SYSTEMATICS AND PHYLOGENY
Evolutionary radiations of cushion plants on the Qinghai-Tibet Plateau: Insights from molecular phylogenetic analysis of two subgenera of Arenaria and Thylacospermum (Caryophyllaceae)
Correction(s) for this article
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Corrigendum to: Evolutionary radiations of cushion plants on the Qinghai-Tibet Plateau: Insights from molecular phylogenetic analysis of two subgenera of Arenaria and Thylacospermum (Caryophyllaceae) [in Taxon 68: 1003–1020. 2019]
- Volume 70Issue 3TAXON
- pages: 687-687
- First Published online: June 19, 2021
Bo Xu,
Dong Luo,
Zhi-Min Li,
Hang Sun,
Bo Xu
College of Forestry, Southwest Forestry University, Kunming, 650224 China
These authors contributed equally to this workSearch for more papers by this authorDong Luo
Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201 China
These authors contributed equally to this workSearch for more papers by this authorZhi-Min Li
School of Life Science, Yunnan Normal University, Kunming, 650500 China
Search for more papers by this authorCorresponding Author
Hang Sun
Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201 China
Address for correspondence: Hang Sun, [email protected]Search for more papers by this authorBo Xu,
Dong Luo,
Zhi-Min Li,
Hang Sun,
Bo Xu
College of Forestry, Southwest Forestry University, Kunming, 650224 China
These authors contributed equally to this workSearch for more papers by this authorDong Luo
Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201 China
These authors contributed equally to this workSearch for more papers by this authorZhi-Min Li
School of Life Science, Yunnan Normal University, Kunming, 650500 China
Search for more papers by this authorCorresponding Author
Hang Sun
Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201 China
Address for correspondence: Hang Sun, [email protected]Search for more papers by this authorAssociate Editor: Hans Peter Comes
Abstract
Cushion plants exhibiting adaptive convergence in cold and dry environments are keystone and foundation species in the alpine/subnival habitat on the Qinghai-Tibet Plateau (QTP). To date, little attention has been paid to the molecular phylogeny, origin, and biogeography of cushion plants on the QTP. We investigated the molecular phylogeny of classic cushion Arenaria subg. Dolophragma, A. subg. Eremogoneastrum, and Thylacospermum on the QTP, within the framework of the Caryophyllaceae. A new Thylacospermum-Dolophragma clade was identified using combined plastid markers (rps16, matK, trnL-trnF, trnS-trnfM) and nuclear ribosomal DNA. Molecular divergence dating suggested that Thylacospermum and A. subg. Dolophragma originated in the middle to late Miocene (11.68 Ma). Combined with ancestral range reconstruction, there is an indication that all species of cushion Arenaria (A. subg. Dolophragma, A. subg. Eremogoneastrum) originated during/after the late Pliocene, and the QTP was their ancestral area. Furthermore, ecological niche modeling showed that the areas occupied by the three studied cushion plants during the last glacial maximum (LGM) was broader than that of their present distribution, implying a reduction in their range after the LGM. This evidence clearly illustrates that multistage uplift of the QTP and bordering mountains since the Miocene associated with climatic change (worldwide cooling, aridification in Central Asia, Quaternary glaciation) played a role in triggering and facilitating the speciation and/or evolutionary radiations of the species studied.
