Skip to main content

Comparative phylogeography of Acanthocalyx (Caprifoliaceae) reveals distinct genetic structures in the Himalaya–Hengduan Mountains

Abstract

The Himalaya–Hengduan Mountain (HHM) region consists of two global biodiversity hotspots characterized by a high degree of plant endemism. However, little is known about how these endemic species are formed and maintained in relation to the regional geomorphology of the past or current time. Thus, this study investigated the genetic structure of the herbaceous genus Acanthocalyx (Caprifoliaceae) endemic to the HHM to demonstrate if major geographic or ecological barriers in the HHM region have influenced its phylogeographic patterns. Our analyses revealed distinct genetic structures within A. alba and A. nepalensis and indicated that A. delavayi may have recently evolved from isolated peripheral populations of A. nepalensis. In particular, we not only confirmed a well-known genetic structure of alpine plants between the Himalayas and the Hengduan Mountains but also discovered a notable floristic boundary (bounded by 30° to 31°N latitude) within the Hengduan Mountains from A. alba. This study provides new insights into the dispersal and intraspecific genetic variation of Acanthocalyx and highlights the importance of geomorphological features for the diversification of HHM alpine flora.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data availability

Please see appendix file.

Code availability

Not applicable.

References

  1. An ZS, Kutzbach JE, Prell WL, Porter SC (2001) Evolution of Asian monsoons and phased uplift of the Himalaya–Tibetan plateau since Late Miocene times. Nature 411:62–66. https://doi.org/10.1038/35075035

    CAS  Article  Google Scholar 

  2. Antonelli A, Kissling WD, Flantua SG, Bermúdez MA, Mulch A, Muellner-Riehl AN, Kreft H, Linder HP, Badgley C, Fjeldså J (2018) Geological and climatic influences on mountain biodiversity. Nat Geosci 11:718–725. https://doi.org/10.1038/s41561-018-0236-z

    CAS  Article  Google Scholar 

  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Barraclough TG, Vogler AP (2000) Detecting the geographical pattern of speciation from species-level phylogenies. Am Nat 155:419–434. https://doi.org/10.1086/303332

    Article  PubMed  Google Scholar 

  5. Bell CD, Donoghue MJ (2005) Dating the Dipsacales: comparing models, genes, and evolutionary implications. Am J Bot 92:284–296. https://doi.org/10.3732/ajb.92.2.284

    CAS  Article  PubMed  Google Scholar 

  6. Bouckaert R, Heled J, Kühnert 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:e1003537. https://doi.org/10.1371/journal.pcbi.1003537

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15:e1006650. https://doi.org/10.1371/journal.pcbi.1006650

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Brzosko E, Wróblewska A, Ratkiewicz M (2002) Allozyme differentiation and spatial clonal structure in isolated Cypripedium calceolus populations (NE Poland). Mol Ecol 11:2499–2509. https://doi.org/10.1046/j.1365-294X.2002.01630.x

    CAS  Article  PubMed  Google Scholar 

  9. Bunge A (1852) Beitrag zur Kentniss der Flor Russlands. St Petersburg, pp 321–323

  10. Cannon MJ, Cannon JFM (1984) A revision of Morinaceae (Magnoliophyta-Dipsacales). Bull Br Mus Botany 12(1):1–15

    Google Scholar 

  11. Clark M et al (2004) Surface uplift, tectonics, and erosion of eastern Tibet from large-scale drainage patterns. Tectonics. https://doi.org/10.1029/2002TC001402

    Article  Google Scholar 

  12. Deng T, Abbott RJ, Li WQ, Sun H, Volis S (2019) Genetic diversity hotspots and refugia identified by mapping multi-plant species haplotype diversity in China. Israel J Plant Sci 66:136–151. https://doi.org/10.1163/22238980-20191083

    Article  Google Scholar 

  13. Ding WN, Ree RH, Spicer RA, Xing YW (2020) Ancient orogenic and monsoon-driven assembly of the world’s richest temperate alpine flora. Science 369:578–581. https://doi.org/10.1126/science.abb4484

    CAS  Article  PubMed  Google Scholar 

  14. Donoghue MJ, Bell CD, Winkworth RC (2003) The evolution of reproductive characters in Dipsacales. Int J Plant Sci 164:S453–S464. https://doi.org/10.1086/376874

