Abstract
Past geological and climatic changes have promoted shifts in both intraspecific differentiation and distribution ranges for many desert plants, though little is known about the effects of these changes specifically on spring ephemerals in Northwest China. In the present study, we aimed to survey the population structure and phylogeographic history of an endemic spring ephemeral species, Ixiolirion songaricum P. Yan in Northwest China. We sequenced the nITS and two ptDNA fragments (psbB–psbH and ycf6–psbM) for 265 individuals from 15 populations across the entire range. Eight nITS ribotypes and eleven plastid chlorotypes were identified, with three of them dominant. A significant phylogeographic structure was detected for the species in which two larger, distinct phylogeographic lineages were identified. A high proportion of the total genetic variation existed between populations and between the two lineages. The species had undergone a sudden range expansion in the late Quaternary, which might have been driven by an interglacial warm, humid climate following the largest Pleistocene glaciation period in Northwest China. The ecological niche modeling suggested the species experienced continuous shrinkage of potential range since the last interglacial, which is distinct from other desert plants. Overall, our results indicated that climate change associated with the Quaternary greatly promoted differentiation of I. songaricum. The shift in population distribution was likely driven by increasing aridity in Xinjiang during the Quaternary.
Similar content being viewed by others
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
Austerlitz F, Jung-Muller B, Godelle B, Gouyon PH (1997) Evolution of coalescence times, genetic diversity and structure during colonization. Theor Popul Biol 51:148–164
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Avise JC (2012) Molecular markers, natural history and evolution. Sinauer Associates, Sunderland
Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molec Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Beatley JC (1974) Phenological events and their environmental triggers in Mojave Desert ecosystems. Ecology 55:856–863. https://doi.org/10.2307/1934421
Brown G (2003) Species richness, diversity and biomass production of desert annuals in an ungrazed Rhanterium epapposum community over three growth seasons in Kuwait. Pl Ecol 165:53–68. https://doi.org/10.1023/A:1021425308451
Carbone I, Kohn LM (2001) Multilocus nested haplotype networks extended with DNA fingerprints show common origin and fine-scale, ongoing genetic divergence in a wild microbial metapopulation. Molec Ecol 10:2409–2422. https://doi.org/10.1046/j.0962-1083.2001.01380.x
Castoe TA, Spencer CL, Parkinson CL (2007) Phylogeographic structure and historical demography of the western diamondback rattlesnake (Crotalus atrox): a perspective on North American desert biogeography. Molec Phylogen Evol 42:193–212. https://doi.org/10.1016/j.ympev.2006.07.002
Chen C (2013) Phylogeographical study of an intercontinental disjunct Smilax aspera: a basal taxon of Smilacaceae. Zhejiang University, Hangzhou (in Chinese)
Chen HZ, Jin J, Dong GR (2001) Holocene evolution processes of Gurbantunggut Desert and climatic changes. J Desert Res 21: 333–339 (in Chinese)
Clark MK, House MA, Royden LH, Whipple KX, Burchfiel BC, Zhang X, Tang W (2005) Late Cenozoic uplift of Southeastern Tibet. Geology 33:525–528. https://doi.org/10.1130/G21265.1
Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Pl Sci 3:432–438. https://doi.org/10.1098/rstb.2003.1435
Dong GR, Chen HZ, Wang GY, Li XZ, Shao YJ, Jin W (1995) Evolution of desert sands and climate change in Northern China since 150 ka. Chin Sci 25:1303–1312 (in Chinese)
Dong GR, Shang KZ, Wang SG, Yang DB (1997) Possible development trend of modern natural desertification process in northern China. Studies on the climate change and climate impact of China. Meteorological Press, Beijing (in Chinese)
Dong GR, Jin J, Shao YJ, Li S (2002) Climate change in the sandy area of China since the late Quaternary. In: Dong GR (ed) Desert formation and evolution, climate change and desertification research in China. Ocean Press, Beijing, pp 212–232 (in Chinese)