Supporting Information
| Filename | Description |
|---|---|
| tax12127-sup-0003-FigureS1.jpgJPEG image, 2.2 MB | Fig. S1 Potential distribution ranges of three studied species at the Present and during the Mid-Holocene (ca. 6 ka) based on the outputs of CCSM4 and MIROC-ESM. The logistic value of habitat suitability is shown by the colored gradient scale bars. Red dots correspond to all available collection locations used in ecological niche modeling. Maps of the potential stable, reduced and expanded areas compared between the present and the Mid-Holocene (CCSM4, MIROC-ESM) are displayed on the right. |
| tax12127-sup-0001-appendixS1.nexPDF document, 566.9 KB | Appendix S1. Combined cpDNA alignment. |
| tax12127-sup-0002-appendixS2.nexPDF document, 81 KB | Appendix S2. ITS alignment. |
| tax12127-sup-0004-TableS1.docWord document, 57.5 KB | Table S1 Dispersal multipliers used in ancestral range reconstruction. Letters A-I denote areas delineated for analysis: (A) Europe to Central Asia (including Central Asian mountains, Tianshan); (B) northern Asia; (C) QTP containing Hengduan Mountains and Himalaya; (D) East Asia including Taiwan, Mongolia, Korean peninsula and Japan; (E) Central and North America; (F) South America; (G) Southeast Asia; (H) Malay Archipelago and Australia; (I) Southeast Africa. Dispersal probabilities between areas were defined as follows: 1, dispersal between adjacent areas; 0.5, dispersal across adjacent areas separated by intermittent/climatic barriers or dispersal across several areas; 0.1, dispersal across at least two areas separated by intermittent/climatic barriers; 0.01, very unlikely dispersal events. Only one half of symmetrical matrices is shown for simplicity. |
| tax12127-sup-0005-TableS2.docWord document, 106 KB | Table S2 Presence locality records of the three concerned species used for ecological niche modeling (ENM) based on herbarium specimens. Province abbreviations: XJ, Xinjiang; GS, Gansu; QH, Qinghai; SC, Sichuan; YN, Yunnan; XZ, Xizang. |
| tax12127-sup-0006-TableS3.docWord document, 40.5 KB | Table S3 List of variables used as inputs to generate ensemble distribution models for Ecological Niche Modeling. |
| tax12127-sup-0007-TableS4.docWord document, 122.5 KB | Table S4 Pearson's correlation (r) matrix performed among the 19 bioclimatic variables (for definitions, see suppl. Table S3). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
LITERATURE CITED
- Aubert, S., Boucher, F., Lavergne, S., Renaud, J. & Choler, P. 2014. 1914–2014: A revised worldwide catalogue of cushion plants 100 years after Hauri and Schroter. Alpine Bot. 124: 59–70. https://doi.org/10.1007/s00035-014-0127-x
- Badano, E.I., Jones, C., Cavieres, L. & Wright, J. 2006. Assessing impacts of ecosystem engineers on community organization: A general approach illustrated by effects of a high-Andean cushion plant. Oikos 115: 369–385.
- Biomatters 2013. Geneious, version 7.0.2. Auckland: Biomatters. https://www.geneious.com/
- Bittrich, V. 1993. Caryophyllaceae. Pp. 206–236 in: K. Kubitzki, J.G. Rohwer & V. Bittrich (eds.), The families and genera of vascular plants, vol. 2. Berlin: Springer. https://doi.org/10.1007/978-3-662-02899-5
- Boucher, F.C., Thuiller, W., Roquet, C., Douzet, R., Aubert, S., Alvarez, N. & Lavergne, S. 2012. Reconstructing the origins of high-alpine niches and cushion life form in the genus Androsace s.l. (Primulaceae). Evolution 66: 1255–1268. https://doi.org/10.1111/j.1558-5646.2011.01483.x
- Boucher, F.C., Lavergne, S., Basile, M., Choler, P. & Aubert, S. 2016. Evolution and biogeography of the cushion life form in angiosperms. Perspect. Pl. Ecol. Evol. Syst. 20: 22–31. https://doi.org/10.1016/j.ppees.2016.03.002
- Butterfield, B.J., Cavieres, L.A., Callaway, R.M., Cook, B.J., Kikvidze, Z., Lortie, C.J., Michalet, R., Pugnaire, F.I., Schöb, C., Xiao, S., Anthelme, F., Björk, R.G., Dickinson, K.J.M., Cranston, B.H., Gavilán, R., Gutiérrez-Giróon, A., Kanka, R., Maalouf, J.P., Mark, A.F., Noroozi, J., Parajuli, R., Phoenix, G.K., Reid, A.M., Ridenour, W.M., Rixen, C., Wipf, S., Zhao, L., Escudero, A., Zaitchik, B.F., Lingua, E., Aschehoug, E.T. & Callaway, R.M. 2013. Alpine cushion plants inhibit loss of phylogenetic diversity in severe environments. Ecol. Lett. 16: 478–486. https://doi.org/10.1111/ele.12070
