770
Chen XH, Jiang JP (2002) A new species of the genus Paa from China. Herpetol China 9:231
Cheng J (1997) The mammalian faunas showing climatic fluctuation: as an example of the Early Pleistocene mammalian faunas from Zhoukoudian. Earth Sci Front 4:275–279
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1659
Crawford AJ (2003) Relative rates of nucleotide substitution in frogs. J Mol Evol 57:636–641
Cui ZJ, Zhang W (2003) Discussion about the glacier extent and advance/retreat asynchrony during the last glaciation. J Glaciol Geocryol 25:510–516
De A, Durrett R (2007) Stepping-stone spatial structure causes slow decay of linkage disequilibrium and shifts the site frequency spectrum. Genetics 176:969–981
DeChaine EG, Martin AP (2006) Using coalescent simulations to test the impact of quaternary climate cycles on divergence in an alpine plant–insect association. Evolution 60:1004–1013
Ding L, He SP, Gan XN, Zhao EM (2011) A phylogeographic, demographic and historical analysis of the short-tailed pit viper (Gloydius brevicaudus): evidence for early divergence and late expansion during the Pleistocene. Mol Ecol 20:1905–1922
Dong YP, Zhang GW, Neubauer F, Liu XM, Genser J, Hauzenberger C (2011) Tectonic evolution of the Qinling orogen, China: review and synthesis. J Asian Earth Sci 41:213–237
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22(5):1185–1192
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710
Edwards SV, Beerli P (2000) Gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854
Excoffier L, Schneider S (1999) Why hunter–gatherer populations do not show signs of Pleistocene demographic expansions. Proc Natl Acad Sci USA 96:10597–10602
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50
Fei L, Ye CY, Jiang JP (2010) Colored atlas of Chinese amphibians. Sichuan Publishing House of Science and Technology, Chengdu
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J, Kishino H (1993) Is there something wrong with the bootstrap on phylogeny? A reply to Hillis and Bull. Syst Zool Syst Zool 42:193–200
Fernando P, Pfrender ME, Encalada SE, Landa R (2000) Mitochondrial DNA variation, phylogeography and population structure of the Asian elephant. Heredity 84:362–372
Fitzpatrick SW, Brasileiro CA, Haddad CF, Zamudio KR (2009) Geographical variation in genetic structure of an Atlantic coastal forest frog reveals regional differences in habitat stability. Mol Ecol 18:2877–2896
Fontanella FM, Feldman CR, Siddall ME (2008) Phylogeography of Diadophis punctatus: extensive lineage diversity and repeated patterns of historical demography in a transcontinental snake. Mol Phylogenet Evol 46:1049–1070
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Guiher TJ, Burbrink FT (2008) Demographic and phylogeographic histories of two venomous North American snakes of the genus Agkistrodon. Mol Phylogenet Evol 48:543–553
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. BMC Syst Biol 52:696–704
Guo P, Liu Q, Li C, Cheng X, Jiang K, Wang YZ, Malhotra A (2011) Molecular phylogeography of Jerdon’s pitviper (Protobothrops jerdonii): importance of the uplift of the Tibetan plateau. J Biogeogr 38:2326–2336
Hardin G (1960) The competitive exclusion principle. Science 131(3409):1292–1297
Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associates, Sunderland
Hedges SB (1992) The number of replications needed for accurate estimation of the bootstrap P-value in phylogenetic studies. Mol Biol Evol 9:366–369
Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318
Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276
Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405(6789):907–913
Hewitt GM (2004) Genetic consequences of climatic oscillations in the quaternary. Philos Trans R Soc B 359(1442):183–195
Hillesheim MB, Hodell DA, Leyden BW, Brenner M, Curtis JH, Anselmetti FS, Ariztegui D, Buck DG, Guilderson TP, Rosenmeier MF, Schnurrenberger DW (2005) Climate change in lowland Central America during the late deglacial and early Holocene. J Quat Sci 20:363–376
Hillis DM, Mable BK, Larson A, Davis SK, Zimmer EA (1996) Nucleic acids IV: sequencing and cloning. In: Hillis D, Moritz C, Mable B (eds) Molecular systematics. Sinauer Associates, Sunderland, pp 321–378
Huelsenbeck JP, Hillis DM (1993) Success of phylogenetic methods in the four-taxon case. Syst Biol 42:247–264
Hurvich CM, Tsai CL (1989) Regression and time series model selection in small samples. Biometrika 76:297–307
