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Plant Systematics and Evolution

, Volume 302, Issue 9, pp 1179–1193 | Cite as

Phylogeographic study revealed microrefugia for an endemic species on the Qinghai–Tibetan Plateau: Rhodiola chrysanthemifolia (Crassulaceae)

  • Qing-Bo Gao
  • Fa-Qi Zhang
  • Rui Xing
  • Richard J. Gornall
  • Peng-Cheng Fu
  • Yan Li
  • Zhuo-Ma Gengji
  • Shi-Long ChenEmail author
Original Article

Abstract

Most phylogeographic studies on the Qinghai–Tibetan Plateau and in adjacent regions have focused on tree or shrub species, or on herbaceous species that mainly inhabit alpine meadows or grasslands. The phylogeography of herbaceous species that inhabit woodlands and shrubberies has been largely neglected. Here we investigate the evolutionary history of a woodland- and shrubbery-inhabited herbaceous species, Rhodiola chrysanthemifolia, which grows in southern Tibet and in the mountains of the Hengduan ecoregion. The cpDNA trnL-F, rpl20-rps12 and nrDNA ITS regions of 183 individuals from 13 populations were sequenced. The ITS dataset revealed a significant phylogeographic structure across the distribution range of R. chrysanthemifolia, while the cpDNA dataset showed no significant structure. Besides, analyses of molecular variance showed that among-population variation was described as 96.27 % of the total variation for ITS marker, much higher than that for cpDNA (63.68 %). Limited seed migration among populations together with inbreeding within populations of R. chsysanthemifolia may result in the different phylogeographic and genetic patterns for ITS and cpDNA markers in this species. A high frequency and an even distribution of private cpDNA haplotypes were discovered throughout the distribution range of R. chrysanthemifolia; ITS genotypes formed three main lineages which showed a geographical distribution pattern. Furthermore, populations with above-average gene diversity were evenly spread across the current distribution range of R. chrysanthemifolia, supporting the existence of microrefugia for this species during Last Glacial Maximum, even earlier glaciations, similar to the pattern of sympatric tree and shrub species of the Juniperus tibetica complex and Hippophae tibetana. Allopatric divergence of populations in isolated microrefugia could be responsible for large number of private cpDNA haplotypes across the current distribution range of R. chrysanthemifolia. The putative factors which drove diversification between R. chrysanthemifolia and R. alsia were also discussed.

Keywords

Allopatric divergence Limited seed dispersal with increasing inbreeding Microrefugia Phylogeography Qinghai–Tibetan Plateau Rhodiola chrysanthemifolia 

Notes

Acknowledgments

This research was supported by National Natural Science Foundation of China (Grant Nos. 31200281, 31270270, 31400322), CAS “Light of West China” Program and Youth Innovation Promotion Association, CAS (Grant No. 2016378).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2016_1324_MOESM1_ESM.meg (35 kb)
Online Resource 1. Alignment of 20 concatenated cpDNA (rpl20-rps12+trnL-F) haplotypes plus outgroup (MEG 36 kb)
606_2016_1324_MOESM2_ESM.meg (20 kb)
Online Resource 2. Alignment of 27 ITS haplotypes plus outgroup (MEG 20 kb)

