Phylogeography of a living fossil: Pleistocene glaciations forced Ginkgo biloba L. (Ginkgoaceae) into two refuge areas in China with limited subsequent postglacial expansion

Molecular Phylogenetics and Evolution

Volumn 48, Issue 3, 2008, Pages 1094-1105

  Gong, Wei ^a,b,c   Chen, Chuan ^a,b   Dobeš, Christoph ^c   Fu, Cheng Xin ^a,b   Koch, Marcus A ^c  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c Heidelberg Inst of Plant Sciences   (Germany)

Author keywords

AFLP; China; Chloroplast DNA; Ginkgo biloba; Introduced history; Phylogeography; Pleistocene; Refugia

Indexed keywords

CHLOROPLAST DNA; SPACER DNA;

ARTICLE; CHINA; EVOLUTION; FOSSIL; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; GINKGO BILOBA; HAPLOTYPE; MOLECULAR EVOLUTION; PHYLOGENY; TIME;

CHINA; DNA, CHLOROPLAST; DNA, INTERGENIC; EVOLUTION; EVOLUTION, MOLECULAR; FOSSILS; GEOGRAPHY; GINKGO BILOBA; HAPLOTYPES; PHYLOGENY; POLYMORPHISM, GENETIC; TIME FACTORS; VARIATION (GENETICS);

GINKGO (GENUS); GINKGO BILOBA; GINKGOACEAE; MYA;

EID: 50549089121     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2008.05.003     Document Type: Article

References (78)

