Tree Genetics & Genomes

, 13:100 | Cite as

Allopatric divergence, demographic history, and conservation implications of an endangered conifer Cupressus chengiana in the eastern Qinghai-Tibet Plateau

  • Ting-Ting Xu
  • Qian Wang
  • Matthew S. Olson
  • Zhong-Hu Li
  • Ning Miao
  • Kang-Shan Mao
Original Article
First Online:
Received:
Revised:
Accepted:
Part of the following topical collections:
  1. Gene Conservation

Abstract

Isolation and demographic history are key factors that affect lineage divergence of tree species in topographic complex areas, such as the Qinghai-Tibet Plateau (QTP), yet few studies have evaluated these factors in a coalescent-based modeling framework. In the present study, we surveyed ten nuclear DNA sequence loci (nDNA) and six nuclear microsatellite loci (nSSR) for an endangered conifer, Cupressus chengiana, throughout its natural range in the eastern QTP. BARRIER analyses revealed a strong genetic barrier between Gansu and Sichuan populations of C. chengiana, and isolation with migration models detected limited gene flow between them, supporting the division of this species into two evolutionary significant units (ESUs). Two independent coalescent-based approaches suggest a Quaternary divergence between ESUs, their consensus age range ((0.09–) 0.59–1.53 (–2.71) Mya) largely overlaps with the time period when the largest glaciation occurred in the QTP. Both demographic inferences, IMa2 and DIYABC, suggest that both ESUs may have experienced a bottleneck or population contraction event during the late Quaternary. A documented massive recent anthropogenic habitat loss and fragmentation may have led to further decrease of the natural distribution of this conifer. We propose that the conservation and management of both natural stands and plantations of C. chengiana should be reconsidered in the light of our findings.

Keywords

Approximate Bayesian computation (ABC) Genetic diversity Microsatellite Evolutionary significant units (ESU) Qinghai-Tibet Plateau (QTP) 
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Notes

Acknowledgements

The authors thank Dr. Felix Gugerli and four anonymous reviewers for their constructive comments, Dr. Jianquan Liu for his constructive suggestions, and Liqiang Fan and Honglei Zheng for their help with data analyses. This work was financially supported by the Major Program of National Natural Science Foundation of China (grant 31590821), the National Basic Research Program of China (grant 2014CB954100), the National Natural Science Foundation of China (grant 31370261, 31622015), Sichuan Provincial Department of Science and Technology (grant 2015JQ0018), and Sichuan University.

Compliance with ethical standards

The authors declare that all experiments described herein comply with the law of government in which they were carried out.

Data archiving statement

Nuclear microsatellite (nSSR) genotype data are available at Research Gate (www.researchgate.net) (http://doi.org/10.13140/RG.2.1.3709.1926), and nuclear DNA sequences have been deposited in the NCBI GenBank (accession no. KU377363–KU377433).

Conflict of interest

The authors declare that they have no competing interest.

Supplementary material

11295_2017_1183_MOESM1_ESM.pdf (9 mb)
ESM 1 (PDF 9221 kb)