Huybers P (2009) Pleistocene glacial variability as a chaotic response to obliquity forcing. Clim Past 5:481–488
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service v. 3.14. BMC Genet 6:13
Jesus FF, Wilkins JF, Solferini VN, Wakeley J (2006) Expected coalescent times and segregating sites in a model of glacial cycles. Genet Mol Res 5:466–474
Jiang JP, Dubois A, Ohler A, Tillier A, Chen XH, Xie F, Stöck M (2005) Phylogenetic relationships of the tribe Paini (Amphibia, Anura, Ranidae) based on partial sequences of mitochondrial 12s and 16s rRNA genes. Zool Sci 22:353–362
Jin YT, Brown RP, Liu NF (2008) Cladogenesis and phylogeography of the lizard Phrynocephalus vlangalii (Agamidae) on the Tibetan plateau. Mol Ecol 17:1971–1982
Ju L, Wang H, Jiang D (2007) Simulation of the last glacial maximum climate over East Asia with a regional climate model nested in a general circulation model. Palaeogeogr Palaeoclimatol Palaeoecol 248:376–390
Kelly MJ, Edwards RL, Cheng H et al (2006) High resolution characterization of the Asian Monsoon between 146 146,000 and 99 99,000 years B.P. from Dongge Cave, China and global correlation of events surrounding Termination II. Palaeogeogr Palaeoclimatol Palaeoecol 236:20–38
Knowles LL (2000) Tests of Pleistocene speciation in montane grasshoppers (genus Melanoplus) from the sky islands of western North America. Evolution 54:1337–1348
Knowles LL (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Mol Ecol 10:691–701
Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol Ecol 11:2623–2635
Knutti R, Flückiger J, Stocker TF, Timmermann A (2004) Strong hemispheric coupling of glacial climate through freshwater discharge and ocean circulation. Nature 430:851–856
Kozak KH, Wiens JJ (2006) Does niche conservatism promote speciation? A case study in North American salamanders. Evolution 60:2604–2621
Kvist L, Viiri K, Dias PC, Rytkonen S, Orell M (2004) Glacial history and colonization of Europe by the blue tit Parus caeruleus. J Avian Biol 35:352–359
Leaché AD, Reeder TW (2002) Molecular systematics of the eastern fence lizard (Sceloporus undulatus): a comparison of parsimony, likelihood, and Bayesian approaches. Syst Biol 51:44–68
Li JJ, Shu Q, Zhou SZ, Zhao ZJ, Zhang JM (2004) Review and prospects of quaternary glaciation research in China. J Glaciol Geocryol 26(3):235–243
Li SH, Yeung CK, Feinstein J, Han L, Le MH, Wang CX, 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(4):622–633
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187
Lisiecki LE, Raymo ME (2007) Plio–Pleistocene climate evolution: trends and transitions in glacial cycle dynamics. Quatern Sci Rev 26:56–69
Liu JH, Zhang PZ, Zheng DW, Wang JL, Wang WT (2010) The cooling history of Cenozoic exhumation and uplift of Taibai Mountain, Qinling, China: evidence from the apatite fission track (AFT) analysis. Chin J Geophys 53(10):2405–2414
Macey JR, Schulte JA II, Ananjeva NB, Larson A, Rastegar-Pouyani N, Shammakovb SM, Papenfuss TJ (1998a) Phylogenetic relationships among Agamid Lizards of the Laudakia caucasia species group: testing hypotheses of biogeographic fragmentation and an Area Cladogram for the Iranian Plateau. Mol Phylogenet Evol 10:118–131
Macey JR, Schulte JAII, Larson A, Fang Z, Wang Y, Tuniyev BS, Papenfuss TJ (1998b) Phylogenetic relationships of toads in the Bufo bufo species group from the eastern escarpment of the Tibetan Plateau: a case of vicariance and dispersal. Mol Phylogenet Evol 9:80–87
Macey JR, Wang Y, Ananjeva NB, Larson A, Papenfuss TJ (1999) Vicariant patterns of fragmentation among gekkonid lizards of the genus Teratoscincus produced by the Indian Collision: a molecular phylogenetic perspective and an area cladogram for Central Asia. Mol Phylogenet Evol 12:320–332
Macey JR, Strasburg J, Brisson J, Vredenburg V, Jennings M, Larson A (2001) Molecular phylogenetics of western North American frogs of the Rana boylii species group. Mol Phylogenet Evol 19:131–143
Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org
Maddison WP, McMahon M (2000) Divergence and reticulation among montane populations of a jumping spider (Habronattus pugillis Griswold). Syst Biol 49:400–421
Maggs C, Castilho R, Foltz D, Kelly J, Olsen J, Perez KE, Stam W, Väinölä R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89(11 Suppl):S108–S122
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76(2):173–190
Marjoram P, Donnelly P (1994) Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution. Genetics 136:673–683
