Abstract
Yunnan Plateau and its adjacent areas (YPA) with typical subtropical evergreen broad-leaved forests (SEBF) have a rich number of vascular plants and high endemism. However, how ancient geological and climatic events in YPA have shaped the SEBF remains poorly understood. In this study, we integrated multilocus phylogeography, species distribution models (SDMs), and regression analysis to investigate the effects of paleoenvironmental changes on the contemporary genetic patterns of Quercus schottkyana, an endemic and dominant evergreen oak in the YPA. A total of 380 samples were taken from 29 populations, covering the natural geographical distribution of Q. schottkyana. Molecular dating indicated that haplotype divergence began at late Miocene; this finding supported the hypothesis that major uplifting of YPA occurred after late Miocene, which led to the speciation and divergence of Q. schottkyana. Unlike previous biome reconstruction studies based on palynology data, our SDM analysis indicated that the distribution ranges of Q. schottkyana was comparatively stable after the Last Glacial Maximum (LGM) and experienced only a slight northward expansion afterward. Species genetic diversity showed a significant negative correlation to the habitat stability using regression analysis. These analyses suggested the admixture of individuals from genetically differentiated populations in the unstable habitats, which in turn increased the genetic diversity of Q. schottkyana. We also found that climate gradient along the latitude cline influenced the genetic structure of Q. schottkyana. This study provides new insights into the understanding of the evolutionary history of SEBF in YPA.
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 et al (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst:489–522
Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29:2157–2167
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Burger R, Lynch M (1995) Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution:151–163
Chen LY (1984) On the characteristic of paleoclimate by spore-pollen assemblages from the North edge of Dianchi Lake of Kunming Basin in Quaternary. Bulletin of the Chengdu Institute of Geology and Mineral Resources, The Chinese Academy of Geological Sciences 5:93–107
Clark M et al (2004) Surface uplift, tectonics, and erosion of eastern Tibet from large-scale drainage patterns. Tectonics 23
Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438
Dao KQ et al (2013) A new material of Lindera (Lauraceae) of the Late Pliocene from Tengchong, Yunnan and the genus’ biogeography significance. Acta Geol Sin-Engl 87:690–706
Davis MB, Shaw RG, Etterson JR (2005) Evolutionary responses to changing climate. Ecology 86:1704–1714
Deng M, Zhou ZK, Li Q (2013) Taxonomy and systematics of Quercus subgenus Cyclobalanopsis. Int Oaks 24:48–60
Deng M, Hipp A, Song Y-G, Li Q-S, Coombes A, Cotton A (2014) Leaf epidermal features of Quercus subgenus Cyclobalanopsis (Fagaceae) and their systematic significance. Bot J Linnean Soc 176:224–259
Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973
Eaton DA, Hipp AL, González-Rodríguez A, Cavender-Bares J (2015) Historical introgression among the American live oaks and the comparative nature of tests for introgression. Evolution 69:2587–2601
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
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 10:564–567
Favre A, Päckert M, Pauls SU, Jähnig SC, Uhl D, Michalak I, Muellner-Riehl AN (2015) The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biol Rev 90:236–253
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gao H, Williamson S, Bustamante CD (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176:1635–1651
Gugger PF, Ikegami M, Sork VL (2013) Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata Née. Mol Ecol 22:3598–3612
Guo SX (1978) Pliocene floras of Western Sichuan. Acta Palaeontol Sin 17:343–349
Guo SX (2011) The late Miocene Bangmai flora from Lincang county of Yunnan, southwestern China. Acta Palaeontol Sin 50:353–408
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Harrison TM, Copeland P, Kidd W, Yin A (1992) Raising tibet. Science 255:1663–1670
Harrison SP, Yu G, Takahara H, Prentice IC (2001) Palaeovegetation (communications arising): diversity of temperate plants in east Asia. Nature 413:129–130
He D, Chen Y (2006) Biogeography and molecular phylogeny of the genus Schizothorax (Teleostei: Cyprinidae) in China inferred from cytochrome b sequences. J Biogeogr 33:1448–1460