1. Acheré V., Faivre-Rampant P., Jeandroz S., Besnard G., Markussen T., Aragones A., Fladung M., Ritter E., and Favre J.M. A full saturated linkage map of Picea abies including AFLP, SSR, ESTP, 5S rDNA and morphological markers. Theor. Appl. Genet. 108 (2004) 1602-1613
2. Archangelsky S.R., and Cuneo R. Polyspermophyllum, a new Permian gymnosperm from Argentina, with considerations about the Dicranophyllales. Rev. Paleo. Palyn. 63 (1990) 117-135
3. Axelrod D.I., Ai-Shehbaz I., and Raven P.H. History of the modern flora of China. In: Zhang A., and Wu A. (Eds). Floristic Characteristics and Diversity of East Asian Plants (1996), Springer, New York 43-55
4. Bowe L.M., Coat G., and Depamphilis C.W. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetale's closest relatives are conifers. Proc. Natl. Acad. Sci. 97 (2000) 4092-4097
5. Chaw S.M., Parkinson C.L., Cheng Y.C., Vincent T.M., and Palmer J.D. Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natl. Acad. Sci. 97 (2000) 4086-4091
6. Clement M., Posada D., and Crandall K.A. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9 (2000) 1657-1659
7. Corander J., Marttinen P., and Mätyniemi S. Bayesian identification of stock mixtures from molecular marker data. Fish. Bull. 104 (2006) 550-558
8. Corander J., Waldmann P., Marttinen P., and Sillanpää M.J. BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20 (2004) 2363-2369
9. Corander J., Waldmann P., and Sillanpää M.J. Bayesian analysis of genetic differentiation between populations. Genetics 163 (2003) 367-374
10. Del Tredici P. Ginkgos and people: a thousand years of interaction. Arnoldia 51 (1991) 2-15
11. Del Tredici P. Natural regeneration of Ginkgo biloba from downward growning cotyledonary buds (basal chichi). Am. J. Bot. 79 (1992) 522-530
12. Del Tredici P. Ginkgo chichi in nature, legend & cultivation. Int. Bonsai 4 (1993) 20-25
13. Del Tredici P., Lin H., and Yang G. The Ginkgos of Tian Mu Shan. Conserv. Biol. 4 (1992) 202-209
14. Demesure B., Sodzi N., and Petit R.J. A set of universal primers for amplification of non-coding regions of mitochondrial and chloroplast DNA in plants. Mol. Ecol. 4 (1995) 129-131
15. Doyle J.J., and Doyle J.L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19 (1987) 11-15
16. Doyle J.J. DNA protocols for plants: CTAB total DNA isolation. In: Hewitt G.M., and Johnston A. (Eds). Molecular Techniques in Taxonomy (1991), Springer-Verlag, Berlin, Germany 283-293
17. Editor Board of Mt. Tianmu, 1991. The history of Mt. Tianmu. Hangzhou, Zhejiang People's Press, China, pp. 186-190 (in Chinese).
18. Ehrich D. AFLPdat: a collection of R functions for convenient handling of AFLP data. Mol. Ecol. Notes 6 (2006) 603-604
19. Ehrich, D., Gaudeul, M., Assefa, A., Koch, M.A., Mummenhoff, K., Nemomissa, S., IntraBioDiv consortium, Brochmann, C. 2007. Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the East African mountains. Mol. Ecol. 16, 2542-2559.
20. Evanno G., Regnaut S., and Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14 (2005) 2611-2620
21. Fan X.X., Shen L., Zhang X., Chen X.Y., and Fu C.X. Assessing genetic diversity of Ginkgo biloba L. (Ginkgoaceae) populations from China by RAPD markers. Biochem. Genet. 42 (2004) 269-278
22. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985) 783-791
23. Ge Y.Q., Qiu Y.X., and Fu C.X. Genetic diversity of the "living fossil" Ginkgo biloba based on ISSR marker. Biodivers. Sci. 11 (2003) 276-287 (in Chinese with English abstract)
24. Grivet D., Heinze B., Vendramin G.G., and Petit R.J. Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol. Ecol. Notes 1 (2001) 345-349
25. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic. Acids Symp. Ser. 41 (1999) 95-98
26. Hamilton M.B. Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol. Ecol. Notes 8 (1999) 513-525
27. Harris T.M. The fossil flora of Scoresby Sound, East Greenland 4: Ginkgoales, Coniferals, Lycopodiales, and isolated fructification. Meddelser om Gronland 112 (1874) 1-176
28. Harrison S.P., Yu G., Takahar H., and Prentice I.C. Diversity of temperate plants in east Asia. Nature 413 (2001) 129-130
29. Hewitt G.M. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68 (1999) 87-112
