Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot

New Phytologist

Volumn 199, Issue 4, 2013, Pages 1093-1108

  Liu, Jie ^a,b   Möller, Michael ^a,c   Provan, Jim ^d   Gao, Lian Ming ^a   Poudel, Ram Chandra ^a,b   Li, De Zhu ^a  

^a KUNMING INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Ecological differentiation; Himalaya Hengduan Mountains region; Population demography; Speciation; Species distribution modeling; Taxus wallichiana

Indexed keywords

BIODIVERSITY; CLIMATE CHANGE; CORRELATION; CRYPSIS; LAST GLACIAL; MOUNTAIN; PHYLOGEOGRAPHY; PLANT COMMUNITY; POPULATION GENETICS; POPULATION STRUCTURE; SPECIATION (BIOLOGY); TIMESCALE;

HIMALAYAS;

CHLOROPLAST DNA; MICROSATELLITE DNA;

ARTICLE; BAYES THEOREM; BIODIVERSITY; BIOLOGICAL MODEL; CHINA; CLIMATE; DNA SEQUENCE; ECOLOGICAL DIFFERENTIATION; GENETIC VARIABILITY; GENETICS; GEOGRAPHIC AND GEOLOGICAL PHENOMENA; GEOGRAPHY; HAPLOTYPE; HIMALAYA-HENGDUAN MOUNTAINS REGION; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; POPULATION DEMOGRAPHY; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; SPECIES DISTRIBUTION MODELING; TAXUS; TAXUS WALLICHIANA;

ECOLOGICAL DIFFERENTIATION; HIMALAYA-HENGDUAN MOUNTAINS REGION; POPULATION DEMOGRAPHY; SPECIATION; SPECIES DISTRIBUTION MODELING; TAXUS WALLICHIANA;

BAYES THEOREM; BIODIVERSITY; CLIMATE; DNA, CHLOROPLAST; GENETIC SPECIATION; GENETIC VARIATION; GEOGRAPHY; GEOLOGICAL PHENOMENA; HAPLOTYPES; MICROSATELLITE REPEATS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TAXUS; TIBET;

EID: 84881244468     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12336     Document Type: Article

References (102)

