Abstract
The northern parts of Yunnan belong to ‘Mountains of SW China’ biodiversity hot spot, one of the most species-rich areas on earth. Although some progress, relatively little attention has been given to explore the evolutionary history of the fern diversity of this hot spot. According to recent progress, Yunnan exhibits the heterogeneity of species diversity among regions. In this study, we focused on the Dehong Dai-Jingpo Autonomous Prefecture, an overlooked area in western Yunnan geographically and geologically, which is connected to SE Tibet and NE Myanmar; thus, the flora of this region will likely share several unique taxa, but this pattern may be obscured by the lack of reported distributions. To examine this, we conducted floristic investigation targeting rare species shared between Dehong and adjacent areas in Lepisorus. We performed morphological, phylogenetical, and biogeographical analyses with the accessions obtained. Lepisorus cespitosus was firstly found in Dehong, which was previously only known from the type location in SE Tibet. Our analyses revealed that L. cespitosus is a lineage morphologically and phylogenetically isolated from all other sections of Lepisorus. Divergence time estimates and ancestral area reconstruction supported that L. cespitosus is a relict species survived in this region since the Late Miocene. Our results showed the affinity in the flora between western Yunnan and SE Tibet and supported the hypothesis that this region has served as a climate refugia for relict species during the Cenozoic. Thus, we propose that more attention should be given to floristic investigation in this area and adjacent regions.
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Voucher specimen used in this study was deposited in HIBIC. All sequences generated in this study were uploaded in GenBank.
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Nexus file used for phylogenetic analysis can be downloaded as Supplementary Data.
References
Bouckaert R, Heled J, Kühnert D et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:1–6. https://doi.org/10.1371/journal.pcbi.1003537
Chen CC, Hyvönen J, Schneider H (2020) Exploring phylogeny of the microsoroid ferns (Polypodiaceae) based on six plastid DNA markers. Molec Phylogen Evol 143:106665. https://doi.org/10.1016/j.ympev.2019.106665
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and high-performance computing. Nat Meth 9:772. https://doi.org/10.1038/nmeth.2109
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Farnsworth A, Lunt DJ, Robinson SA et al (2019) Past East Asian monsoon evolution controlled by paleogeography, not CO2. Sci Advances 5:eaax1697. https://doi.org/10.1126/sciadv.aax1697
Fujiwara T, Serizawa S, Watano Y (2018) Phylogenetic analysis reveals the origins of tetraploid and hexaploid species in the Japanese Lepisorus thunbergianus (Polypodiaceae) complex. J Pl Res 131:945–959. https://doi.org/10.1007/s10265-018-1061-6
He LY, Tang CQ, Wu ZL, Wang HC, Ohsawa M, Yan K (2015) Forest structure and regeneration of the Tertiary relict Taiwania cryptomerioides in the Gaoligong Mountains, Yunnan, southwestern China. Phytocoenologia 45:135–156. https://doi.org/10.1127/phyto/2015/0038
Huang YJ, Su T, Zhou ZK (2016) Late Pliocene diversity and distribution of Drynaria (Polypodiaceae) in western Yunnan explained by forest vegetation and humid climates. Pl Diversity 38:194–200. https://doi.org/10.1016/j.pld.2016.06.003
Jacques FMB, Su T, Zhou ZK (2013) The first fossil Microsoroid fern (Palaeosorum ellipticum gen. et sp. nov.) from the middle Miocene of Yunnan, SW China. J Syst Evol 51:758–764. https://doi.org/10.1111/jse.12030
Khine PK, Fraser-Jenkins C, Lindsay S, Middleton D, Miehe G, Thomas P, Kluge J (2017) A contribution toward the knowledge of ferns and lycophytes from northern and northwestern Myanmar. Amer Fern J 107:219–256. https://doi.org/10.1640/0002-8444-107.4.219
Larsson A (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30:3276–3278. https://doi.org/10.1093/bioinformatics/btu531
Li R, Yue J (2019) A phylogenetic perspective on the evolutionary processes of floristic assemblages within a biodiversity hotspot in eastern Asia. J Syst Evol (Early View). https://doi.org/10.1111/jse.12539
Lin YX (2000) Lepisorioideae. In: Lin YX (ed) Flora Reipublicae Popularis Sinicae, 6(3). Science Press, Beijing, pp 32–115
Liu HM, Zhang XC, Wang MP, Shang H, Zhou SL, Yan YH, Wei XP, Xu WB, Schneider H (2016) Phylogenetic placement of the enigmatic fern genus Trichoneuron informs on the infra-familial relationship of Dryopteridaceae. Pl Syst Evol 302:319–332. https://doi.org/10.1007/s00606-015-1265-3