    Article  Google Scholar 

  15. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 13:13–15

    Google Scholar 

  16. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Du FK, Hou M, Wang W, Mao K, Hampe A (2017) Phylogeography of Quercus aquifolioides provides novel insights into the Neogene history of a major global hotspot of plant diversity in south-west China. J Biogeogr 44:294–307. https://doi.org/10.1111/jbi.12836

    Article  Google Scholar 

  18. Duminil J, Fineschi S, Hampe A, Jordano P, Salvini D, Vendramin GG, Petit RJ (2007) Can population genetic structure be predicted from life-history traits? Am Nat 169:662–672. https://doi.org/10.1086/513490

    Article  PubMed  Google Scholar 

  19. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  PubMed Central  Google Scholar 

  20. Feng L, Zheng QJ, Qian ZQ, Yang J, Zhang YP, Li ZH, Zhao GF (2016a) Genetic structure and evolutionary history of three alpine sclerophyllous oaks in East Himalaya–Hengduan Mountains and adjacent regions. Front Plant Sci 7:1688. https://doi.org/10.3389/fpls.2016.01688

    Article  PubMed  PubMed Central  Google Scholar 

  21. Feng B, Zhao Q, Xu J, Qin J, Yang ZL (2016b) Drainage isolation and climate change-driven population expansion shape the genetic structures of Tuber indicum complex in the Hengduan Mountains region. Sci Rep 6:1–10. https://doi.org/10.1038/srep21811

    CAS  Article  Google Scholar 

  22. Flantua SG, Hooghiemstra H (2018) Historical connectivity and mountain biodiversity. Mountains, Climate and Biodiversity. Wiley Blackwell, Chichester, UK, pp 171–185

  23. Flora of the Pan-Himalayas (2011) General guidelines. J Syst Evol 49(6):617–624. https://doi.org/10.1111/j.1759-6831.2011.00146.x

    Article  Google Scholar 

  24. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925. https://doi.org/10.1017/S0016672397002966

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Gao QB et al (2016) Phylogeographic study revealed microrefugia for an endemic species on the Qinghai-Tibetan Plateau: Rhodiola chrysanthemifolia (Crassulaceae). Plant Syst Evol 302:1179–1193. https://doi.org/10.1007/s00606-016-1324-4

    Article  Google Scholar 

  26. Gao YD, Gao XF, Harris A (2019) Species boundaries and parapatric speciation in the complex of alpine shrubs, Rosa sericea (Rosaceae), based on population genetics and ecological tolerances. Front Plant Sci 10:321. https://doi.org/10.3389/fpls.2019.00321

    Article  PubMed  PubMed Central  Google Scholar 

  27. Gavrilets S, Li H, Vose MD (2000) Patterns of parapatric speciation. Evolution 54:1126–1134. https://doi.org/10.1111/j.0014-3820.2000.tb00548.x

    CAS  Article  PubMed  Google Scholar 

  28. Guo JL, Zhang XY, Zhang JW, Li ZM, Sun WG, Zhang YH (2016) Genetic diversity of Meconopsis integrifolia (Maxim.) Franch. In the East Himalaya–Hengduan Mountains inferred from fluorescent amplified fragment length polymorphism analysis. Biochem Syst Ecol 69:67–75. https://doi.org/10.1016/j.bse.2016.08.007

    CAS  Article  Google Scholar 

  29. He K, Jiang XL (2014) Sky islands of southwest China. I: an overview of phylogeographic patterns. Chin Sci Bull 59:585–597. https://doi.org/10.1007/s11434-013-0089-1

    Article  Google Scholar 

  30. He X, Burgess KS, Yang XF, Ahrends A, Gao LM, Li DZ (2019) Upward elevation and northwest range shifts for alpine Meconopsis species in the Himalaya–Hengduan Mountains region. Ecol Evol 9:4055–4064. https://doi.org/10.1002/ece3.5034

    Article  PubMed  PubMed Central  Google Scholar 

  31. Hijmans RJ (2020) raster: Geographic Data Analysis and Modeling. R package version 3.0-12. https://CRAN.R-project.org/package=raster