1. Akciz S, Burchfiel BC, Crowley JL, Yin J, Chen L. 2008. Geometry, kinematics, and regional significance of the Chong Shan shear zone, Eastern Himalayan Syntaxis, Yunnan, China. Geosphere 4: 292-314.
2. An ZS, Kutzbach JE, Prell WL, Porter SC. 2001. Evolution of Asian monsoons and phased uplift of the Himalayan-Tibetan plateau since Late Miocene times. Nature 411: 62-66.
3. Batalha-Filho H, Cabanne GS, Miyaki CY. 2012. Phylogeography of an Atlantic forest passerine reveals demographic stability through the last glacial maximum. Molecular Phylogenetics and Evolution 65: 892-902.
4. Bisconti R, Canestrelli D, Colangelo P, Nascetti G. 2011. Multiple lines of evidence for demographic and range expansion of a temperate species (Hyla sarda) during the last glaciation. Molecular Ecology 20: 5313-5327.
5. Chang Z, Xiao J, Lü L, Yao H. 2010. Abrupt shifts in the Indian monsoon during the Pliocene marked by high-resolution terrestrial records from the Yuanmou Basin in southwest China. Journal of Asian Earth Sciences 37: 166-175.
6. Comes HP, Kadereit JW. 1998. The effect of Quaternary climatic changes on plant distribution and evolution. Trends in Plant Science 3: 432-438.
7. Crawford NG. 2010. SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources 10: 556-557.
8. Cun YZ, Wang XQ. 2010. Plant recolonization in the Himalaya from the southeastern Qinghai-Tibetan Plateau: geographical isolation contributed to high population differentiation. Molecular Phylogenetics and Evolution 56: 972-982.
9. Cunha RL, Lopes EP, Reis DM, Castilho R. 2011. Genetic structure of Brachidontes puniceus populations in Cape Verde archipelago shows signature of expansion during the last glacial maximum. Journal of Molluscan Studies 77: 175-181.
10. Davis MB, Shaw RG. 2001. Range shifts and adaptive responses to Quaternary climate change. Science 292: 673-679.
11. Dieringer D, Schlötterer C. 2003. Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 3: 167-169.
12. Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W. 2002. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161: 1307-1320.
13. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
14. Dupanloup I, Schneider S, Excoffier L. 2002. A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11: 2571-2581.
15. Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611-2620.
16. Excoffier L, Lischer HEL. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564-567.
17. Falush D, Stephens M, Pritchard JK. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
18. Farjon A. 2010. A handbook of the World's conifers. Leiden, the Netherlands: Brill Academic Publishers, 983-985.
19. Florin R. 1958. On Jurassic taxads and conifers from north-western Europe and eastern Greenland. Acta Horti Bergiani 17: 257-410.
20. Fu LG, Li N, Mill RR. 1999. Taxaceae. In: Wu ZY, Peter RH, eds. Floral of China. Beijing, China: Science Press and St. Louis, MO, USA: Missouri Botanical Garden Press, 89-96.
21. Funk DJ, Nosil P, Etges WJ. 2006. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proceedings of the National Academy of Sciences, USA 103: 3209-3213.
22. Gao LM, Möller M, Zhang XM, Hollingsworth ML, Liu J, Mill RR, Gibby M, Li DZ. 2007. High variation and strong phylogeographic pattern among cpDNA haplotypes in Taxus wallichiana (Taxaceae) in China and North Vietnam. Molecular Ecology 16: 4684-4698.
23. Givnish TJ. 2010. Ecology of plant speciation. Taxon 59: 1326-1366.
24. Goudet J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). [WWW document] URL http://www2.unil.ch/popgen/softwares/fstat.htm. [Accessed on 20 March 2013].
25. Hao DC, Xiao PG, Huang BL, Ge GB, Yang L. 2008. Interspecific relationships and origins of Taxaceae and Cephalotaxaceae revealed by partitioned Bayesian analyses of chloroplast and nuclear DNA sequences. Plant Systematics and Evolution 276: 89-104.
26. Harmon LJ, Melville J, Larson A, Losos JB. 2008. The role of geography and ecological opportunity in the diversification of day geckos (Phelsuma). Systematic Biology 57: 562-573.