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Jia H, Sun BN, Li XC, Xiao L, Wu JY (2009) Microstructures of one species of Quercus from the Neogene in Eastern Zhejiang and its palaeoenvironmental indication. Earth Sci Front 16:79–90
Jiang XZ, Yang XD, Wang SM (2002) Pollen records and environmental evolution of Heqing Basin in Yunnan province since 1.0 Ma. Mar Geol Quat Geol 22:99–104
Jiménez-Valverde A, Lobo JM (2007) Threshold criteria for conversion of probability of species presence to either–or presence–absence. Acta Oecol 31:361–369
Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189
Li XW, Li J (1997) The Tanaka-Kaiyong line-an important floristic line for the study of the flora of East Asia. Ann Mo Bot Gard 84:888–892
Li N, Sun B, Wu J, Yan D, Xiao L, Dai J (2009) Cuticular structure of Quercus presenescens from the Pliocene in Baoshan, Yunnan, and its palaeoclimatic implications. Acta Palaeontol Sin 48:654–661
Li Y, Yan HF, Ge XJ (2012) Phylogeographic analysis and environmental niche modeling of widespread shrub Rhododendron simsii in China reveals multiple glacial refugia during the last glacial maximum. J Syst Evol 50:362–373
Li L et al (2013) Pliocene intraspecific divergence and Plio-Pleistocene range expansions within Picea likiangensis (Lijiang spruce), a dominant forest tree of the Qinghai-Tibet Plateau. Mol Ecol 22:5237–5255
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Liu KB (1988) Quaternary history of the temperate forests of China. Quaternary Sci Rev 7:1–20
Liu YF, Wang Y, Huang HW (2009) Species-level phylogeographical history of Myricaria plants in the mountain ranges of western China and the origin of M. laxiflora in the Three Gorges mountain region. Mol Ecol 18:2700–2712
López-Pujol J, Zhang FM, Sun HQ, Ying TS, Ge S (2011) Centres of plant endemism in China: places for survival or for speciation? J Biogeogr 38:1267–1280
Luo Y, Zhou ZK (2000) Phytogeography of Quercus subg. Cyclobalanopsis. Acta Bot Yunnanica 23:1–16
Marcott SA, Shakun JD, Clark PU, Mix AC (2013) A reconstruction of regional and global temperature for the past 11,300 years. Science 339:1198–1201
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Ortego J, Riordan EC, Gugger PF, Sork VL (2012) Influence of environmental heterogeneity on genetic diversity and structure in an endemic southern Californian oak. Mol Ecol 21:3210–3223
Ortego J, Gugger PF, Riordan EC, Sork VL (2014) Influence of climatic niche suitability and geographical overlap on hybridization patterns among southern Californian oaks. J Biogeogr 41:1895–1908
Ortego J, Gugger PF, Sork VL (2015) Climatically stable landscapes predict patterns of genetic structure and admixture in the Californian canyon live oak. J Biogeogr 42:328–338
Petit RJ et al (2002) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol Manag 156:49–74
Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Qin Y, Fei AW, Jin KL (1992) Late Pleistocene sporopollen assemblages and evolution of palaeovegetation, palaeoclimate and palaeoenvironments in Tengchong Basin, western Yunnan. Mar Geol Quat Geol 12:109–118
Qin AL, Wang MM, Cun YZ, Yang FS, Wang SS, Ran JH, Wang XQ (2013) Phylogeographic evidence for a link of species divergence of Ephedra in the Qinghai-Tibetan Plateau and adjacent regions to the Miocene Asian aridification. PLoS One 8:e56243
Qiu YX, Fu CX, Comes HP (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Mol Phylogenet Evol 59:225–244
Shen J, Jones RT, Yang XD, Dearing JA, Wang SM (2006) The Holocene vegetation history of Lake Erhai, Yunnan province southwestern China: the role of climate and human forcings. The Holocene 16:265–276
Shi YF, Ren BH, Wang JT, Derbyshire E (1986) Quaternary glaciation in China. Quaternary Sci Rev 5:503–507
Shi MM, Michalski SG, Welk E, Chen XY, Durka W (2014) Phylogeography of a widespread Asian subtropical tree: genetic east–west differentiation and climate envelope modelling suggest multiple glacial refugia. J Biogeogr 41:1710–1720
Sork VL, Davis FW, Westfall R, Flint A, Ikegami M, Wang HF, Grivet D (2010) Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Née) in the face of climate change. Mol Ecol 19:3806–3823
Sun BN et al (2011) Reconstructing Neogene vegetation and climates to infer tectonic uplift in western Yunnan, China. Palaeogeogr Palaeocl 304:328–336
Swoford D (2000) Phylogenetic analysis using parsimony (* and other methods).