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molec Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molec Ecol 11:2571–2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x
Edmonds CA, Lillie AS, Cavalli-Sforza LL (2004) Mutations arising in the wave front of an expanding population. Proc Natl Acad Sci USA 101:975–979. https://doi.org/10.1073/pnas.0308064100
Excoffier L, Schneider S (1999) Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions. Proc Natl Acad Sci USA 96:10597–10602. https://doi.org/10.1073/pnas.96.19.10597
Fang XM, Yan MD, Van der Voo R, Rea DK, Song CH, Pares JM, Gao JP, Nie JS, Dai S (2005) Late Cenozoic deformation and uplift of the NE Tibetan plateau: evidence from high-resolution magneto stratigraphy of the Guide Basin, Qinghai Province, China. Geol Soc Am Bull 117:1208–1225. https://doi.org/10.1130/B25727.1
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gao XY, Meng HH, Zhang ML (2014) Diversification and vicariance of desert plants: evidence inferred from chloroplast DNA sequence variation of Lagochilus ilicifolius (Lamiaceae). Biochem Syst Ecol 55:93–100. https://doi.org/10.1016/j.bse.2014.03.002
Gao YD, Zhang Y, Gao XF, Zhu ZM (2015) Pleistocene glaciations, demographic expansion and subsequent isolation promoted morphological heterogeneity: a phylogeographic study of the alpine Rosa sericea complex (Rosaceae). Sci Rep 5:11698. https://doi.org/10.1038/srep11698
Graur D, Li WH (2000) Fundamentals of molecular evolution, 2nd edn. Sinauer Associates, Sunderland
Guo SX, Gu CG (1993) Fossil plants from calcareous Tufa and Palaeoenvironments in Ruoqiang, Xinjiang. Acta Palaeontol Sin 32:82–88 (in Chinese)
Guo ZT, Ruddiman WF, Hao QZ, Wu HB, Qiao YS, Zhu RX, Peng SZ, Wei JJ, Yuan BY, Liu TS (2002) Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature 416:159–163. https://doi.org/10.1038/416159a
Guu YP, Zhang R, Chen CY, Zhou DW, Liu JQ (2010) Allopatric divergence and regional range expansion of Juniperus sabina in China. J Syst Evol 48:153–160. https://doi.org/10.1111/j.1759-6831.2010.00073.x
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276. https://doi.org/10.1007/s10336-004-0024-y
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. https://doi.org/10.1038/35016000
Hewitt GM (2004) Genetic consequence of climatic oscillations in the quaternary. Philos Trans R Soc Lond B Biol Sci 359:183–195
Hijmans RJ, Cameron SE, Parra JL, Jones PG, 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
Huang PY (1991) Relations between living things and environment in desert of Dzungaria. Chin J Ecol 10:6–10 (in Chinese). https://doi.org/10.13292/j.1000-4890.1991.0072
Hudson RR (1990) Gene genealogies and the coalescent process. Oxford Surv Evol Biol 7:1–44
Jermakowicz E, Wroblewska A, Brzosko E, Mirski P, Hirse T (2015) Phylogeographical structure of the boreal-montane orchid Malaxis monophyllos as a result of multi-directional gene flow. Bot J Linn Soc 178:138–154. https://doi.org/10.1111/boj.12268
Jia J, Tan DY (2012) Variation in style length and anther-stigma distance in Ixiolirion songaricum (Amaryllidaceae). S African J Bot 81:19–24. https://doi.org/10.1016/j.sajb.2012.03.011
Jian HY, Tang KX, Sun H (2015) Phylogeography of Rosa soulieana (Rosaceae) in the Hengduan Mountains: refugia and ‘melting’ pots in the Quaternary climate oscillations. Pl Syst Evol 301:1819–1830. https://doi.org/10.1007/s00606-015-1195-0
Jiang RF, Song ZB, Qin M, Ye Z, Wang AM, Shi L (1992) The preliminary research on the characteristics of the biology and ecology of the early spring plants near to the Urumqi. J Pl Ecol 16:354–362 (in Chinese)
Jiang XL, An M, Zheng SS, Deng M, Su ZH (2018) Geographical isolation and environmental heterogeneity contribute to the spatial genetic patterns of Quercus kerrii (Fagaceae). Heredity 120:219–233. https://doi.org/10.1038/s41437-017-0012-7
Lan HY, Zhang FC (2008) Reviews on special mechanisms of adaptability of early-spring ephemeral plants to desert habitats in Xinjiang. Acta Bot Boreal-Occid Sin 28:1478–1485 (in Chinese)