Liu HM, Schneider H, Yu Y, Fujiwara T, Khine PK (2019a) Towards the conservation of the Mesozoic relict fern Christensenia: a fern species with extremely small populations in China. J Pl Res 132:601–616. https://doi.org/10.1007/s10265-019-01140-8
Liu HM, Shen JY, Liang ZL, Peng F, Wang WZ, Yang ZW, Wang S, Parris B, Schneider H (2019b) Two out of one: revising the diversity of the epiphytic fern genus Scleroglossum (Polypodiaceae, Grammitidoideae) in southern China. PhytoKeys 130:115–133. https://doi.org/10.3897/phytokeys.130.33979
López-Pujol J, Zhang FM, Sun HQ, Ying TS, Ge S (2011) Centres of plant endemism in China: places for survival or for speciation? J Biogeogr 38:1267–1280. https://doi.org/10.1111/j.1365-2699.2011.02504.x
Matzke NJ (2013) Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Frontiers Biogeogr 5:4. https://doi.org/10.21425/f5fbg19694
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov 2010, IEEE, New Orleans, pp 1–8
PPGI (2016) A community-derived classification for extant lycophytes and ferns. J Syst Evol 54:563–603. https://doi.org/10.1111/jse.12229
Qi XP, Zhang XC (2009) Taxonomic revision of Lepisorus (J. Sm.) Ching sect. Lepisorus (Polypodiaceae) from China. J Syst Evol 47:581–598. https://doi.org/10.1111/j.1759-6831.2009.00056
Qi XP, Zhang XC, Wei R (2010) Taxonomic revision of Lepisorus sect. Sclerophyllon (Polypodiaceae) from China. Acta Bot Yunnanica 17:55–64
Rambaut A, Drummond AJ (2013) Tracer V1.6. Available at: http://beast.bio.ed.ac.uk/Tracer
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (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
Schneider H (2016) Tempo and mode in the evolution of morphological disparity in the Neotropical fern genus Pleopeltis. Biol J Linn Soc 118:929–939. https://doi.org/10.1111/bij.12774
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Su T, Jacques FMB, Liu YS, Xiang J, Xing Y, Huang Y, Zhou ZK (2011) A new Drynaria (Polypodiaceae) from the Upper Pliocene of Southwest China. Rev Palaeobot Palynol 164:132–142. https://doi.org/10.1016/j.revpalbo.2010.11.011
Tang ZY, Wang ZH, Zheng CY, Fang JY (2006) Biodiversity in China’s mountains. Frontiers Ecol Environm 4:347–352. https://doi.org/10.1890/1540-9295(2006)004%5b0347:bicm%5d2,09.co;2
Tang CQ, Peng MC, He LY, Ohsawa M, Wang CY, Xie TH, Li WS, Li JP, Zhang HY, Li Y, Yang XM, Li GS (2013) Population persistence of a Tertiary relict tree Tetracentron sinense on the Ailao Mountains, Yunnan, China. J Pl Res 126:651–659. https://doi.org/10.1007/s10265-013-0559-1
Tang CQ, Matsui T, Ohashi H, Dong YF, Momohara A, Herrando-Moraira S, Qian S, Yang Y, Ohsawa M, Luu HT, Grote PJ, Krestov PV, Ben LP, Werger M, Robertson K, Hobohm C, Wang CY, Peng MC, Chen X, Wang HC, Su WH, Zhou R, Li S, He LY, Yan K, Zhu MY, Hu J, Yang RH, Li WJ, Tomita M, Wu ZL, Yan HZ, Zhang GF, He H, Yi SR, Gong H, Song K, Song D, Li XS, Zhang ZY, Han PB, Shen LQ, Huang DS, Luo K, López-Pujol J (2018) Identifying long-term stable refugia for relict plant species in East Asia. Nat Commun 9:1–14. https://doi.org/10.1038/s41467-018-06837-3
Testo W, Sundue M (2016) A 4000-species dataset provides new insight into the evolution of ferns A 4000-species dataset provides new insight into the evolution of ferns. Molec Phylogenet Evol 105:200–211. https://doi.org/10.1016/j.ympev.2016.09.003
Tsutsumi C, Chen CW, Larsson A, Hirayama Y, Kato M (2016) Phylogeny and classification of Davalliaceae on the basis of chloroplast and nuclear markers. Taxon 65:1236–1248. https://doi.org/10.12705/656.2
Wang L, Qi XP, Xiang QP, Heinrichs J, Schneider H, Zhang XC (2010a) Phylogeny of the paleotropical fern genus Lepisorus (Polypodiaceae, Polypodiopsida) inferred from four chloroplast DNA regions. Molec Phylogen Evol 54:211–225. https://doi.org/10.1016/j.ympev.2009.08.032
Wang L, Wu ZQ, Xiang QP, Heinrichs J, Schneider H, Zhang XC (2010b) A molecular phylogeny and a revised classification of tribe Lepisoreae (Polypodiaceae) based on an analysis of four plastid DNA regions. Bot J Linn Soc 162:28–38. https://doi.org/10.1111/j.1095-8339.2009.01018.x
Wang L, Wu ZQ, Bystriakova N, Ansell SW, Xiang QP, Heinrichs J, Schneider H, Zhang XC (2011) Phylogeography of the Sino-Himalayan fern Lepisorus clathratus on “the roof of the world”. PLoS ONE 6:e25896. https://doi.org/10.1371/journal.pone.0025896