References

  1. Bagnoli F, Vendramin GG, Buonamici A, Doulis AG, González-Martínez SC, La Porta N, Magri D, Raddi P, Sebastiani F, Fineschi S (2009) Is Cupressus sempervirens native in Italy? An answer from genetic and palaeobotanical data. Mol Ecol 18:2276–2286CrossRefPubMedGoogle Scholar
  2. Beaumont MA (2010) Approximate Bayesian computation in evolution and ecology. Annu Rev Ecol Evol Syst 41:379–406CrossRefGoogle Scholar
  3. Beaumont M, Zhang W, Balding D (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035PubMedPubMedCentralGoogle Scholar
  4. Beaumont MA, Nielsen R, Robert C, Hey J, Gaggiotti O, Knowles L, Estoup A, Panchal M, Corander J, Hickerson M, Sisson SA, Fagundes N, Chikhi L, Beerli P, Vitalis R, Cornuet JM, Huelsenbeck J, Foll M, Yang ZH, Rousset F, Balding D, Excoffier L (2010) In defence of model-based inference in phylogeography reply. Mol Ecol 19:436–446CrossRefGoogle Scholar
  5. Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773PubMedPubMedCentralGoogle Scholar
  6. Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin JM, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189CrossRefPubMedGoogle Scholar
  10. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295CrossRefPubMedGoogle Scholar
  11. Csilléry K, Blum MGB, Gaggiotti OE, François O (2010) Approximate Bayesian computation (ABC) in practice. Trends Ecol Evol 25:410–418CrossRefPubMedGoogle Scholar
  12. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772CrossRefPubMedPubMedCentralGoogle Scholar
  13. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510CrossRefPubMedGoogle Scholar
  14. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  15. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  16. Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  18. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567CrossRefGoogle Scholar
  19. Favre A, Packert M, Pauls SU, Jahnig 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 90:236–253CrossRefPubMedGoogle Scholar
  20. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  21. Freeland JR, Kirk H, Petersen SD (2011) Molecular ecology. Wiley, West SussexCrossRefGoogle Scholar
  22. Fu LK (1992) Red book of China: rare and threatened plants. Science Press, BeijingGoogle Scholar
  23. Fu LK, Yu YF, Farjon A (1999) Cupressaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 4. Science Press & Missouri Botanical Garden Press, Beijing pp 62–77Google Scholar
  24. Fujimoto A, Kado T, Yoshimaru H, Tsumura Y, Tachida H (2008) Adaptive and slightly deleterious evolution in a conifer, Cryptomeria japonica. J Mol Evol 67:201–210CrossRefPubMedGoogle Scholar
  25. Hamilton MB (2009) Population genetics. Wiley, West SussexGoogle Scholar
  26. Hao BQ, Li W, Mu LC, Li Y, Rui Z, Tang MX, Bao WK (2006) A study of conservation genetics in Cupressus chengiana, an endangered endemic of China, using ISSR markers. Biochem Genet 44:29–43CrossRefGoogle Scholar
  27. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  28. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond Ser B Biol Sci 359:183–195CrossRefGoogle Scholar
  29. Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920CrossRefPubMedGoogle Scholar
  30. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH, Johnson JB, Rissler L, Victoriano PF, Yoder AD (2010) Phylogeography's past, present, and future: 10 years after Avise, 2000. Mol Phylogenet Evol 54:291–301CrossRefPubMedGoogle Scholar
  32. Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartin I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Sarkinen T, Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931CrossRefPubMedGoogle Scholar
  33. IUCN (2012) IUCN red list categories and criteria: version 3.1. IUCN, GlandGoogle Scholar
  34. IUCN (2016) Cupressus chengiana var. chengiana. In: The IUCN red list of threatened species, version 2016.3. Available at  https://doi.org/10.2305/IUCN.UK.2013-1.RLTS.T32478A2820376.en. Accessed 16 Dec 2016
  35. Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602CrossRefPubMedGoogle Scholar
  36. Jia D-R, Liu T-L, Wang L-Y, Zhou D-W, Liu J-Q (2011) Evolutionary history of an alpine shrub Hippophae tibetana (Elaeagnaceae): allopatric divergence and regional expansion. Biol J Linn Soc 102:37–50CrossRefGoogle Scholar