  32. Hughes CE, Atchison GW (2015) The ubiquity of alpine plant radiations: from the Andes to the Hengduan Mountains. New Phytol 207:275–282. https://doi.org/10.1111/nph.13230

    Article  PubMed  Google Scholar 

  33. Jian HY, Zhang YH, Qiu XQ, Yan HJ, Wang QG, Zhang H, Sun H (2016) Yalongjiang River has had an important role in the dispersal and divergence of Rosa soulieana in the Hengduan Mountains of China. PLoS ONE 11:e0158586. https://doi.org/10.1371/journal.pone.0158586

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Jiang C, Tan K, Ren MX (2017) Effects of monsoon on distribution patterns of tropical plants in Asia. Chin J Plant Ecol 41:1103–1112. https://doi.org/10.17521/cjpe.2017.0070

    Article  Google Scholar 

  35. Kalisz S, Nason JD, Hanzawa FM, Tonsor SJ (2001) Spatial population genetic structure in Trillium grandiflorum: the roles of dispersal, mating, history, and selection. Evolution 55:1560–1568. https://doi.org/10.1111/j.0014-3820.2001.tb00675.x

    CAS  Article  PubMed  Google Scholar 

  36. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  38. Körner C, Paulsen J, Spehn EM (2011) A definition of mountains and their bioclimatic belts for global comparisons of biodiversity data. Alp Bot 121:73–78. https://doi.org/10.1007/s00035-011-0094-4

    Article  Google Scholar 

  39. Levin SA, Muller-Landau HC, Nathan R, Chave J (2003) The ecology and evolution of seed dispersal: a theoretical perspective. Annu Rev Ecol Evol Syst Biodivers Sci 34:575–604. https://doi.org/10.1146/annurev.ecolsys.34.011802.132428

    Article  Google Scholar 

  40. Li BY (1989) Geomorphologic regionalization of the Hengduan Mountainous region. J Mt Res 7:13–20

    Google Scholar 

  41. Li XW, Li J (1993) A preliminary floristic study on the seed plants from the region of Hengduan Mountain. Acta BotanicaYunnanica 15:217–231

    CAS  Google Scholar 

  42. 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). Mol Phylogenet Evol 59:412–424. https://doi.org/10.1016/j.ympev.2011.01.009

    Article  PubMed  Google Scholar 

  43. Li DB, Ou XK, Zhao JL, Li QJ (2019) An ecological barrier between the Himalayas and the Hengduan Mountains maintains the disjunct distribution of Roscoea. J Biogeogr 47:326–341. https://doi.org/10.1111/jbi.13729

    Article  Google Scholar 

  44. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187

    CAS  Article  Google Scholar 

  45. Liu JQ, Sun YS, Ge XJ, Gao LM, Qiu YX (2012) Phylogeographic studies of plants in China: advances in the past and directions in the future. J Syst Evol 50:267–275. https://doi.org/10.1111/j.1759-6831.2012.00214.x

    Article  Google Scholar 

  46. 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 199:1093–1108. https://doi.org/10.1111/nph.12336

    Article  PubMed  Google Scholar 

  47. Liu HR, Gao QB, Zhang FQ, Khan G, Chen SL (2018) Westwards and northwards dispersal of Triosteum himalayanum (Caprifoliaceae) from the Hengduan Mountains region based on chloroplast DNA phylogeography. PeerJ 6:e4748. https://doi.org/10.7717/peerj.4748

    Article  PubMed  PubMed Central  Google Scholar 

  48. Loo YY, Billa L, Singh A (2015) Effect of climate change on seasonal monsoon in Asia and its impact on the variability of monsoon rainfall in Southeast Asia. Geosci Front 6:817–823. https://doi.org/10.1016/j.gsf.2014.02.009

    Article  Google Scholar 

  49. Luo D, Yue JP, Sun WG, Xu B, Li ZM, Comes HP, 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

    Article  Google Scholar 

  50. Luo D, Xu B, Li ZM, 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

    Article  Google Scholar 

  51. Meng LH, Chen G, Li ZH, Yang YP, Wang ZK, Wang LY (2015) Refugial isolation and range expansions drive the genetic structure of Oxyria sinensis (Polygonaceae) in the Himalaya–Hengduan Mountains. Sci Rep 5:10396. https://doi.org/10.1038/srep10396