- Cavieres, L.A., Quiroz, C.L. & Molina-Montenegro, M.A. 2008. Facilitation of the non-native Taraxacum officinale by native nurse cushion species in the high Andes of central Chile: Are there differences between nurses? Funct. Ecol. 22: 148–156. https://doi.org/10.1111/j.1365-2435.2007.01338.x
- Chen, J.G., Yang, Y., Stöcklin, J., Cavieres, L.A., Peng, D.L., Li, Z.M. & Sun, H. 2015. Soil nutrient availability determines the facilitative effects of cushion plants on other plant species at high elevations in the south-eastern Himalayas. Pl. Ecol. Diversity 8: 199–210. https://doi.org/10.1080/17550874.2013.872206
- Chen, Y.S., Deng, T., Zhou, Z. & Sun, H. 2018. Is the East Asian flora ancient or not? Natl. Sci. Rev. 5: 920–932. https://doi.org/10.1093/nsr/nwx156
- Darriba, D., Taboada, G.L., Doallom R. & Posada, D. 2012. jModelTest 2: More models, new heuristics and parallel computing. Nature, Meth. 9: 772. https://doi.org/10.1038/nmeth.2109
- De Bello, F., Doležal, J., Dvorský, M., Chlumská, Z., Řeháková, K., Klimešová, J. & Klimeš, L. 2011. Cushions of Thylacospermum caespitosum (Caryophyllaceae) do not facilitate other plants under extreme altitude and dry condition in the northwest Himalayas. Ann. Bot. (Oxford) 108: 567–573. https://doi.org/10.1093/aob/mcr183
- Dillenberger, M.S. & Kadereit, J.W. 2014. Maximum polyphyly: Multiple origins and delimitation with plesiomorphic characters require a new circumscription of Minuartia (Caryophyllaceae). Taxon 63: 64–88. https://doi.org/10.12705/632.42
- Drummond, A.J. & Rambaut, A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. B. M. C. Evol. Biol. 7: 214–221. https://doi.org/10.1186/1471-2148-7-214
- Drummond, A.J., Ho, S.Y., Phillips, M.J. & Rambaut, A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4: 699–710. https://doi.org/10.1371/journal.pbio.0040088
- Dvorský, M., Doležal, J., Kopecký, M., Chlumská, Z., Janatková, K., Altman, J., De Bello, F. & Řeháková, K. 2013. Testing the stress gradient hypothesis at the roof of the world: Effects of the cushion plant Thylacospermum caespitosum on species assemblages. PLoS ONE 8: e53514. https://doi.org/10.1371/journal.pone.0053514
- Ebersbach, J., Schnitzler, J., Favre, A. & Muellner-Riehl, A.N. 2017. Evolutionary radiations in the species-rich mountain genus Saxifraga L. B. M. C. Evol. Biol. 17: 119. https://doi.org/10.1186/s12862-017-0967-2
- Favre, A., Yuan, Y.M., Kuepfer, P. & Alvarez, N. 2010. Phylogeny of subtribe Gentianinae (Gentianaceae): Biogeographic inferences despite limitations in temporal calibration points. Taxon 59: 1701–1711. https://doi.org/10.1002/tax.596005
- Favre, A., Päckert, M., Pauls, S.U., Jähnig, S.C., Uhl, D., Michalak, I. & Muellner-Riehl, A.N. 2015. The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biol. Rev. (Cambridge) 90: 236–253. https://doi.org/10.1111/brv.12107
- Fior, S., Karis, P.O., Casazza, G., Minuto, L. & Sala, F. 2006. Molecular phylogeny of the Caryophyllaceae (Caryophyllales) inferred from chloroplast matK and nuclear rDNA ITS sequences. Amer. J. Bot. 93: 399–411. https://doi.org/10.3732/ajb.93.3.399
- Gao, Y.D., Harris, A.J., Zhou, S.D. & He, X.J. 2013. Evolutionary events in Lilium (including Nomocharis, Liliaceae) are temporally correlated with orogenies of the Q-T plateau and the Hengduan Mountains. Molec. Phylogen. Evol. 68: 443–460. https://doi.org/10.1016/j.ympev.2013.04.026
- Gene Codes 2002. Sequencher, version 4.14. Ann Arbor: Gene Codes Corporation. https://www.genecodes.com/sequencher
- Gizaw, A., Brochmann, C., Nemomissa, S., Wondimu, T., Masao, C.A., Tusiime, F.M., Abdi, A.A., Oxelman, B., Popp, M. & Dimitrov, D. 2016. Colonization and diversification in the African ‘sky islands’: Insights from fossil-calibrated molecular dating of Lychnis (Caryophyllaceae). New Phytol. 211: 719–734. https://doi.org/10.1111/nph.13937
- Greenberg, A.K. & Donoghue, M.J. 2011. Molecular systematics and character evolution in Caryophyllaceae. Taxon 60: 1637–1652. https://doi.org/10.1002/tax.606009
- Haffer, J. 1997. Alternative models of vertebrate speciation in Amazonia: An overview. Biodivers. & Conservation 6: 451–476. https://doi.org/10.1023/A:1018320925954
- Halloy, S.R.P. 2002. Variations in community structure and growth rates of high-Andean plants with climatic fluctuations. Pp. 227–240 in: C. Körner & E.M. Spehn (eds.), Moutain biodiversity: A global assessment. Boca Raton: CRC Press.