Wang L, Schneider H, Wu ZQ, He LJ, Zhang XC, Xiang QP (2012a) Indehiscent sporangia enable the accumulation of local fern diversity at the Qinghai-Tibetan Plateau. BMC Evol Biol 12:158. https://doi.org/10.1186/1471-2148-12-158
Wang L, Schneider H, Zhang XC, Xiang QP (2012b) The rise of the Himalaya enforced the diversification of SE Asian ferns by altering the monsoon regimes. BMC Pl Biol 12:210. https://doi.org/10.1186/1471-2229-12-210
Wen WW, Xie SP, Liu KN, Sun BN, Wang L, Li H, Dao KQ (2013) Two species of fern macrofossil from the late Miocene of Lincang, Yunnan, China and their paleoecological implications. Palaeoworld 22:144–152. https://doi.org/10.1016/j.palwor.2013.06.004
Wu JY, Sun BN, Xie SP, Ding ST, Wen WW (2012) Dimorphic fronds and in situ spores of Drynaria (Polypodiaceae) from the upper Pliocene of Southwest China. Rev Palaeobot Palynol 172:1–9. https://doi.org/10.1016/j.revpalbo.2012.01.007
Xie SP, Li BK, Zhang SH, Shao Y, Wu JY, Sun BN (2016) First megafossil record of Neolepisorus (Polypodiaceae) from the late Miocene of Yunnan, Southwest China. Paläontol Z 90:413–423. https://doi.org/10.1007/s12542-016-0304-x
Xu CL, Huang J, Su T, Zhang XC, Li SF, Zhou ZK (2017) The first megafossil record of Goniophlebium (Polypodiaceae) from the Middle Miocene of Asia and its paleoecological implications. Palaeoworld 26:543–552. https://doi.org/10.1016/j.palwor.2017.01.006
Xu CL, Su T, Huang J, Huang YJ, Li SF, Zhao YS, Zhou ZK (2019a) Occurrence of Christella (Thelypteridaceae) in Southwest China and its indications of the paleoenvironment of the Qinghai-Tibetan Plateau and adjacent areas. J Syst Evol 57:169–179. https://doi.org/10.1111/jse.12452
Xu KW, Jiang L, Liao WB, Zhang LB (2019b) Asplenium simaoense (Aspleniaceae), a New Fern Species from Yunnan, China, Based on Morphological and Molecular Data. Syst Bot 44:494–500. https://doi.org/10.1600/036364419X15620113920554
Yang J, Gao Z, Sun W, Zhang C (2016) High regional genetic differentiation of an endangered relict plant Craigia yunnanensis and implications for its conservation. Pl Diversity 38:221–226. https://doi.org/10.1016/j.pld.2016.07.002
Zhang XC, Lu SG, Lin YX, Qi XP, Moore S, Xing FW, Wang FG, Hovenkamp PH, Gilbert MG, Nooteboom HP, Parris BS, Haufler C, Kato M, Smith AR (2013) Polypodiaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vols. 2-3. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis, pp 758–850
Zhao CF, Wei R, Zhang XC, Xiang QP (2019) Backbone phylogeny of Lepisorus (Polypodiaceae) and a novel infrageneric classification based on the total evidence from plastid and morphological data. Cladistics 36:235–258. https://doi.org/10.1111/cla.12403
Acknowledgement
The research was supported by the postdoctoral fellowships granted to TF and PKK by the Yunnan Provinces (Y7YN021B13) and (Y7YN021B14), respectively, and talent program to HS by Chinese government and Yunnan Province. Fieldwork was financially supported by funds to HM and HS from Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences (2017XTBG-T03, 2017XTBG-F05). We thank Ran Wei, Xianchun Zhang, and Xiaohua Jin, the curators for providing access to the herbarium collections especially the type species of Lepisorus cespitosus in PE and Zhenlong Liang for supporting the fieldwork and providing images. We thank Yuanbo Li and Ting Shen for field trip organization and Guihua Xu, Xiansheng He, and Liyan Wang for field guidance and support.
Funding
The research was supported by the postdoctoral fellowships granted to T.F. and P. K.K by the Yunnan Provinces (Y7YN021B13) and (Y7YN021B14), respectively, and talent program to H.S. by the Chinese government and Yunnan province. Fieldwork was financially supported by funds to H.M and H.S. from Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences (2017XTBG-T03, 2017XTBG-F05).
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TF, HL, and HS planned and designed research; TF, PKK, AZ, SZ, and DX collected specimens. TF conducted experiments and performed analyses. TF, HL, PKK, and HS prepared manuscript.
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Online Resource 1. Information about vouchers and GenBank accession numbers of all accessions used in this study.
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Fujiwara, T., Liu, H., Khine, P.K. et al. Rediscovery of Lepisorus cespitosus supported the floristic affinities between western Yunnan and southeast Tibet. Plant Syst Evol 306, 77 (2020). https://doi.org/10.1007/s00606-020-01701-8
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DOI: https://doi.org/10.1007/s00606-020-01701-8