References

  1. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molec Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  2. Chen S, Wu G, Zhang D, Gao Q, Duan Y, Zhang F, Chen S (2008) Potential refugium on the Qinghai–Tibet Plateau revealed by the chloroplast DNA phylogeography of the alpine species Metagentiana striata (Gentianaceae). Bot J Linn Soc 157:125–140CrossRefGoogle Scholar
  3. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  4. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochem Bull Bot Soc Amer 19:11–15Google Scholar
  5. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedPubMedCentralGoogle Scholar
  6. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molec Ecol 11:2571–2581CrossRefGoogle Scholar
  7. Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259CrossRefGoogle Scholar
  8. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molec Ecol 13:853–864CrossRefGoogle Scholar
  9. Excoffier L, Laval G, Schneider S (2005) Arlequin (ver. 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  10. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  11. Fjeldsa J, Lovett JC (1997) Geographical patterns of old and young species in African forest biota: the significance of specific montane areas as evolutionary centres. Biodiversity Conservation 6:325–346CrossRefGoogle Scholar
  12. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  13. Funk DJ, Nosil P, Etges WJ (2006) Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc Natl Acad Sci USA 103:3209–3213CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gao Q, Zhang D, Chen S, Duan Y, Zhang F, Li Y, Chen S (2009) Chloroplast DNA phylogeography of Rhodiola alsia (Crassulaceae) in the Qinghai–Tibet Plateau. Botany 87:1077–1088CrossRefGoogle Scholar
  15. Gao Q, Zhang D, Duan Y, Zhang F, Li Y, Fu P, Chen S (2012) Intraspecific divergences of Rhodiola alsia (Crassulaceae) based on plastid DNA and internal transcribed spacer fragments. Bot J Linn Soc 168:204–215CrossRefGoogle Scholar
  16. Gao QB, Li YH, Gornall RJ, Zhang ZX, Zhang FQ, Xing R, Fu PC, Wang JL, Liu HR, Tian ZZ, Chen SL (2015) Phylogeny and speciation in Saxifraga sect. Ciliatae (Saxifragaceae): evidence from psbA-trnH, trnL-F and ITS sequences. Taxon 64:703–713CrossRefGoogle Scholar
  17. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Statist Sci 7:457–511CrossRefGoogle Scholar
  18. Grivet D, Petit RJ (2002) Phylogeography of the common ivy (Hedera sp.) in Europe: genetic differentiation through space and time. Molec Ecol 11:1351–1362CrossRefGoogle Scholar
  19. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  20. Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molec Ecol 8:521–523Google Scholar
  21. Harmon LJ, Melville J, Larson A, Losos JB (2008) The role of geography and ecological opportunity in the diversification of day geckos (Phelsuma). Syst Biol 57:562–573CrossRefPubMedGoogle Scholar
  22. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biol 66:591–600PubMedGoogle Scholar
  23. Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR, Sherry ST (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967CrossRefPubMedPubMedCentralGoogle Scholar
  24. Harrison TM, Copeland P, Kidd WSF, Yin A (1992) Raising Tibet. Science 255:1663–1670CrossRefPubMedGoogle Scholar
  25. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  26. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans, Ser B 359:183–195CrossRefGoogle Scholar
  27. 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 Phytol 194:1123–1133CrossRefPubMedGoogle Scholar
  28. Kapp P, DeCelles PG, Gehrels GE, Heizier M, Ding L (2007) Geological records of the Lhasa-Qiangtang and Indo-Asian collisions in the Nima area of central Tibet. Geol Soc Amer Bull 119:917–932CrossRefGoogle Scholar
  29. Knowles LL (2000) Tests of Pleistocene speciation in montane grasshoppers (genus Melanoplus) from the sky islands of western North America. Evolution 54:1337–1348CrossRefPubMedGoogle Scholar
  30. Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molec Biol Evol 16:750–759CrossRefGoogle Scholar
  31. Lehmkuhl F, Owen LA (2005) Late Quaternary glaciation of Tibet and the bordering mountains: a review. Boreas 34:87–100CrossRefGoogle Scholar
  32. Li JJ, Fang XM, Ma HZ, Zhu JJ, Pan BT, Chen HL (1996) Geomorphological and environmental evolution in the upper reaches of the Yellow River during the late Cenozoic. Sci China D 39:380–390Google Scholar
  33. 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. Molec Ecol 22:5237–5255CrossRefGoogle Scholar
  34. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  35. 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
  36. Meng L, Yang R, Abbott RJ, Miehe G, Hu T, Liu J (2007) Mitochondrial and chloroplast phylogeography of Picea crassifolia Kom. (Pinaceae) in the Qinghai–Tibetan Plateau and adjacent highlands. Molec Ecol 16:4128–4137CrossRefGoogle Scholar
  37. Mes THM, van Brederode J, t’Hart H (1996) Origion of the woody Macaronesian Sempervivoideae and the phylogenetic position of the east African species of Aeonium. Bot Acta 109:477–481CrossRefGoogle Scholar
  38. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  39. 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
  40. Polzin T, Daneshmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Operations Res Lett 31:12–20CrossRefGoogle Scholar
  41. Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245PubMedPubMedCentralGoogle Scholar
  42. Rambaut A (2009) FigTree version 1.3.1. http://tree.bio.ed.ac.uk/software/figtree
  43. Rambaut A, Drummond AJ (2009a) LogCombiner version 1.5.3. http://beast.bio.ed.ac.uk/LogCombiner
  44. Rambaut A, Drummond AJ (2009b) TreeAnnotator version 1.5.3. http://beast.bio.ed.ac.uk/TreeAnnotator
