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.
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References
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
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
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
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
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
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
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
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
Bunge A (1852) Beitrag zur Kentniss der Flor Russlands. St Petersburg, pp 321–323
Cannon MJ, Cannon JFM (1984) A revision of Morinaceae (Magnoliophyta-Dipsacales). Bull Br Mus Botany 12(1):1–15
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
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
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
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
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 13:13–15
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
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
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
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
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
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
Flantua SG, Hooghiemstra H (2018) Historical connectivity and mountain biodiversity. Mountains, Climate and Biodiversity. Wiley Blackwell, Chichester, UK, pp 171–185
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
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
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
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
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
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
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
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
Hijmans RJ (2020) raster: Geographic Data Analysis and Modeling. R package version 3.0-12. https://CRAN.R-project.org/package=raster
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
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
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
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
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
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
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
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
Li BY (1989) Geomorphologic regionalization of the Hengduan Mountainous region. J Mt Res 7:13–20
Li XW, Li J (1993) A preliminary floristic study on the seed plants from the region of Hengduan Mountain. Acta BotanicaYunnanica 15:217–231
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford University Press, Oxford, pp 36–171
Nei M, Takeo M, Ranajit C (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
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
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
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
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
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
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
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
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
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
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
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
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
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
Stockhouse RE (1973) Biosystematic Studies of Oenothera L. Subgenus Pachylophus. Ph.D. diss., Colorado State University, Fort Collins, Colorado, USA
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
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
Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (* and other methods), v. 4.0b4a. Sinauer Associates, Sunderland, MA
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
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
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
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
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
Ward FK (1921) The Mekong-Salween Divide as a geographical barrier. Geogr J 58:49–56
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
Wu ZY (1988) Hengduan mountain flora and her significance. J Jpn Botany 63:297–311
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
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
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
Yang QE, Landrein S, Osborne J, Borosova R (2011) Flora of China, vol 19. Science Press, Beijing, pp 649–650
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
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
Zhang RZ, Zheng D, Yang QY, Liu YH (1997) Physical geography of Hengduan mountains. Science Press, Beijing
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
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
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
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
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
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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.
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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.
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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.
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Mu, QY., Yu, CC., Wang, Y. et al. Comparative phylogeography of Acanthocalyx (Caprifoliaceae) reveals distinct genetic structures in the Himalaya–Hengduan Mountains. Alp Botany 132, 153–168 (2022). https://doi.org/10.1007/s00035-021-00262-x
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DOI: https://doi.org/10.1007/s00035-021-00262-x