- Hara, H. & Tebbs, M.C. 1979. Caryophyllaceae. Pp. 51–59 in: H. Hara & L.H.J. Williams (eds.), An enumeration of the flowering plants of Nepal, vol. 2. London: The British Museum (Natural History).
- Harbaugh, D.T., Nepokroeff, M., Rabeler, R.K., McNeill, J., Zimmer, E.A. & Wagner, W.L. 2010. A new lineage-based tribal classification of the family Caryophyllaceae. Int. J. Pl. Sci. 171: 185–198. https://doi.org/10.1086/648993
- Harrison, T.M., Copland, P., Kidd, W.S.F. & Yin, A. 1992. Raising Tibet. Science 255: 1663–1670. https://doi.org/10.1126/science.255.5052.1663
- Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25: 1965–1978. https://doi.org/10.1002/joc.1276
- Ho, S.Y. & Phillips, M.J. 2009. Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst. Biol. 58: 367–380. https://doi.org/10.1093/sysbio/syp035
- Huang, R.F. 1994. The cushion plant in the Hoh Xil area of Qinghai. Acta Bot. Sin. 36: 130–137.
- Huelsenbeck, J.P. & Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
- Jabbour, F. & Renner, S.S. 2012. A phylogeny of Delphinieae (Ranunculaceae) shows that Aconitum is nested within Delphinium and that Late Miocene transitions to long life cycles in the Himalayas and Southwest China coincide with bursts in diversification. Molec. Phylogen. Evol. 62: 928–942. https://doi.org/10.1016/j.ympev.2011.12.005
- Jordan, G.J. & Macphail, M.K. 2003. A Middle-Late Eocene inflorescence of Caryophyllaceae from Tasmania, Australia. Amer. J. Bot. 90: 761–768. https://doi.org/10.3732/ajb.90.5.761
- Kirchner, N., Greve, R., Stroeven, A.P. & Heyman, J. 2011. Paleoglaciological reconstructions for the Tibetan Plateau during the last glacial cycle: Evaluating numerical ice sheet simulations driven by GCM-ensembles. Quatern. Sci. Rev. 30: 248–267. https://doi.org/10.1016/j.quascirev.2010.11.006
- Körner, C. 2003. Alpine plant life: Functional plant ecology of high mountain ecosystems, 2nd ed. Berlin: Springer.
10.1007/978-3-642-18970-8 Google Scholar
- Li, G.D., Kim, C.K., Zha, H.G., Zhou, Z., Nie, Z.L. & Sun, H. 2014. Molecular phylogeny and biogeography of the arctic-alpine genus Lagotis (Plantaginaceae). Taxon 63: 103–115. https://doi.org/10.12705/631.47
- Linnaeus, C. 1753. Species plantarum, vol. 1. Holmiae [Stockholm]: impensis Laurentii Salvii. https://doi.org/10.5962/bhl.title.669
- Luo, D., Yue, J.P., Sun, W.G., Xu, B., Li, Z.M., Comes, H.P. & Sun, H. 2016. Evolutionary history of the subnival flora of the Himalaya-Hengduan Mountains: First insights from comparative phylogeography of four perennial herbs. J. Biogeogr. 43: 31–43. https://doi.org/10.1111/jbi.12610
- Luo, D., Xu, B., Li, Z.M. & Sun, H. 2017. The ‘Ward Line–Mekong–Salween Divide’ is an important floristic boundary between the eastern Himalaya and Hengduan Mountains: Evidence from the phylogeographical structure of subnival herbs Marmoritis complanatum (Lamiaceae). Bot. J. Linn. Soc. 185: 482–496. https://doi.org/10.1093/botlinnean/box067
- Luo, D., Xu, B., Li, Z.M. & Sun, H. 2018. Phylogeography of rare fern Polystichum glaciale endemic to the subnival zone of the Sino-Himalaya. Pl. Syst. Evol. 304: 485–499. https://doi.org/10.1007/s00606-018-1495-2
- McNeill, J. 1962. Taxonomic studies in the Alsinoideae. I. Generic and infra-generic groups. Notes Roy. Bot. Gard. Edinburgh 24: 79–155
- Mengel, R.M. 1970. The North American central plains as an isolating agent in bird speciation. Pp. 279–340 in: D. Wakefield & J.K. Jones (eds.), Pleistocene and Recent environments of the Central Great Plains. Lawrence: University Press of Kansas.