  37. Kado T, Matsumoto A, Ujino-Ihara T, Tsumura Y (2008) Amounts and patterns of nucleotide variation within and between two Japanese conifers, sugi (Cryptomeria japonica) and hinoki (Chamaecyparis obtusa) (Cupressaceae sensu lato). Tree Genet Genomes 4:133–141CrossRefGoogle Scholar
  38. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191CrossRefPubMedPubMedCentralGoogle Scholar
  39. Li HW, Li J (1993) A preliminary floristic study on the seed plants from the region of Hengduan Mountain. Act Bot Yunn 15:217–231Google Scholar
  40. Li JJ., Wen SX, Zhang QS, Wang FB, Zheng BX, Li BY (1979) A discussion on the period, amplitude and type of the uplift of the Qinghai-Xizang (Tibetan) Plateau. Sci Sin 22:1314–1328Google Scholar
  41. Li JJ, Shi YF, Li BY (1995) Uplift of the Qinghai-Xizang (Tibet) Plateau and global change. Lanzhou University Press, LanzhouGoogle Scholar
  42. Li Y, Stocks M, Hemmilä S, Källman T, Zhu H, Zhou Y, Chen J, Liu J, Lascoux M (2010) Demographic histories of four spruce (Picea) species of the Qinghai-Tibetan Plateau and neighboring areas inferred from multiple nuclear loci. Mol Biol Evol 27:1001–1014CrossRefPubMedGoogle Scholar
  43. Li ZH, Zhang Q, Liu JQ, Källman T, Lascoux M (2011) The Pleistocene demography of an alpine juniper of the Qinghai-Tibetan Plateau: tabula rasa, cryptic refugia or something else? J Biogeogr 38(1):31–43CrossRefGoogle Scholar
  44. Li ZH, Zou JB, Mao KS, Lin K, Li HP, Liu JQ, Kallman T, Lascoux M (2012) Population genetic evidence for complex evolutionary histories of four high altitude juniper species in the Qinghai-Tibetan Plateau. Evolution 66:831–845CrossRefPubMedGoogle Scholar
  45. Li L, Abbott RJ, Liu B, Sun Y, Li L, Zou J, Wang X, Miehe G, Liu J (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 22:5237–5255CrossRefPubMedGoogle Scholar
  46. Li JJ, Fang XM, Song CH, Pan BT, Ma YZ, Yan MD (2014) Late Miocene-Quaternary rapid stepwise uplift of the NE Tibetan Plateau and its effects on climatic and environmental changes. Quat Res 81:400–423CrossRefGoogle Scholar
  47. Li LL, Sun YS, Zou JB, Yue W, Wang X, Liu JQ (2015) Origin and speciation of Picea schrenkiana and Picea smithiana in the center Asian highlands and Himalayas. Plant Mol Biol Rep 33:661–672CrossRefPubMedGoogle Scholar
  48. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  49. Liu JQ, Gao TG, Chen ZD, Lu AM (2002) Molecular phylogeny and biogeography of the Qinghai-Tibet Plateau endemic Nannoglottis (Asteraceae). Mol Phylogenet Evol 23:307–325CrossRefPubMedGoogle Scholar
  50. Liu JQ, Wang YJ, Wang AL, Hideaki O, Abbott RJ (2006) Radiation and diversification within the Ligularia-Cremanthodium-Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Mol Phylogenet Evol 38:31–49CrossRefPubMedGoogle Scholar
  51. Liu J-Q, Sun Y-S, Ge X-J, Gao L-M, Qiu Y-X (2012) Phylogeographic studies of plants in China: advances in the past and directions in the future. J Syst Evol 50:267–275CrossRefGoogle Scholar
  52. Liu J, Möller M, Provan J, Gao LM, Poudel RC, Li DZ (2013) Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot. New Phytol 199:1093–1108CrossRefPubMedGoogle Scholar
  53. Lu X, Xu HY, Li ZH, Shang HY, Adams RP, Mao KS (2014) Genetic diversity and conservation implications of four Cupressus species in China as revealed by microsatellite markers. Biochem Genet 52:181–202CrossRefPubMedGoogle Scholar
  54. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  55. Luo D, Feng Q-H, Shi Z-M, Li D-S, Yang C-X, Liu Q-L, He J-S (2015) Dynamics of carbon and nitrogen storage of Cupressus chengiana plantations in the arid valley of Minjiang River, Southwest China. Chinese J Appl Ecol 26:1099–1105Google Scholar
  56. Ma Y-Z, Li Z-H, Wang X, Shang B-L, Wu G-L, Wang Y-J (2014) Phylogeography of the genus Dasiphora (Rosaceae) in the Qinghai-Tibetan Plateau: divergence blurred by expansion. Biol J Linn Soc 111:777–788CrossRefGoogle Scholar
  57. 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 76:173–190CrossRefPubMedGoogle Scholar
  58. Mao KS, Hao G, Liu JQ, Adams RP, Milne RI (2010) Diversification and biogeography of Juniperus (Cupressaceae): variable diversification rates and multiple intercontinental dispersals. New Phytol 188:254–272CrossRefPubMedGoogle Scholar