27. Harris TM. 1976. Two neglected aspects of fossil conifers. American Journal of Botany 63: 902-910.
28. Harrison SP, Yu G, Takahara H, Prentice IC. 2001. Diversity of temperate plants in east Asia. Nature 413: 129-130.
29. Harrison TM, Copeland P, Kidd WSF, Yin A. 1992. Raising Tibet. Science 255: 1663-1670.
30. Hedrick PW. 2005. A standardized genetic differentiation measure. Evolution 59: 1633-1638.
31. Hewitt GM. 2004. Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B 359: 183-195.
32. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.
33. Hijmans RJ, Guarino L, Cruz M, Rojas E. 2001. Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genetic Resources Newsletter 127: 15-19.
34. Hoskin CJ, Higgie M, McDonald KR, Moritz C. 2005. Reinforcement drives rapid allopatric speciation. Nature 437: 1353-1356.
35. Jia DR, Abbott RJ, Liu TL, Mao KS, Bartish IV, Liu JQ. 2012. Out of the Qinghai-Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophaë rhamnoides (Elaeagnaceae). New Phytologist 194: 1123-1133.
36. Jia DR, Liu TL, Wang LY, Zhou DW, Liu JQ. 2011. Evolutionary history of an alpine shrub Hippophaë tibetana (Elaeagnaceae): allopatric divergence and regional expansion. Biological Journal of the Linnean Society 102: 37-50.
37. Jiang X, Wang S, Yang X. 1998. Paleoclimatic and environmental changes over the last 30 000 years in Heqing Basin, Yunnan Province. Journal of Lake Sciences 10: 1-7.
38. Keller I, Seehausen O. 2012. Thermal adaptation and ecological speciation. Molecular Ecology 21: 782-799.
39. King MG, Horning ME, Roalson EH. 2009. Range persistence during the last glacial maximum: Carex macrocephala was not restricted to glacial refugia. Molecular Ecology 18: 4256-4269.
40. Kou XY, Ferguson DK, Xu JX, Wang YF, Li CS. 2006. The reconstruction of paleovegetation and paleoclimate in the Late Pliocene of West Yunnan, China. Climatic Change 77: 431-448.
41. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23: 2947-2948.
42. Li JJ, Fang XM. 1999. Uplift of the Tibetan Plateau and environmental changes. Chinese Science Bulletin 44: 2117-2124.
43. Li SH, Yeung CKL, 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. Molecular Ecology 18: 622-633.
44. Li Y, Zhai SN, Qiu YX, Guo YP, Ge XJ, Comes HP. 2011. Glacial survival east and west of the 'Mekong-Salween Divide' in the Himalaya-Hengduan Mountains region as revealed by AFLPs and cpDNA sequence variation in Sinopodophyllum hexandrum (Berberidaceae). Molecular Phylogenetics and Evolution 59: 412-424.
45. Li WH, Zhang YG. 2010. The vertical climate of Hengduan Mountains region and its impact on forest distribution. Beijing, China: China Meteorological Press.
46. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
47. Liu J, Gao LM. 2011. Comparative analysis of three different methods of total DNA extraction used in Taxus. Guihaia 31: 244-249.
48. Liu JQ, Gao TG, Chen ZD, Lu AM. 2002. Molecular phylogeny and biogeography of the Qinghai-Tibet Plateau endemic Nannoglottis (Asteraceae). Molecular Phylogenetics and Evolution 23: 307-325.
49. Liu J, Gao LM, Li DZ, Zhang DQ, Möller M. 2011a. Cross-species amplification and development of new microsatellite loci for Taxus wallichiana (Taxaceae). American Journal of Botany 98: e70-e73.
50. Liu J, Möller M, Gao LM, Zhang DQ, Li DZ. 2011b. DNA barcoding for the discrimination of Eurasian yews (Taxus L., Taxaceae) and the discovery of cryptic species. Molecular Ecology Resources 11: 89-100.
51. 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. Molecular Phylogenetics and Evolution 38: 31-49.
52. Lowry DB, Rockwood RC, Willis JH. 2008. Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution 62: 2196-2214.
53. Manni F, Guérard E, Heyer E. 2004. Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier's algorithm. Human Biology 76: 173-190.