Lee C, Wen J (2004) Phylogeny of Panax using chloroplast trnC-trnD intergenic region and the utility of trnC-trnD in interspecific studies of plants. Molec Phylogen Evol 31:894–903. https://doi.org/10.1016/j.ympev.2003.10.009
Li JJ (1999) Studies on the geomorphological evolution of the Qinghai-Xizang (Tibetan) Plateau and Asian monsoon. Mar Geol Quaternary Geol 19:1–11 (in Chinese). https://doi.org/10.16562/j.cnki.0256-1492.1999.01.002
Li JJ, Fang XM (1999) Uplift of the Tibetan Plateau and environmental changes. Chin Sci Bull 44:2117–2124. https://doi.org/10.1007/BF03182692
Li JJ, Wang XB (1994) Formation and evolution of arid areas in Northwest China and development of resources and environment. In: Li JJ (ed) Compile of resource and environment of Western China. Lanzhou University Press, Lanzhou (in Chinese)
Li JJ, Wen SX, Zhang QS, Wang FB, Zheng BX, Li BY (1979) A discussion on the period, amplitude and type of the uplift of the Qinghai-Xizang plateau. Sci Sin 22:1314–1328
Li J, Yimit A, Kerim A (2000) Ananatomical study on the vegetative organs of Senecio subdentatus Idb. ephemeral plant in Xinjiang. J Xinjiang Normal Univ (Nat Sci Edi) 19:51–55 (in Chinese)
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
Lu HY, Guo ZT (2014) Evolution of the monsoon and dry climate in East Asia during late Cenozoic: a review. Sci China Earth Sci 57:70–79. https://doi.org/10.1007/s11430-013-4790-3
Ma SM, Zhang ML (2012) Phylogeography and conservation genetics of the relic Gymnocarpos przewalskii (Caryophyllaceae) restricted to Northwestern China. Conservation Genet 13:1531–1541. https://doi.org/10.1007/s10592-012-0397-z
Mao ZM, Zhang DM (1994) The conspectus of ephemeral flora in Northern Xinjiang. Arid Zone Res 11:1–26 (in Chinese)
Meng HH, Zhang ML (2013) Diversification of plant species in arid Northwest China: species-level phylogeographical history of Lagochilus Bunge ex Bentham (Lamiaceae). Molec Phylogen Evol 68:398–409. https://doi.org/10.1016/j.ympev.2013.04.012
Meng HH, Gao XY, Huang JF, Zhang ML (2015) Plant phylogeography in arid Northwest China: retrospectives and perspectives. J Syst Evol 53:33–46. https://doi.org/10.1111/jse.12088
Miao YF, Herrmann M, Wu FL, Yan XL, Yang SL (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
Oberprieler C, Konowalik K, Fackelmann A, Vogt R (2018) Polyploid speciation across a suture zone: phylogeographyand species delimitation in S French Leucanthemum Mill.representatives (Compositae–Anthemideae). Pl Sys Evol 304:1141–1155. https://doi.org/10.1007/s00606-018-1537-9
Pan WB, Huang PY (1995) The ecology of four ephemeral plants. Acta Phytoecol Sin 19:85–91 (in Chinese)
Peterson AT (2006) Uses and requirements of ecological niche models and related distributional models. Biodivers Inform 3:59–72
Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck GM, Demesure-Musch B, Palme A, Martin JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565. https://doi.org/10.1126/science.1083264
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Rehfeld K, Munch T, Ho SL, Laepple T (2018) Global patterns of declining temperature variability from the Last Glacial Maximum to the Holocene. Nature 554:356. https://doi.org/10.1038/nature25454
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molec Biol Evol 9:552–569. https://doi.org/10.1093/oxfordjournals.molbev.a040727
Shaw J, Lickey EB, Beck JT, Farmer SB, Liu WS, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (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 YF, Cui ZJ, Su Z (2005) The Quaternary glaciations and environmental variations in China. Hebei Science and Technology Publishing House, Shijiazhuang, pp 99–100
Su ZH, Zhang ML (2016) Evolutionary history of a desert shrub Ephedra przewalskii (Ephedraceae): allopatric divergence and range shifts in Northwestern China. PLoS ONE 11:e0158284. https://doi.org/10.1371/journal.pone.0158284
Su ZH, Zhang ML, Sanderson SC (2011) Chloroplast phylogeography of Helianthemum songaricum (Cistaceae) from Northwestern China: implications for preservation of genetic diversity. Conservation Genet 12:1525–1537. https://doi.org/10.1007/s10592-011-0250-9