Milá B, McCormack JE, Castaneda G, Wayne RK, Smith TB (2007) Recent postglacial range expansion drives the rapid diversification of a songbird lineage in the genus Junco. Proc R Soc B 274:2653–2660
Molnar P (2005) Mio-Pliocene growth of the Tibetan Plateau and evolution of East Asian climate. Palaeontol Elect 8(1):1–23
Monney JC (1996) Biologie comparée de Vipera aspis L. et de Vipera berus L. (Reptilia, Ophidia, Viperidae) dans une station des Préalpes bernoises. Unpublished PhD Thesis, Université de Neuchatel, Neuchatel
Nei M, Takahata N (1993) Effective population size, genetic diversity, and coalescence time in subdivided populations. J Mol Evol 37:240–244
Parra-Olea G, García-París M, Wake DB (2004) Molecular diversification of salamanders of the tropical American genus Bolitoglossa (Caudata: Plethodontidae) and its evolutionary and biogeographical implications. Biol J Linn Soc 81:325–346
Pinot S, Ramstein G, Harrison SP, Prentice IC, Guiot J, Stute M, Joussaume S et al (1999) Tropical paleoclimates at the last glacial maximum: comparison of Paleoclimate Modeling Intercomparison Project (PMIP) simulations and paleodata. Clim Dyn 15:857–874
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256
Pybus OG, Charleston MA, Gupta S, Rambaut A, Holmes EC, Harvey PH (2001) The epidemic behavior of the hepatitis C virus. Science 292:2323–2325
Qi D, Guo S, Zhao X, Yang J, Tang W (2007) Genetic diversity and historical population structure of Schizopygopsis pylzovi (Teleostei: Cyprinidae) in the Qinghai–Tibetan Plateau. Freshw Biol 52:1090–1104
Qian H, Ricklefs RE (2000) Large-scale processes and the Asian bias in temperate plant species diversity. Nature 407:180–182
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
Rambaut A, Drummond AJ (2007) Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer
Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86
Richards CL, Carstens BC, Knowles LL (2007) Distribution modelling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographical hypotheses. J Biogeogr 34:1833–1845
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Rogers AR, Fraley AE, Bamshad MJ, Watkins WS, Jorde LB (1996) Mitochondrial mismatch analysis is insensitive to the mutational process. Mol Biol Evol 13:895–902
Ronquist FR, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rost KT (1994) Paleoelimatic field studies in and along the Qinling Shan (Central China). GeoJournal 34(1):107–120
Schwarz GE (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464
Shi YF (2002) Characteristics of late quaternary monsoonal glaciation on the Tibetan Plateau and in East Asia. Quatern Int 97(98):79–91
Shi YF (2007) The Pleistocene glaciation of China and environmental change. Henan Science and Technology Publishing House, Zhengzhou
Shi YF, Li JJ, Li BY (1998) Uplift and environmental changes of Qinghai–Tibetan plateau in the Late Cenozoic. Guangdong Science and Technology Press, Guangzhou
Shi YF, Li JJ, Li BY et al (1999) Uplift of the Qinghai–Xizang (Tibetan) Plateau and East Asia environmental change during late Cenozoic. Acta Geogr Sinica 54:10–20
Slatkin M, Maddison WP (1989) A cladistic measure of gene flow inferred from phylogenies of alleles. Genetics 123:603–613
Smith CI, Farrell BD (2005) Phylogeography of the longhorn cactus beetle Moneilema appressum LeConte (Coleoptera: Cerambycidae): was the differentiation of the Madrean sky islands driven by Pleistocene climate changes? Mol Ecol 14:3049–3065
Song G, Qu YH, Yin ZH, Li SS, Liu NF, Lei FM (2009) Phylogeography of the Alcippe morrisonia (Aves: Timaliidae): long population history beyond late Pleistocene glaciations. BMC Evol Biol 9:143. doi:10.1186/1471-2148-9-143
Swofford D (2002) PAUP*: phylogenetic analysis using parsimony (* and other methods), 4.0th edn. Sinauer Associates, Sunderland
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595
Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction site endonuclease mapping and DNA sequence data. (III) Cladogram estimation. Genetics 132:619–633
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequences alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Wakeley J (2000) The effects of subdivision on the genetic divergence of populations and species. Evolution 54:1092–1101
Wang B, Jiang JP, Chen XH, Xie F, Zheng ZH (2007) Morphometrical study on populations of the genus Feirana (Amphibia, Anura, Ranidae). Acta Zootaxonomic Sinica 3:139–145