- Miao, Y.F., Herrmann, M., Wu, F.L., Yan, X.L. & Yang, S.L. 2012. What controlled Mid-Late Miocene long-term aridification in Central Asia? – Global cooling or Tibetan Plateau uplift: A review. Earth-Sci. Rev. 112: 155–172. https://doi.org/10.1016/j.earscirev.2012.02.003
- Miller, M.A., Pfeiffer, W. & Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Pp. 45–52 in: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, Louisiana, 14 Nov 2010. Piscataway: IEEE. https://doi.org/10.1109/GCE.2010.5676129
10.1109/GCE.2010.5676129 Google Scholar
- Moore, A.J. & Dillenberger, M.S. 2017. A conspectus of the genus Cherleria (Minuartia s.l., Caryophyllaceae). Willdenowia 47: 5–11. https://doi.org/10.3372/wi.47.47101
- Núñez, C.I., Aizen, M.A. & Ezcurra, C. 1999. Species associations and nurse plant effects in patches of high-Andean vegetation. J. Veg. Sci. 10: 357–364. https://doi.org/10.2307/3237064
- Oxelman, B., Lidén, M. & Berglund, D. 1997. Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Pl. Syst. Evol. 206: 393–410. https://doi.org/10.1007/Bf00987959
- Pax, F.A. & Hoffmann, K. 1934. Caryophyllaceae. Pp. 275–364 in: A Engler. (ed.), Die natürlichen Pflanzenfamilien, 2nd ed., vol. 16c. Berlin: Duncker & Humblot.
- Phillips, S.J., Anderson, R.P. & Schapire, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecol. Modelling 190: 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
- Popp, M. & Oxelman, B. 2001. Inferring the history of the polyploid Silene aegaea (Caryophyllaceae) using plastid and homoeologous nuclear DNA sequences. Molec. Phylogen. Evol. 20: 474–481. https://doi.org/10.1006/mpev.2001.0977
- Pusalkar, P.K. 2015. Redefining Thylacospermum and a new tribe Thylacospermeae (Caryophyllaceae). J. Jap. Bot. 90: 351–355.
- Pusalkar, P.K. & Singh, D.K. 2015. Taxonomic rearrangement of Arenaria (Caryophyllaceae) in Indian Western Himalaya. J. Jap. Bot. 90: 77–91.
- Rabeler, R.K. & Wagner, W.L. 2015. Eremogone (Caryophyllaceae): New combinations for Old World species. Phytokeys 50: 35–42. https://doi.org/10.3897/phytokeys.50.4736
- Rambaut, A. 2009. FigTree, version 1.3.1. Institute of Evolutionary Biology, University of Edinburgh. Available online at: https://tree.bio.ed.ac.uk/software/FigTree/
- Ree, R.H. & Smith, S.A. 2008. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 57: 4–14. https://doi.org/10.1080/10635150701883881
- Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
- Sadeghian, S., Zarre, S., Rabeler, R.K. & Heubl, G. 2015. Molecular phylogenetic analysis of Arenaria (Caryophyllaceae: tribe Arenarieae) and its allies inferred from nuclear DNA internal transcribed spacer and plastid DNA rps16 sequences. Bot. J. Linn. Soc. 178: 648–669. https://doi.org/10.1111/boj.12293
- Shao, H.B., Guo, Q.J., Chu, L.Y., Zhao, X.N., Su, Z.L., Hu, Y.C. & Cheng, J.F. 2007. Understanding molecular mechanism of higher plant plasticity under abiotic stress. Colloids Surfaces B, Biointerfaces 54: 37–45.