    Article  PubMed  PubMed Central  Google Scholar 

  52. Meng HH, Su T, Gao XY, Li J, Jiang XL, Sun H, Zhou ZK (2017) Warm-cold colonization: response of oaks to uplift of the Himalaya–Hengduan Mountains. Mol Ecol 26:3276–3294. https://doi.org/10.1111/mec.14092

    CAS  Article  PubMed  Google Scholar 

  53. Miller M, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE). https://www.phylo.org

  54. Mosbrugger V, Favre A, Muellner-Riehl AN, Päckert M, Mulch A (2018) Cenozoic evolution of geobiodiversity in the Tibeto-Himalayan region. Mountains, Climate, and Biodiversity. Wiley Blackwell, Chichester, UK, pp 429–448

  55. Mu QY, Yu CC, Xing YW (2020) Notes on the type specimen of Acanthocalyx delavayi (Caprifoliaceae) at Herbarium of the National Museum of Natural History in Paris (P). Phytotaxa 451:90–92. https://doi.org/10.11646/phytotaxa.451.1.8

    Article  Google Scholar 

  56. Muellner-Riehl AN (2019) Mountains as evolutionary arenas: patterns, emerging approaches, paradigm shifts, and their implications for plant phylogeographic research in the Tibeto-Himalayan Region. Front Plant Sci 10:195. https://doi.org/10.3389/fpls.2019.00195

    Article  PubMed  PubMed Central  Google Scholar 

  57. Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford University Press, Oxford, pp 36–171

    Google Scholar 

  58. Nei M, Takeo M, Ranajit C (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  59. Ngamriabsakul C, Newman M, Cronk Q (2000) Phylogeny and disjunction in Roscoea (Zingiberaceae). Edinb J Bot 57:39–61. https://doi.org/10.1017/S0960428600000032

    Article  Google Scholar 

  60. Niu YT, Ye JF, Zhang JL, Wan JZ, Yang T, Wei XX, Lu LM, Li JH, Chen ZD (2018) Long-distance dispersal or postglacial contraction? Insights into disjunction between Himalaya–Hengduan Mountains and Taiwan in a cold-adapted herbaceous genus, Triplostegia. Ecol Evol 8:1131–1146. https://doi.org/10.1002/ece3.3719

    Article  PubMed  Google Scholar 

  61. Ohsawa T, Ide Y (2008) Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Glob Ecol Biogeogr 17:152–163. https://doi.org/10.1111/j.1466-8238.2007.00357.x

    Article  Google Scholar 

  62. Owen LA, Dortch JM (2014) Nature and timing of Quaternary glaciation in the Himalayan-Tibetan orogen. Quatern Sci Rev 88:14–54. https://doi.org/10.1016/j.quascirev.2013.11.016

    Article  Google Scholar 

  63. Pons O, Petit R (1996) Measwring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245. https://doi.org/10.1093/genetics/144.3.1237

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  65. Rahbek C, Borregaard MK, Antonelli A, Colwell RK, Holt BG, Nogues-Bravo D, Rasmussen CM, Richardson K, Rosing MT, Whittaker RJ (2019) Building mountain biodiversity: geological and evolutionary processes. Science 365:1114–1119. https://doi.org/10.1126/science.aax0151

    CAS  Article  PubMed  Google Scholar 

  66. Rana HK, Luo D, Rana SK, Sun H (2020) Geological and climatic factors affect the population genetic connectivity in Mirabilis himalaica (Nyctaginaceae): insight from phylogeography and dispersal corridors in the Himalaya–Hengduan biodiversity hotspot. Front Plant Sci 10:1721. https://doi.org/10.3389/fpls.2019.01721

    Article  PubMed  PubMed Central  Google Scholar 

  67. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569. https://doi.org/10.1093/oxfordjournals.molbev.a040727

    CAS  Article  PubMed  Google Scholar 

  68. Ronquist F et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  69. Rozas J, Ferrer-Mata A, Sánchez-Delbarrio JC, Guirao Rico S, Librado P, Ramos Onsins SE, Sánchez Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248