  59. Marko PB, Hart MW (2011) The complex analytical landscape of gene flow inference. Trends Ecol Evol 26:448–456CrossRefPubMedGoogle Scholar
  60. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  61. Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L, Guillemaud T (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992–992CrossRefPubMedGoogle Scholar
  62. Moritz CC (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375CrossRefPubMedGoogle Scholar
  63. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  64. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefPubMedGoogle Scholar
  65. O’Connell LM, Ritland K, Thompson SL (2008) Patterns of postglacial colonization by western redcedar (Thuja plicata, Cupressaceae) as revealed by microsatellite markers. Botany 86:194–203CrossRefGoogle Scholar
  66. Opgenoorth L, Vendramin GG, Mao K, Miehe G, Miehe S, Liepelt S, Liu J, Ziegenhagen B (2010) Tree endurance on the Tibetan Plateau marks the world’s highest known tree line of the Last Glacial Maximum. New Phytol 185:332–342CrossRefPubMedGoogle Scholar
  67. Pandey M, Rajora OP (2012) Genetic diversity and differentiation of core vs. peripheral populations of eastern white cedar, Thuja occidentalis (Cupressaceae). Am J Bot 99:690–699CrossRefPubMedGoogle Scholar
  68. Pascual M, Chapuis MP, Mestres F, Balanya J, Huey RB, Gilchrist GW, Serra L, Estoup A (2007) Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods. Mol Ecol 16:3069–3083CrossRefPubMedGoogle Scholar
  69. Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  70. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  71. Qiu Y-X, Fu C-X, 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 59:225–244CrossRefPubMedGoogle Scholar
  72. Rosenberg NA (2003) The shapes of neutral gene genealogies in two species: probabilities of monophyly, paraphyly, and polyphyly in a coalescent model. Evolution 57:1465–1477CrossRefPubMedGoogle Scholar
  73. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  74. Rovito SM (2010) Lineage divergence and speciation in the web-toed salamanders (Plethodontidae: Hydromantes) of the Sierra Nevada, California. Mol Ecol 19:4554–4571CrossRefPubMedGoogle Scholar
  75. Shang HY, Li ZH, Dong M, Adams RP, Miehe G, Opgenoorth L, Mao KS (2015) Evolutionary origin and demographic history of an ancient conifer (Juniperus microsperma) in the Qinghai-Tibetan Plateau. Sci Rep-UK 5:10216CrossRefGoogle Scholar
  76. Shi YF, Li JJ, Li BY (1998) Uplift and environmental changes of Qinghai-Tibetan Plateau in the late Cenozoic. Guangdong Science and Technology Press, GuangzhouGoogle Scholar
  77. Sobel JM, Chen GF, Watt LR, Schemske DW (2010) The biology of speciation. Evolution 64:295–315CrossRefPubMedGoogle Scholar
  78. Sun BN, Wu JY, Liu YS, Ding ST, Li XC, Xie SP, Yan DF, Lin ZC (2011) Reconstructing Neogene vegetation and climates to infer tectonic uplift in western Yunnan, China. Palaeogeogr Palaeocl 304:328–336CrossRefGoogle Scholar
  79. Sun Y-S, Wang A-L, Wan D-S, Wang Q, Liu J-Q (2012) Rapid radiation of Rheum (Polygonaceae) and parallel evolution of morphological traits. Mol Phylogenet Evol 63:150–158CrossRefPubMedGoogle Scholar
  80. 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 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  81. Tani N, Tsumura Y, Sato H (2003) Nuclear gene sequences and DNA variation of Cryptomeria japonica samples from the postglacial period. Mol Ecol 12:859–868CrossRefPubMedGoogle Scholar
  82. Tsumura Y, Suyama Y, Yoshimura K, Shirato N, Mukai Y (1997) Sequence-tagged-sites (STSs) of cDNA clones in Cryptomeria japonica and their evaluation as molecular markers in conifers. Theor Appl Genet 94:764–772CrossRefGoogle Scholar
  83. Wakeley J (2009) Coalescent theory. Roberts and Company Publishers, Greenwood VillageGoogle Scholar
  84. Wang LY, Abbott RJ, Zheng W, Chen P, Wang YJ, Liu JQ (2009a) History and evolution of alpine plants endemic to the Qinghai-Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae). Mol Ecol 18:709–721CrossRefPubMedGoogle Scholar
  85. Wang YJ, Susanna A, Raab-straube EV, Milne RI, Liu JQ (2009b) Island-like radiation of Saussurea (Asteraceae: Cardueae) triggered by uplifts of the Qinghai-Tibetan Plateau. Biol J Linn Soc 97:893–903CrossRefGoogle Scholar