  45. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer version 1.6. http://beast.bio.ed.ac.uk/Tracer
  46. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Molec Biol Evol 20:76–86CrossRefPubMedGoogle Scholar
  47. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molec Biol Evol 9:552–569PubMedGoogle Scholar
  48. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  49. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  50. Rowley DB, Currie BS (2006) Palaeo-altimetry of the late Eocene to Miocene Lunpola basin, central Tibet. Nature 439:677–681CrossRefPubMedGoogle Scholar
  51. Seong YB, Owen LA, Bishop MP, Bush A, Clendon P, Copland L, Finkel R, Kamp U, Shroder JF (2008) Quaternary glacier history of the Central Karakoram—reply. Quaternary Sci Rev 27:1656–1658CrossRefGoogle Scholar
  52. 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
  53. Shimono A, Ueno S, Gu S, Zhao X, Tsumura Y, Tang Y (2010) Range shifts of Potentilla fruticosa on the Qinghai–Tibetan Plateau during glacial and interglacial periods revealed by chloroplast DNA sequence variation. Heredity 104:534–542CrossRefPubMedGoogle Scholar
  54. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity Evol 12:335–337CrossRefGoogle Scholar
  55. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedPubMedCentralGoogle Scholar
  56. Spicer RA, Harris NB, Widdowson M, Herman AB, Guo S, Valdes PJ, Wolfe JA, Kelley SP (2003) Constant elevation of southern Tibet over the past 15 million years. Nature 421:622–624CrossRefPubMedGoogle Scholar
  57. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313CrossRefPubMedPubMedCentralGoogle Scholar
  58. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. Amer J Human Genet 76:449–462CrossRefGoogle Scholar
  59. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Amer J Human Genet 68:978–989CrossRefGoogle Scholar
  60. Sun Y, Wang A, Wan D, Wang Q, Liu J (2012) Rapid radiation of Rheum (Polygonaceae) and parallel evolution of morphological traits. Molec Phylogen Evol 63:150–158CrossRefGoogle Scholar
  61. Sun Y, Abbott RJ, Li L, Li L, Zou J, Liu J (2014) Evolutionary history of Purple cone spruce (Picea Purpurea) in the Qinghai–Tibet Plateau: homoploid hybrid origin and Pleistocene expansion. Molec Ecol 23:343–359CrossRefGoogle Scholar
  62. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (and other methods), version 4.0 Beta. Sinauer, SunderlandGoogle Scholar
  63. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109CrossRefGoogle Scholar
  64. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  65. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Molec Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wang YJ, Liu JQ (2004) A preliminary investigation on the phylogeny of Saussurea (Asteraceae: Cardueae) based on chloroplast DNA trnL-F sequences. Acta Phytotax Sin 42:136–153Google Scholar
  67. Wang A, Yang M, Liu J (2005) Molecular phylogeny, recent radiation and evolution of gross morphology of the Rhubarb genus Rheum (Polygonaceae) inferred from chloroplast DNA trnL-F sequences. Ann Bot (Oxford) 96:489–498CrossRefGoogle Scholar
  68. Wang C, Zhao X, Liu Z, Lippert PC, Graham SA, Coe RS, Yi H, Zhu L, Liu S, Li Y (2008) Constraints on the early uplift history of the Tibetan Plateau. Proc Natl Acad Sci USA 105:4987–4992CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wang LY, Ikeda H, Liu TL, Wang YJ, Liu JQ (2009a) Repeated range expansion and glacial endurance of Potentilla glabra (Rosaceae) in the Qinghai–Tibetan Plateau. J Integr Pl Biol 51:698–706CrossRefGoogle Scholar
  70. Wang L, Abbott RJ, Zheng W, Chen P, Wang Y, Liu J (2009b) History and evolution of alpine plants endemic to the Qinghai–Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae). Molec Ecol 18:709–721CrossRefGoogle Scholar
  71. 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. Molec Ecol 19:2964–2979CrossRefGoogle Scholar
  72. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols. Academic Press, San Diego, pp 315–322Google Scholar
  73. Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058CrossRefPubMedPubMedCentralGoogle Scholar
  74. Wu CY (1987) Origin and evolution of flora of Xizang. In: Wu CY (ed) Flora Xizangica. Science Press, BeijingGoogle Scholar
  75. Wu SG, Yang YP, Fei Y (1995) On the flora of the alpine region in the Qinghai–Xizang (Tibet) Plateau. Acta Bot Yunnan 17:233–250Google Scholar
  76. Xu T, Abbott RJ, Milne RI, Mao K, Du FK, 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
  77. 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. Molec Ecol 17:5135–5145CrossRefGoogle Scholar
  78. Zhang D, Fengquan L, Jianmin B (2000) Eco-environmental effects of the Qinghai–Tibet Plateau uplift during the Quaternary in China. Environm Geol 39:1352–1358CrossRefGoogle Scholar
  79. 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. Molec Ecol 14:3513–3524CrossRefGoogle Scholar
  80. Zhang YH, Volis S, Sun H (2010) Chloroplast phylogeny and phylogeography of Stellera chamaejasme on the Qinghai–Tibet Plateau and in adjacent regions. Molec Phylogen Evol 57:1162–1172CrossRefGoogle Scholar
  81. Zheng D (1996) The system of physico-geographical regions of the Qinghai–Xizang (Tibet) Plateau. Sci China D 39:410–417Google Scholar
  82. 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 Int 97–8:93–101CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau BiologyChinese Academy of SciencesXiningChina
  2. 2.Department of GeneticsUniversity of LeicesterLeicesterUK
  3. 3.Department of Life SciencesLuoyang Normal UniversityLuoyangChina
  4. 4.University of Chinese Academy of SciencesBeijingChina

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