- Shaw, J., Lickey, E.B., Beck, J.T., Farmer, S.B., Liu, W., Miller, J., Siripun, K.C., Winder, C.T., Schilling, E.E. & Small, R.L. 2005. The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Amer. J. Bot. 92: 142–166. https://doi.org/10.3732/ajb.92.1.142
- Shi, Y.F., Li, J.J. & Li, B.Y. 1998. The uplift and environment effectivity of the Qinghai-Tibet Plateau during the late Cenozoic. Guangzhou: Guangdong Science and Technology Press.
- Singh, R.K. & Diwakar, P.G. 2010. Notes on some species of genus Arenaria L. (Caryophyllaceae). Indian J. Forest. 33: 432.
- Sun, B.N., Wu, J.Y., Ding, S.T., Li, X.C., Xie, S.P., Yan, D.F. & Lin, Z.C. 2011. Reconstructing Neogene vegetation and climates to infer tectonic uplift in western Yunnan, China. Paleogeogr. Paleoclimatol. Paleoecol. 304: 328–336. https://doi.org/10.1016/j.palaeo.2010.09.023b
- Sun, H., Niu, Y., Chen, Y.S., Song, B., Liu, C.Q., Peng, D.L., Chen, J.G. & Yang, Y. 2014. Survival and reproduction of plant species in the Qinghai-Tibet Plateau. J. Syst. Evol. 52: 378–396. https://doi.org/10.1111/Jse.12092
- Sun, H., Zhang, J.W., Deng, T. & Boufford, D.E. 2017. Origins and evolution of plant diversity in the Hengduan Mountains, China. Pl. Divers. 39: 161–166. https://doi.org/10.1016/j.pld.2017.09.004
- Swofford, D.L. 2002. PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sunderland, MA: Sinauer.
- Taberlet, P., Gielly, L., Pautou, G. & Bouvet, J. 1991. Universal primers for amplification of three noncoding regions of chloroplast DNA. Pl. Molec. Biol. 17: 1105–1109. https://doi.org/10.1007/BF00037152
- Tu, T.Y., Volis, S., Dillon, M.O., Sun, H. & Wen, J. 2010. Dispersals of Hyoscyameae and Mandragoreae (Solanaceae) from the New World to Eurasia in the early Miocene and their biogeographic diversification within Eurasia. Molec. Phylogen. Evol. 57: 1226–1237. https://doi.org/10.1016/j.ympev.2010.09.007
- Wang, C., Zhao, X., Liu, Z., Lippert, P.C., Graham, S.A., Coe, R.S., Yi, H., Zhu, L., Liu, S. & Li, Y. 2008. Constraints on the early uplift history of the Tibetan Plateau. Proc. Natl. Acad. Sci. U.S.A. 105: 4987–4992. https://doi.org/10.1073/pnas.0703595105
- Wang, E., Kirby, E., Furlong, K.P., van Soest, M., Xu, G., Shi, X., Kamp, P.J.J. & Hodges, K.V. 2012. Two-phase growth of high topography in eastern Tibet during the Cenozoic. Nature, Geosci. 5: 640–645. https://doi.org/10.1038/ngeo1538
- Wang, L.N., Ji, J.Q., Sun, D.X., Xu, Q.Q., Tu, J.Y., Zhang, Z.C. & Han, B.F. 2010. The uplift history of south-western Tianshan-Implications from AFT analysis of detrital samples. Chin. J. Geophys. (Chin. Ed.) 53: 931–945. https://doi.org/10.3969/j.issn.0001-5733.2010.04.018
- Wang, Y.J., Susanna, A., von Raab-Straube, E., Milne, R. & Liu, J.Q. 2009. Island-like radiation of Saussurea (Asteraceae: Cardueae) triggered by uplifts of the Qinghai-Tibetan Plateau. Biol. J. Linn. Soc. 97: 893–903. https://doi.org/10.1111/j.1095-8312.2009.01225.x
- Wen, J., Zhang, J., Nie, Z.L., Zhong, Y. & Sun, H. 2014. Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Frontiers Genet. (Lausanne) 5: 4. https://doi.org/10.3389/fgene.2014.00004
- Williams, F. 1898. A revision of the genus Arenaria. Bot. J. Linn. Soc. 33: 326–437. https://doi.org/10.1111/j.1095-8339.1898.tb00290.x
10.1111/j.1095-8339.1898.tb00290.x Google Scholar
- Wu, C.Y., Ke, P., Zhou, L.H., Tang, C.L. & Lu, D.Q. 1996. Caryophyllaceae. Pp. 47–449 in: C.L Tang. (ed.), Flora Reipublicae Popularis Sinicae, vol. 26. Beijing: Science Press.