Wang B, Jiang JP, Xie F, Chen XH, Dubois A, Liang G, Wagner S (2009) Molecular phylogeny and genetic identification of populations of two species of Feirana frogs (Amphibia: Anura, Ranidae, Dicroglossinae, Paini) endemic to China. Zool Sci 26:500–509
Wang B, Jiang JP, Xie F, Li C (2012) Postglacial colonization of the Qinling Mountains: phylogeography of the Swelled Vent frog (Feirana quadranus). PLoS ONE 7(7):e41579. doi:10.1371/journal.pone.0041579
Weisrock DW, Macey JR, Ugurtas IH, Larson A, Papenfuss TJ (2001) Molecular phylogenetics and historical biogeography among salamandrids of the “true” salamander clade: rapid branching of numerous highly divergent lineages in Mertensiella luschani associated with the rise of Anatolia. Mol Phylogenet Evol 18:434–448
Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Syst 36:519–539
Wright S (1943) Isolation by genetics. Genetics 28:114–138
Yang J (2007) Study on the ecology and embryonic development of Feirana taihangnicus [DM]. Graduate School of Henan Normal University, Xinxiang
Yang X (2011) Speciation and geographic distribution pattern of the genus Feirana [M]. Chengdu Institute of biology, Chinese Academy of Sciences, Sichuan
You Y, Sun KP, Xu LJ, Wang L, Jiang TL, Liu S, Lu GJ, Berquist SW, Feng J (2010) Pleistocene glacial cycle effects on the phylogeography of the Chinese endemic bat species, Myotis davidii. BMC Evol Biol 10:208. http://www.biomedcentral.com/1471-2148/10/208
Yu G, Gui F, Shi Y, Zheng Y (2007) Late marine isotope stage 3 palaeoclimate for East Asia: a data–model comparison. Palaeogeogr Palaeoclimatol Palaeoecol 250:167–183
Yuan JH, Cheng FY, Zhou SL (2012) Genetic structure of the tree Peony (Paeonia rockii) and the Qinling Mountains as a geographic barrier driving the fragmentation of a large population. PLoS ONE 7(4):e34955. doi:10.1371/journal.pone.0034955
Zhang RZ (1999) Zoogeography of China. Science Press, Beijing
Zhang RZ (2004) Relict distribution of land vertebrates and quaternary glaciation in China. Acta Zool Sinica 50:841–851
Zhang PZ, Zheng DW, Yin GM, Yuan DY, Zhang GL, Li CY, Wang ZC (2006) Discussion on late Cenozoic growth and rise of northeastern margin of the Tibetan plateau. Quat Sci 26(1):5–13
Zhang H, Yan J, Zhang GQ, Zhou KY (2008) Phylogeography and demographic history of Chinese black-spotted frog populations (Pelophylax nigromaculata): evidence for independent refugia expansion and secondary contact. BMC Evol Biol 8:21
Zheng B, Rutter N (1998) On the problem of quaternary glaciations, and the extent and patterns of Pleistocene cover in the Qinghai–Xizang (Tibet) plateau. Quat Int 45(46):109–122
Zhou HY (2000) Environmental events and catastrophes from the end of early pleistocene to the early stage of middle pleistocene. J Nat Disasters 9:123–129
Acknowledgments
We are grateful to Gang Liang, Xiaohong Chen, Junhua Hu, Xin Yang, and Rongchuan Xiong for their help in the collection of samples. Also thanks to JinZhong Fu from University of Guelph and Li Ding for polishing this manuscript. This study was supported by the National Natural Sciences Foundation of China (NSFC-31071906 and NSFC-31270568 granted to Jianping Jiang, NSFC-31172055 to Cheng Li, and NSFC-31201702 to Bin Wang), the field front project of the knowledge innovation program of CAS (KSCX2-EW-J-22, Y1C2021200, Y1B3021), and Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization in CIB of CAS and Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
239_2013_9544_MOESM1_ESM.xls
Table S1 Number of shared haplotypes for each pair of the 17 sampled populations of Feirana taihangnica. Populations 1–17 were given in Table 1. (XLS 26 kb)
239_2013_9544_MOESM2_ESM.xls
Table S2 Fst among the 17 sampled populations of Feirana taihangnica. Populations 1–17 were given in Table 1. * P > 0.05. (XLS 29 kb)
239_2013_9544_MOESM3_ESM.xls
Table S3 Fst among groups in different grouping arrangements according to phylogenetic arrays and geographic occurrences for populations of Feirana taihangnica. All P < 0.01. (XLS 27 kb)
Rights and permissions
About this article
Cite this article
Wang, B., Jiang, J., Xie, F. et al. Phylogeographic Patterns of mtDNA Variation Revealed Multiple Glacial Refugia for the Frog Species Feirana taihangnica Endemic to the Qinling Mountains. J Mol Evol 76, 112–128 (2013). https://doi.org/10.1007/s00239-013-9544-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-013-9544-5