    CAS  Article  PubMed  Google Scholar 

  70. Salick J, Fang ZD, Hart R (2019) Rapid changes in eastern Himalayan alpine flora with climate change. Am J Bot 106:520–530. https://doi.org/10.1002/ajb2.1263

    Article  PubMed  Google Scholar 

  71. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. https://doi.org/10.1093/bioinformatics/btl446

    CAS  Article  PubMed  Google Scholar 

  72. Stockhouse RE (1973) Biosystematic Studies of Oenothera L. Subgenus Pachylophus. Ph.D. diss., Colorado State University, Fort Collins, Colorado, USA

  73. Sullivan J, Smith ML, Espíndola A, Ruffley M, Rankin A, Tank D, Carstens B (2019) Integrating life history traits into predictive phylogeography. Mol Ecol 28:2062–2073. https://doi.org/10.1111/mec.15029

    Article  PubMed  Google Scholar 

  74. Sun H, Zhang JW, Deng T, Boufford DE (2017) Origins and evolution of plant diversity in the Hengduan Mountains, China. Plant Divers 39:161. https://doi.org/10.1016/j.pld.2017.09.004

    Article  PubMed  PubMed Central  Google Scholar 

  75. Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (* and other methods), v. 4.0b4a. Sinauer Associates, Sunderland, MA

  76. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Article  Google Scholar 

  77. Vásquez DL, Balslev H, Hansen MM, Sklenář P, Romoleroux K (2016) Low genetic variation and high differentiation across sky island populations of Lupinus alopecuroides (Fabaceae) in the northern Andes. Alp Bot 126:135–142. https://doi.org/10.1007/s00035-016-0165-7

    Article  Google Scholar 

  78. Wang FY, Ge XJ, Gong X, Hu CM, Hao G (2008) Strong genetic differentiation of Primula sikkimensis in the East Himalaya–Hengduan Mountains. Biochem Genet 46:75–87. https://doi.org/10.1007/s10528-007-9131-9

    CAS  Article  PubMed  Google Scholar 

  79. Wang P, Scherler D, Liu-Zeng J, Mey J, Avouac J-P, Zhang Y, Shi D (2014) Tectonic control of Yarlung Tsangpo Gorge revealed by a buried canyon in Southern Tibet. Science 346:978–981. https://doi.org/10.1126/science.1259041

    CAS  Article  PubMed  Google Scholar 

  80. Wang HX, Liu H, Moore MJ, Landrein S, Liu B, Zhu ZX, Wang HF (2020) Plastid phylogenomic insights into the evolution of the Caprifoliaceae sl (Dipsacales). Mol Phylogenet Evol 142:106641. https://doi.org/10.1016/j.ympev.2019.106641

    Article  PubMed  Google Scholar 

  81. Ward FK (1921) The Mekong-Salween Divide as a geographical barrier. Geogr J 58:49–56

    Article  Google Scholar 

  82. Wroblewska A, Brzosko E, Czarnecka B, Nowosielski J (2003) High levels of genetic diversity in populations of Iris aphylla L. (Iridaceae), an endangered species in Poland. Bot J Linn Soc 142:65–72. https://doi.org/10.1046/j.1095-8339.2003.00162.x

    Article  Google Scholar 

  83. Wu ZY (1988) Hengduan mountain flora and her significance. J Jpn Botany 63:297–311

    Google Scholar 

  84. Wu YJ, Colwell RK, Rahbek C, Zhang CL, Quan Q, Wang CK, Lei FM (2013) Explaining the species richness of birds along a subtropical elevational gradient in the Hengduan Mountains. J Biogeogr 40:2310–2323. https://doi.org/10.1111/jbi.12177

    Article  Google Scholar 

  85. Xing YW, Ree RH (2017) Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc Natl Acad Sci 114:E3444–E3451. https://doi.org/10.1073/pnas.1616063114

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  86. Yan Y, Carter A, Huang CY, Chan LS, Hu XQ, Lan Q (2012) Constraints on Cenozoic regional drainage evolution of SW China from the provenance of the Jianchuan Basin. Geochem Geophys Geosyst. https://doi.org/10.1029/2011GC003803