- Wu, C.Y., Zhou, L.H. & Wagner, W. 2001. Arenaria L. Pp. 40–66 in: Flora of China Editorial Committee (ed.), Flora of China, vol. 6. Beijing: Science Press; St. Louis: Missouri Botanical Garden Press.
- Wu, S.G. & Feng, Z.J. 1996. The biology and human physiology in the Hoh Xili region. Beijing: Science Press.
- Xu, B., Li, Z.M. & Sun, H. 2014. Seed plants of alpine subnival in Hengduan Mountains. Beijing: Science Press.
- Yang, Y., Niu, Y., Cavieres, L.A. & Sun, H. 2010. Positive associations between the cushion plant Arenaria polytrichoides (Caryophyllaceae) and other alpine plant species increase with altitude in the Sino-Himalayas. J. Veg. Sci. 21: 1048–1057. https://doi.org/10.1111/j.1654-1103.2010.01215.x
- Yu, Y., Harris, A.J. Blair, C. & He, X.J. 2015. RASP (Reconstruct Ancestral State in Phylogenies): A tool for historical biogeography. Molec. Phylogen. Evol. 87: 46–49. https://doi.org/10.1016/j.ympev.2015.03.008
- Yue, J.P., Sun, H., Baum, D.A., Li, J.H., Al-Shehbaz, I.A. & Ree, R. 2009. Molecular phylogeny of Solms-Laubachia (Brassicaceae) s.l., based on multiple nuclear and plastid DNA sequences, and its biogeographic implications. J. Syst. Evol. 47: 402–415. https://doi.org/10.1111/j.1759-6831.2009.00041.x
- Zhang, J.W., Nie, Z.L., Wen, J & Sun, H. 2011. Molecular phylogeny and biogeography of three closely related genera, Soroseris, Stebbinsia, and Syncalathium (Asteraceae, Cichorieae), endemic to the Tibetan Plateau, SW China. Taxon 60: 15–26. https://doi.org/10.1002/tax.601003
- Zhang, Y.L., Li, B.Y. & Zheng, D. 2002. A discussion on the boundary and area of the Tibetan plateau in China. Geogr. Res. 21: 1–8. https://doi.org/10.11821/yj2002010001
- Zheng, B.X., Xu, Q.Q. & Shen, Y.P. 2002. The relationship between climate change and Quaternary glacial cycles on the Qinghai-Tibetan Plateau: Review and speculation. Quatern. Int. 97–98: 93–101. https://doi.org/10.1016/S1040-6182(02)00054-X
- Zhou, L.H. 1980. Taxa nova generis Arenaria. Acta Phytotax. Sin. 18: 357–361.
- Zhou, L.H. 1996. On the geographical distribution of Arenaria L. Acta Phytotax. Sin. 3: 229–241.
- Zhou, Z., Hong, D.Y., Niu, Y., Li, G.D., Nie, Z.L., Wen, J. & Sun, H. 2013. Phylogenetic and biogeographic analyses of the Sino-Himalayan endemic genus Cyananthus (Campanulaceae) and implications for the evolution of its sexual system. Molec. Phylogen. Evol. 68: 482–497. https://doi.org/10.1016/j.ympev.2013.04.027
- Zhu, W.D., Nie, Z.L., Wen, J. & Sun, H. 2013. Molecular phylogeny and biogeography of Astilbe (Saxifragaceae) in Asia and eastern North America. Bot. J. Linn. Soc. 171: 377–394. https://doi.org/10.1111/j.1095-8339.2012.01318.x