30. Hong Y.P., Cho K.J., Hong K.N., and Shin E.M. Diversity of ISSR variants in Ginkgo biloba L. planted in six regions of Korea. J. Korean For. Soc. 90 (2001) 169-175
31. Hori S., and Hori T. A culture history of Ginkgo biloba in Japan and the generic name Ginkgo. In: Hori T., Ridge R.W., Tulecke W., Del Tredici P., Trémouillaux-Guille J., and Tobe H. (Eds). Ginkgo biloba-A Global Treasure: From Biology to Medicine (1997), Springer, Tokyo, Japan 385-411
32. Hwang S.Y., Lin T.P., Ma C.S., Lin C.L., Chung J.D., and Yang J.C. Postglacial population growth of Cunninghamia konishii (Cupressaceae) inferred from phylogeographical and mismatch analysis of chloroplast DNA variation. Mol. Ecol. 12 (2003) 2689-2695
33. Kuddus R.H., Kuddus N.N., and Dvorchik I. DNA polymorphism in the living fossil Gingko biloba from the Eastern United States. Genome 45 (2002) 8-12
34. Jin-Xing, L., Yu-Shi, H., Xian-Pu, W., 1996. Old Ginkgo trees in China, in: International Dendrology Society Yearbook, 1995, pp. 32-37.
35. Koch M., and Bernhardt K.-G. Comparative biogeography of different cytotypes of the European Annual Microthlaspi perfoliatum (Brassicaceae): refugia, diversity centres and post glacial colonization. Am. J. Bot. 91 (2004) 115-124
36. Li H.L. A horticultural and botanical history of Ginkgo. Bull. Morris Arboretum 7 (1956) 3-12
37. Liang L.X., and Li S.N. Argument about wild populations of Ginkgo. Sci. Silvae Sin. 37 (2001) 135-137
38. Lin X., and Zhang D.H. Analysis for the origin of Ginkgo population in Tianmu Mountains. Sci. Silvae Sin. 2 (2004) 28-31 (in Chinese with an English abstract)
39. Lu S.Y., Peng C.I., Cheng Y.P., Hong K.H., and Chiang T.Y. Chloroplast phylogeography of Cunninghamia konishii (Cupressaceae), an endemic conifer of Taiwan. Genome 44 (2001) 797-807
40. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Res. 27 (1967) 209-220
41. Meyen S.V. Basic features of gymnosperm systematics in phylogeny as evidenced by the fossil record. Bot. Rev. 50 (1984) 1-111
42. Meyen S.V. Gymnosperms of the Angara flora. In: Beck C.B. (Ed). Origin and Evolution of Gymnosperms (1988), Columbia, New York 339-381
43. Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B., and Kent J. Biodiversity hotspots for conservation priorities. Nature 403 (2000) 853-858
44. Mogensen H.L. The hows and whys of cytoplasmic inheritance in seed plants. Am. J. Bot. 83 (1996) 383-404
45. Nei M. Molecular Evolutionary Genetics (1987), Columbia University Press, NY, USA
46. Nei M., and Tajima F. Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105 (1983) 205-217
47. Newton A.C., Allnutt T.R., Gillies A.C.M., Lowe A.J., and Ennos R.A. Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol. Evol. 14 (1999) 140-145
48. Petit R.J., Duminil J., Fineschi S., Hampe A., Salvini D., and Vendramin G.G. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol. Ecol. 14 (2005) 689-701
49. Posada D., Crandall K.A., and Templeton A.R. GeoDis: a program for the cladistic nested analysis of geographic distribution of genetic haplotypes. Mol. Ecol. 9 (2000) 487-488
50. Pritchard J.K., Stephens M., and Donnelly P. Inference of population structure using multilocus genotype data. Genetics 155 (2000) 945-959
51. Ray, N., Adams, J.M., 2001. A GIS-based Vegetation Map of the World at the Last Glacial Maximum (25,000-15,000 BP). Internet Archaeology, 11. Available from: .
52. Remington D.L., Whetten R.W., Liu B.H., and O'malley D.M. Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda. Theor. Appl. Genet. 98 (1999) 1279-1292
53. Rothwell G.W., and Holt B. Fossils and phenology in the evolution of Ginkgo biloba. In: Hori T., Ridge R.W., Tulecke W., Del Tredici P., Trémouillaux-Guille J., and Tobe H. (Eds). Ginkgo biloba-A Global Treasure: From Biology to Medicine (1997), Springer, Tokyo, Japan 223-230
54. Rozas J., Sánchez-Delbarrio J.C., Messeguer X., and Rozas R. DnaSP, DNA polymorphism analyses by coalescent and other methods. Bioinformatics 19 (2003) 2496-2497
55. Schmid, M., Schmoll, H., 2001. Gingko, ur-baum und arzneipflanze, mythos, dichtung und kunst. S. Hirzel Verlag. Stuttgart-Leipzig, Germany.