    Article  Google Scholar 

  87. Yang QE, Landrein S, Osborne J, Borosova R (2011) Flora of China, vol 19. Science Press, Beijing, pp 649–650

    Google Scholar 

  88. Yao YH, Zhang BP, Han F, Pang Y (2010) Diversity and geographical pattern of altitudinal belts in the Hengduan Mountains in China. J Mt Sci 7:123–132. https://doi.org/10.1007/s11629-010-1011-9

    Article  Google Scholar 

  89. Yu HB, Favre A, Sui X, Chen Z, Qi W, Xie GW, van Kleunen M (2019) Mapping the genetic patterns of plants in the region of the Qinghai-Tibet Plateau: implications for conservation strategies. Divers Distrib 25:310–324. https://doi.org/10.1111/ddi.12847

    Article  Google Scholar 

  90. Zhang RZ, Zheng D, Yang QY, Liu YH (1997) Physical geography of Hengduan mountains. Science Press, Beijing

    Google Scholar 

  91. Zhang DC, Boufford DE, Ree RH, Sun H (2009a) The 29°N latitudinal line: an important division in the Hengduan Mountains, a biodiversity hotspot in southwest China. Nord J Bot 27:405–412. https://doi.org/10.1111/j.1756-1051.2008.00235.x

    CAS  Article  Google Scholar 

  92. Zhang DC, Zhang YH, Boufford DE, Sun H (2009b) Elevational patterns of species richness and endemism for some important taxa in the Hengduan Mountains, southwestern China. Biodivers Conserv 18:699–716. https://doi.org/10.1007/s10531-008-9534-x

    Article  Google Scholar 

  93. Zhang TC, Comes HP, Sun H (2011) Chloroplast phylogeography of Terminalia franchetii (Combretaceae) from the eastern Sino-Himalayan region and its correlation with historical river capture events. Mol Phylogenet Evol 60:1–12. https://doi.org/10.1016/j.ympev.2011.04.009

    CAS  Article  PubMed  Google Scholar 

  94. Zhang JM, Lopez-Pujol J, Gong X, Wang HF, Vilatersana R, Zhou SL (2018) Population genetic dynamics of Himalayan-Hengduan tree peonies, Paeonia subsect Delavayanae. Mol Phylogenet Evol 125:62–77. https://doi.org/10.1016/j.ympev.2018.03.003

    Article  PubMed  Google Scholar 

  95. Zhao JL, Gugger PF, Xia YM, Li QJ (2016) Ecological divergence of two closely related Roscoea species associated with late Quaternary climate change. J Biogeogr 43:1990–2001. https://doi.org/10.1111/jbi.12809

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the Public Technology Service Center, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences (CAS) for providing the Experimental Platform for molecular analyses. We are grateful to the comments and supports by Dr. Dong Luo. This work was financially supported by the National Science Foundation of China (U1802242), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB31000000), and the Open Fund from CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden.

Funding

The National Science Foundation of China (U1802242), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB31000000), and the Open Fund from CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden.

Author information

Affiliations

Authors

Contributions

Q-YM, C-CY, Y-WX for conceptualization, drafting the manuscript, and revising the manuscript critically for important intellectual content; Q-YM, HW, T-SH for design of the study, and revising the manuscript critically for important intellectual content; Q-YM, YW for analysis and/or interpretation of data; W-ND and Q-JZ for review and editing; SLL, Q-YZ, CP, and Z-YH for data collecting and field works.

Corresponding author

Correspondence to Yao-Wu Xing.

Ethics declarations

Conflict of interest

Not applicable.

Human and animals rights

Not applicable.

Ethics approval

Not applicable.

Consent to participate.

All the authors have given permissions to participate in the research.

Consent for publication.

All the authors are in agreement with the publication of the research in the journal.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 33151 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mu, QY., Yu, CC., Wang, Y. et al. Comparative phylogeography of Acanthocalyx (Caprifoliaceae) reveals distinct genetic structures in the Himalaya–Hengduan Mountains. Alp Botany (2021). https://doi.org/10.1007/s00035-021-00262-x

Download citation

Keywords

  • Himalaya–Hengduan Mountains
  • Alpine plant
  • Molecular dating
  • Population dynamics
  • Peripatric speciation