54. Mao KS, Milne RI, Zhang LB, Peng YL, Liu JQ, Thomas P, Mill RR, Renner SS. 2012. Distribution of living Cupressaceae reflects the breakup of Pangea. Proceedings of the National Academy of Sciences, USA 109: 7793-7798.
55. Marko PB, Hoffman JM, Emme SA, McGovern TM, Keever CC, Nicole Cox L. 2010. The 'expansion-contraction' model of Pleistocene biogeography: rocky shores suffer a sea change? Molecular Ecology 19: 146-169.
56. Möller M, Gao LM, Mill RR, Li DZ, Hollingsworth ML, Gibby M. 2007. Morphometric analysis of the Taxus wallichiana complex (Taxaceae) based on herbarium material. Botanical Journal of the Linnean Society 155: 307-335.
57. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
58. Nosil P, Harmon LJ, Seehausen O. 2009. Ecological explanations for (incomplete) speciation. Trends in Ecology and Evolution 24: 145-156.
59. Nosil P, Vines TH, Funk DJ. 2005. Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59: 705-719.
60. Nybom H. 2004. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology 13: 1143-1155.
61. Opgenoorth L, Vendramin GG, Mao KS, Miehe G, Miehe S, Liepelt S, Liu JQ, Ziegenhagen B. 2010. Tree endurance on the Tibetan Plateau marks the world's highest known tree line of the Last Glacial Maximum. New Phytologist 185: 332-342.
62. Owen LA. 2009. Latest Pleistocene and Holocene glacier fluctuations in the Himalaya and Tibet. Quaternary Science Reviews 28: 2150-2164.
63. Peakall R, Smouse PE. 2006. GENALEX 6: genetic analysis in Excel: population genetic software for teaching and research. Molecular Ecology Notes 6: 288-295.
64. Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG. 2005. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology 14: 689-701.
65. Phillips SJ, Anderson RP, Schapire RE. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231-259.
66. Pinheiro F, de Barros F, Palma-Silva C, Fay MF, Lexer C, Cozzolino S. 2011. Phylogeography and genetic differentiation along the distributional range of the orchid Epidendrum fulgens: a Neotropical coastal species not restricted to glacial refugia. Journal of Biogeography 38: 1923-1935.
67. Pons O, Petit RJ. 1996. Measuring and testing genetic differentiation with ordered vs unordered alleles. Genetics 144: 1237-1245.
68. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
69. Poudel RC, Möller M, Gao LM, Ahrends A, Baral SR, Liu J, Thomas P, Li DZ. 2012. Using morphological, molecular and climatic data to delimitate yews along the Hindu Kush-Himalaya and adjacent regions. PLoS ONE 7: e46873.
70. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
71. Rice WR. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
72. Rieseberg LH, Burke JM. 2001. The biological reality of species: gene flow, selection, and collective evolution. Taxon 50: 235-255.
73. Royden LH, Burchfiel BC, van der Hilst RD. 2008. The geological evolution of the Tibetan plateau. Science 321: 1054-1058.
74. Ruddiman WF, Kutzbach JE. 1989. Forcing of late Cenozoic Northern Hemisphere climate by plateau uplift in southern Asia and the American West. Journal of Geophysical Research 94: 18 409-18 427.
75. Shi YF, Li JJ, Li BY. 1998. Uplift and environmental changes of Qinghai-Xizang (Tibetan) in the Late Cenozoic. Guangzhou, China: Guangdong Science and Technology Press.
76. Shi YF, Yu G, Liu XD, Li BY, Yao TD. 2001. Reconstruction of the 30-40 ka bp enhanced Indian monsoon climate based on geological records from the Tibetan Plateau. Palaeogeography, Palaeoclimatology, Palaeoecology 169: 69-83.
77. Spicer RA, Harris NBW, Widdowson M, Herman AB, Guo SX, Valdes PJ, Wolfe JA, Kelley SP. 2003. Constant elevation of southern Tibet over the past 15 million years. Nature 421: 622-624.
78. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF. 1998. Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7: 453-464.
79. Taberlet P, Gielly L, Pautou G, Bouvet J. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17: 1105-1109.
80. Tapponnier P, Lacassin R, Leloup PH, Scharer U, Zhong D, Wu H, Liu X, Ji S, Zhang L, Zhong J. 1990. The Ailao Shan/Red River metamorphic belt: tertiary left-lateral shear between Indochina and South China. Nature 343: 431-437.