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tanaka T (1954) Species problem in Citrus Tokyo: Japanese Society for the Promotion of Science
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tian B, Zhou ZL, Du FK, He CZ, Xin PY, Ma HC (2015) The Tanaka Line shaped the phylogeographic pattern of the cotton tree (Bombax ceiba) in Southwest China. Biochem Syst Ecol 60:150–157
TLand J, Putten WF, Villarroel H, Kamping A, Delden WV (2000) Latitudinal variation for two enzyme loci and an inversion polymorphism in Drosophila melanogaster from central and South America. Evolution 54:201–209
Wang BS, Mao JF, Zhao W, Wang XR (2013) Impact of geography and climate on the genetic differentiation of the subtropical pine Pinus yunnanensis. PLoS One 8:e67345
Willyard A, Cronn R, Liston A (2009) Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Mol Phylogenet Evol 52:498–511
Wright S (1943) Isolation by distance. Genetics 28:114
Wu ZY (1979) The regionalization of Chinese flora. Acta Bot Yunn 1:1–22
Wu ZY, Raven PH (1999) Flora of China. Vol. 4 (Cycadaceae through Fagaceae) Sci Press, Beijing
Xia K, Su T, Liu YSC, Xing YW, Jacques FM, Zhou ZK (2009) Quantitative climate reconstructions of the late Miocene Xiaolongtan megaflora from Yunnan, southwest China. Palaeogeogr Palaeocl 276:80–86
Xie WG, Lewis PO, Fan Y, Kuo L, Chen MH (2011) Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol 60:150–160
Xing YW et al (2013) A new Quercus species from the upper Miocene of southwestern China and its ecological significance. Rev Palaeobot Palyno 193:99–109
Xu J, Deng M, Jiang XL, Westwood M, Song YG, Turkington R (2015) Phylogeography of Quercus glauca (Fagaceae), a dominant tree of East Asian subtropical evergreen forests, based on three chloroplast DNA interspace sequences. Tree Genet Genomes 11:1–17
Xu YL, Woeste K, Cai NH, Kang XY, Li GQ, Chen S, Duan AA (2016) Variation in needle and cone traits in natural populations of Pinus yunnanensis. J For Res 27:41–49
Yan F et al (2013) Geological events play a larger role than Pleistocene climatic fluctuations in driving the genetic structure of Quasipaa boulengeri (Anura: Dicroglossidae). Mol Ecol 22:1120–1133
Yang YM, Tian K, Hao JM, Pei SJ, Yang YX (2004) Biodiversity and biodiversity conservation in Yunnan, China. Biodivers Conserv 13:813–826
Yu G et al (2000) Palaeovegetation of China: a pollen data-based synthesis for the mid-Holocene and last glacial maximum. J Biogeogr 27:635–664
Yue LL, Chen G, Sun WB, Sun H (2012) Phylogeography of Buddleja crispa (Buddlejaceae) and its correlation with drainage system evolution in southwestern China. Am J Bot 99:1726–1735
Zhao YJ, Gong X (2015) Genetic divergence and phylogeographic history of two closely related species (Leucomeris decora and Nouelia insignis) across the ‘Tanaka Line’ in Southwest China. BMC Evol Biol 15:134
Zhao LC, Wang YF, Liu CJ, Li CS (2004) Climatic implications of fruit and seed assemblage from Miocene of Yunnan, southwestern China. Quatern Int 117:81–89
Acknowledgments
We thank the two anonymous reviewers for constructive comments on the manuscript. We thank Dou-Dou Wang for the help on the molecular experiments. We are grateful to Yan-Shi Xiong and Yi-Gang Song for their help in the sample collection. This work was supported by grants from the National Natural Science Foundation of China (31100154 and 31270267), the Shanghai Municipal Administration of Forestation and City Appearances (G152428 and G162404, G142430, F132416, G162405), and the Science and Technology Commission of Shanghai Municipality (14DZ2260400).
Data archiving statement
The haplotype sequence of cpDNA obtained in this study has been submitted to GenBank (http://www.ncbi.nlm.nih.gov/genbank/). The accession numbers were KX714758-KX714786, KX714787-KX714802, and KX714740-KX714757 for psbA-trnH, trnT-trnL, and atpI-atpH, respectively.
Authors’ contributions
Xiao-Long Jiang and Min Deng conceived and designed the experiments and wrote and revised the paper; Xiao-Long Jiang and Ying Li performed the experiments; Xiao-Long Jiang analyzed the data; and Min Deng was responsible for field collections and specimen identification.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Kremer
Electronic supplementary material
Fig. S1
Haplotype divergence time of Quercus schottkyana calculated by BEAST v1.8 based on substitute rate. (TIFF 2193 kb)
Fig. S2
Mismatch distribution for populations of Quercus schottkyana. The black and gray lines represent the expected and observed mismatch distributions, r represents the raggedness index and p represents the significance of a simulation value greater than the observed value (TIFF 2057 kb)
Fig. S3
Distribution of delta K values in InStruct analysis (TIFF 3909 kb)
Table S1
(DOCX 16 kb)
Table S2
(DOCX 13 kb)
Table S3
(DOCX 17 kb)
Rights and permissions
About this article
Cite this article
Jiang, XL., Deng, M. & Li, Y. Evolutionary history of subtropical evergreen broad-leaved forest in Yunnan Plateau and adjacent areas: an insight from Quercus schottkyana (Fagaceae). Tree Genetics & Genomes 12, 104 (2016). https://doi.org/10.1007/s11295-016-1063-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-016-1063-2