56. Schneider, S., Roessli, D., Excoffier, L., 2000. Arlequin: a software for population genetics data analysis, version 2.000. Computer program and documentation distributed through the Department of Anthropology and Ecology, University of Geneva, Geneva, Switzerland; Available from: .
57. Shen L., Chen X.Y., Zhang X., Li Y.Y., Fu C.X., and Qiu Y.X. Genetic variation of Ginkgo biloba L. (Ginkgoaceae) based on cpDNA PCR-RFLPs: inference of glacial refugia. Heredity 94 (2005) 396-401
58. Shepherd M., Cross M., Dieters M.J., and Henry R. Genetic maps for Pinus elliottii var. elliottii and P. caribaea var. hondurensis using AFLP and microsatellite markers. Theor. Appl. Genet. 106 (2003) 1409-1419
59. Swofford, D.L., 2002. PAUP* Phylogenetic analysis using parsimony (* and other methods), Version 4.10. Sinauer Associates, Sunderland, MA, USA.
60. Taberlet P., Gielly L., Pautou G., and Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17 (1991) 1105-1109
61. Taberlet P. Biodiversity at the intraspecific level: the comparative phylogeographic approach. J. Biotechnol. 64 (1998) 91-100
62. Taberlet P., Fumagalli L., Wust-Saucy A.G., and Cossons J.F. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7 (1998) 453-464
63. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
64. Traula H. Evolutionary trends in the genus Ginkgo. Lethaia 1 (1967) 63-101
65. Traula H. The phytogeographic evolution of the genus Ginkgo L. Botaniska Notiser 120 (1968) 409-422
66. Tsumura Y., and Ohba K. The genetic diversity of isozymes and the possible dissemination of Ginkgo biloba in ancient times in Japan. In: Hori T., Ridge R.W., Tulecke W., Del Tredici P., Trémouillaux-Guille J., and Tobe H. (Eds). Ginkgo biloba-A Global Treasure: From Biology to Medicine (1997), Springer, Tokyo, Japan 159-172
67. Tzedakis P.C., Lawson I.T., Forgley M.R., and Hewitt G.M. Buffered tree population changes in Quaternary refugium: evolutionary implication. Science 292 (2002) 267-269
68. Uemura K. Cenozoic history of Ginkgo in East Asia. In: Hori T., Ridge R.W., Tulecke W., Del Tredici P., Trémouillaux-Guille J., and Tobe H. (Eds). Ginkgo biloba-A Global Treasure: From Biology to Medicine (1997), Springer, Tokyo, Japan 207-221
69. Vos P., Hogers R., Bleeker M., Reijans M., Van De Lee T., Hornes M., Fritjers A., Pot J., Peleman J., Kuiper M., and Zabeau M. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23 (1995) 4407-4414
70. Wang H.W., and Ge S. Phylogeography of the endangered Cathaya argyrophylla (Pinaceae) inferred from sequence variation of mitochondrial and nuclear DNA. Mol. Ecol. 15 (2006) 4109-4122
71. Wu C.S., Wang Y.N., Liu S.M., and Chaw S.M. Chloroplast Genome (cpDNA) of Cycas taitungensis and 56 Cp protein-coding genes of Gnetum parvifolium: insight into cpDNA evolution and phylogeny of extant seed plants. Mol. Biol. Evol. 24 (2007) 1366-1379
72. Wu J.Y., Cheng P.L., and Tang S.J. Isozyme analysis of the genetic variation of Ginkgo biloba L. population in Tian-Mu Mountain. J. Plant Resour. Environ. 1 (1992) 20-23 (in Chinese with English abstract)
73. Xiang Y.H., and Xiang Z. Ancient Ginkgo biloba report III: Investigation on ancient Ginkgo biloba remnant population in Guiyang. Guizhou Sci. 17 (1999) 221-230 (in Chinese with an English abstract)
74. Xiang Z., Zhang Z.L., and Xiang Y.H. Investigation of natural Ginkgo biloba population on the Golden Buddha mountains of Nanchuan, Chongqing. Guizhou Sci. 19 (2001) 37-52 (in Chinese with an English abstract)
75. Xiang Z., Tu C.L., and Xiang Y.H. A report on Ginkgo resources in Panxian county, Guizhou province. Guizhou Sci. 21 (2003) 159-174 (in Chinese with an English abstract)
76. Xiang B.X., Xiang Z., and Xiang Y.H. Investigation of wild Ginkgo biloba in Wuchuan county of Guizhou, China-Guizhou ancient Ginkgo biloba resources investigation VII. Guizhou Sci. 24 (2006) 56-67 (in Chinese with an English abstract)
77. Ying X.Y. Studies on the production of Ginkgo biloba L. in China and suggestions for the improvement. East China Forest Manage. 16 (2002) 41-43 (in Chinese)
78. Zhou Z.Y. Mesozoic Ginkgoaleans: phylogeny, classification and evolutionary trends. Acta Bot. Yunnan. 25 (2003) 377-396 (in Chinese with English abstract)