81. Thorpe RS, Surget-Groba Y, Johansson H. 2010. Genetic tests for ecological and allopatric speciation in anoles on an island archipelago. PLoS Genetics 6: e1000929.
82. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535-538.
83. Wagner CE, Harmon LJ, Seehausen O. 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487: 366-369.
84. Walker D. 1986. Late Pleistocene-early Holocene vegetational and climatic changes in Yunnan Province, southwest China. Journal of Biogeography 13: 477-486.
85. Wan SM, Li A, Clift PD, Stuut JBW. 2007. Development of the East Asian monsoon: mineralogical and sedimentologic records in the northern South China Sea since 20 Ma. Palaeogeography, Palaeoclimatology, Palaeoecology 254: 561-582.
86. Wang LY, Abbott RJ, Zheng W, Chen P, Wang YL, Liu JQ. 2009a. History and evolution of alpine plants endemic to the Qinghai-Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae). Molecular Ecology 18: 709-721.
87. Wang WB, Jiang YB, Wang DM, Jing YB. 2006. Biological and ecological characteristics of Taxus yunnanensis. Journal of West China Forestry Science 35: 33-39.
88. Wang H, Qiong L, Sun K, Lu F, Wang YG, Song ZP, Wu QH, Chen JK, Zhang WJ. 2010. Phylogeographic structure of Hippophae tibetana (Elaeagnaceae) highlights the highest microrefugia and the rapid uplift of the Qinghai-Tibetan Plateau. Molecular Ecology 19: 2964-2979.
89. Wang YJ, Susanna A, Von Raab-Straube E, Milne R, Liu JQ. 2009b. Island-like radiation of Saussurea (Asteraceae: Cardueae) triggered by uplifts of the Qinghai-Tibetan Plateau. Biological Journal of the Linnean Society 97: 893-903.
90. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
91. Wheeler NC, Jech KS, Masters SA, Obrien CJ, Timmons DW, Stonecypher RW, Lupkes A. 1995. Genetic variation and parameter estimates in Taxus brevifolia (Pacific yew). Canadian Journal of Forest Research 25: 1913-1927.
92. Xiao XY, Shen J, Wang SM, Xiao HF, Tong GB. 2009. Climate change and evolution of the southwest monsoon revealed by pollen records in the Heqing deep drilling core. Acta Palaeontologica Sinica 48: 185-193.
93. Xu TT, Abbott RJ, Milne RI, Mao K, Du FK, Wu GL, Ciren ZX, Miehe G, Liu JQ. 2010. Phylogeography and allopatric divergence of cypress species (Cupressus L.) in the Qinghai-Tibetan Plateau and adjacent regions. BMC Evolutionary Biology 10: 194.
94. Yan HF, Zhang CY, Wang FY, Hu CM, Ge XJ, Hao G. 2012. Population expanding with the phalanx model and lineages split by environmental heterogeneity: a case study of Primula obconica in subtropical China. PLoS ONE 7: e41315.
95. 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. Molecular Ecology 17: 5135-5145.
96. Yang FS, Qin AL, Li YF, Wang XQ. 2012. Great genetic differentiation among populations of Meconopsis integrifolia and its implication for plant speciation in the Qinghai-Tibetan Plateau. PLoS ONE 7: e37196.
97. Yao YF, Bruch AA, Cheng YM, Mosbrugger V, Wang YF, Li CS. 2012a. Monsoon vs uplift in Southwestern China-Late Pliocene climate in Yuanmou basin, Yunnan. PLoS ONE 7: e37760.
98. Yao T, Thompson L, Yang W, Yu W, Gao Y, Guo X, Yang X, Duan K, Zhao H, Xu B et al. 2012b. Different glacier status with atmospheric circulations in Tibetan Plateau and surroundings. Nature Climate Change 2: 663-667.
99. Yin A, Harrison TM. 2000. Geologic evolution of the Himalayan-Tibetan orogen. Annual Review of Earth and Planetary Sciences 28: 211-280.
100. 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. Molecular Ecology 14: 3513-3524.
101. Zhang YG, Ji J, Balsam W, Liu L, Chen J. 2009. Mid-Pliocene Asian monsoon intensification and the onset of Northern Hemisphere glaciation. Geology 37: 599-602.
102. Zheng BX, Xu QQ, Shen YP. 2002. The relationship between climate change and Quaternary glacial cycles on the Qinghai-Tibetan Plateau: review and speculation. Quaternary International 97-98: 93-101.