  86. Wang H, Laqiong, Sun K, Lu F, Wang Y, Song Z, Wu Q, Chen J, Zhang W (2010) Phylogeographic structure of Hippophae tibetana (Elaeagnaceae) highlights the highest microrefugia and the rapid uplift of the Qinghai-Tibetan Plateau. Mol Ecol 19:2964–2979CrossRefPubMedGoogle Scholar
  87. Wen J, Zhang JQ, Nie ZL, Zhong Y, Sun H (2014) Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Front Genet 5:4PubMedPubMedCentralGoogle Scholar
  88. Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: Fst ≠ 1/(4Nm+1). Heredity 82:117–125CrossRefPubMedGoogle Scholar
  89. Willyard A, Syring J, Gernandt DS, Liston A, Cronn R (2007) Fossil calibration of molecular divergence infers a moderate mutation rate and recent radiations for Pinus. Mol Biol Evol 24:90–101CrossRefPubMedGoogle Scholar
  90. Wu CY (1988) Hengduan Mountains flora and her significance. J Jap Bot 63:297–311Google Scholar
  91. Wu SG, Yang YP, Fei Y (1995) On the flora of the alpine region in the Qinghai-Xizang (Tibet) Plateau. Act Bot Yunn 17:233–250Google Scholar
  92. Wu LL, Cui XK, Milne RI, Sun YS, Liu JQ (2010) Multiple autopolyploidizations and range expansion of Allium przewalskianum Regel. (Alliaceae) in the Qinghai-Tibetan Plateau. Mol Ecol 19:1691–1704CrossRefPubMedGoogle Scholar
  93. Wu RD, Zhang S, Yu DW, Zhao P, Li XH, Wang LZ, Yu Q, Ma J, Chen A, Long YC (2011) Effectiveness of China’s nature reserves in representing ecological diversity. Front Ecol Environ 9:383–389CrossRefGoogle Scholar
  94. Wu Z-X, Xu H, Liang P, Bai P, Xiong L (2012) Experiment on planting of green manure under the young growths of Cupressus chengiana S. Y. Hu in the arid valleys of the upper reaches of the Minjiang River. J Sichuan For Sci Technol 33:53–57Google Scholar
  95. Xu T, Abbott R, Milne R, Mao K, Du F, Wu G, Ciren Z, Miehe G, Liu J (2010) Phylogeography and allopatric divergence of cypress species (Cupressus L.) in the Qinghai-Tibetan Plateau and adjacent regions. BMC Evol Biol 10:194CrossRefPubMedPubMedCentralGoogle Scholar
  96. Yang FS, Li YF, Ding X, Wang XQ (2008) Extensive population expansion of Pedicularis longiflora (Orobanchaceae) on the Qinghai-Tibetan Plateau and its correlation with the Quaternary climate change. Mol Ecol 17:5135–5145CrossRefPubMedGoogle Scholar
  97. Zeng PA, Yang QZ (1992) Minjiang cypress forest. China Forestry Press, BeijingGoogle Scholar
  98. Zhang YL, Li BY, Zheng D (2002) A discussion on the boundary and area of the Tibetan Plateau in China. Geogr Res 21:1–8Google Scholar
  99. Zhang Q, Chiang TY, George M, Liu JQ, Abbott RJ (2005) Phylogeography of the Qinghai-Tibetan Plateau endemic Juniperus przewalskii (Cupressaceae) inferred from chloroplast DNA sequence variation. Mol Ecol 14:3513–3524CrossRefPubMedGoogle Scholar
  100. Zheng D (1996) The system of physico-geographical regions of the Qinghai-Tibet (Xizang) Plateau. Sci China Ser D 39:410–417Google Scholar
  101. Zheng BX, Xu QQ, Shen YP (2002) The relationship between climate change and Quaternary glacial cycles on the Qinghai-Tibetan Plateau: review and speculation. Quatern Int 97-98:93–101CrossRefGoogle Scholar
  102. Zhou SZ, Li JJ (1998) The sequence of Quaternary glaciation in the Bayan Har Mountains. Quatern Int 45-46:135–142CrossRefGoogle Scholar
  103. Zhou SZ, Wang XL, Wang J, Xu LB (2006) A preliminary study on timing of the oldest Pleistocene glaciation in Qinghai-Tibetan Plateau. Quat Int 154–155:44–51Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Ting-Ting Xu
    • 1
    • 2
  • Qian Wang
    • 1
    • 3
  • Matthew S. Olson
    • 4
  • Zhong-Hu Li
    • 5
  • Ning Miao
    • 1
  • Kang-Shan Mao
    • 1
  1. 1.Key Laboratory of Bio-resources and Eco-environment, Ministry of Education, College of Life SciencesSichuan UniversityChengduChina
  2. 2.School of Life ScienceNingxia UniversityYinchuanChina
  3. 3.Key Laboratory of Oral Diseases Research, Research Center for Medicine & BiologyZunyi Medical UniversityZunyiChina
  4. 4.Department of Biological SciencesTexas Tech UniversityLubbockUSA
  5. 5.Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life SciencesNorthwest UniversityXi’anChina

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