Su ZH, Zhang ML, Cohen JI (2012) Phylogeographic and demographic effects of Quaternary climate oscillations in Hexinia polydichotoma (Asteraceae) in Tarim Basin and adjacent areas. Pl Syst Evol 298:1767–1776. https://doi.org/10.1007/s00606-012-0677-6
Su ZH, Pan BR, Sanderson SC, Jiang XL, Zhang ML (2015) Conservation genetics and geographic patterns of genetic variation of the endangered officinal herb Fritillaria pallidiflora. Nordic J Bot 33:506–512. https://doi.org/10.1111/njb.00677
Su ZH, Richardson BA, Zhuo L, Jiang XL (2017) Divergent population genetic structure of the endangered Helianthemum (Cistaceae) and its implication to conservation in Northwestern China. Frontiers Pl Sci 7:2010. https://doi.org/10.3389/fpls.2016.02010
Sun XJ, Wang PX (2005) How old is the Asian monsoon system? Palaeobotanical records from China. Palaeogeogr Paleoclimatol Palaeoecol 222:181–222. https://doi.org/10.1016/j.palaeo.2005.03.005
Sun JM, Zhu RX, Bowler J (2004) Timing of the Tianshan Mountains uplift constrained by magnetostratigraphic analysis of molasse deposits. Earth Planet Sci Lett 219:239–253. https://doi.org/10.1016/S0012-821x(04)00008-1
Sun JM, Zhang LY, Deng CL, Zhu RX (2008) Evidence for enhanced aridity in the Tarim Basin of China since 5.3 Ma. Quaternary Sci Rev 27:1012–1023. https://doi.org/10.1016/j.quascirev.2008.01.011
Sunmonu N, Kudo G (2015) Warm temperature conditions restrict the sexual reproduction and vegetative growth of the spring ephemeral Gagea lutea (Liliaceae). Pl Ecol 216:1419–1431. https://doi.org/10.1007/s11258-015-0520-6
Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601
Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669
Templeton AR, Boerwinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343–351
Tian S, Lopez-Pujol J, Wang HW, Ge S, Zhang ZY (2010) Molecular evidence for glacial expansion and interglacial retreat during Quaternary climatic changes in a montane temperate pine (Pinus kwangtungensis Chun ex Tsiang) in Southern China. Pl Syst Evol 284:219–229. https://doi.org/10.1007/s00606-009-0246-9
Tian L, Tian LN, Xie SQ, Yan P (2012) Study on the seed germination characteristics of Ixiolirion songaricum. Jiangsu Agr Sci 40:364–366 (in Chinese). https://doi.org/10.15889/j.issn.1002-1302.2012.05.115
Wang XQ, Jiang J, Wang YC, Luo WL, Song CW, Chen JJ (2006) Responses of ephemeral plant germination and growth to water and heat conditions in the southern part of Gurbantunggut Desert. Chin Sci Bull 51:110–116
Wang LY, Abbott RJ, Zheng W, Chen P, Wang YJ, Liu JQ (2009) History and evolution of alpine plants endemic to the Qinghai-Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae). Molec Ecol 18:709–721. https://doi.org/10.1111/j.1365-294X.2008.04055.x
Wang XY, Li YS, Liang QL, Zhang L, Wang Q, Hu H, Sun YS (2015) Contrasting responses to Pleistocene climate changes: a case study of two sister species Allium cyathophorum and A. spicata (Amaryllidaceae) distributed in the eastern and western Qinghai-Tibet Plateau. Ecol Evol 5:1513–1524. https://doi.org/10.1002/ece3.1449
Wang P, Zhang XZ, Tang N, Liu JJ, Xu LR, Wang K (2016) Phylogeography of Libanotis buchtormensis (Umbelliferae) in disjunct populations along the deserts in Northwest China. PLoS ONE 11:e0159790. https://doi.org/10.1371/journal.pone.0159790
Wen ZB, Xu Z, Zhang HX, Feng Y (2015) Chloroplast phylogeography of a desert shrub, Calligonum calliphysa (Calligonum, Polygonaceae), in arid Northwest China. Biochem Syst Ecol 60:56–62. https://doi.org/10.1016/j.bse.2015.03.001
Wen ZB, Xu Z, Shi XJ, Zhang J, Zhang ML (2016a) Genetic structure of Salsola junatovii (Chenopodiaceae) in the northern edge of the Taklimakan desert and conservational implications. Biochem Syst Ecol 67:86–94. https://doi.org/10.1016/j.bse.2016.05.024
Wen ZB, Xu Z, Zhang HX, Feng Y (2016b) Chloroplast phylogeographic patterns of Calligonum sect. Pterococcus (Polygonaceae) in arid Northwest China. Nordic J Bot 34:335–342. https://doi.org/10.1111/njb.00820
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic Press, New York, pp 315–322
Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc Roy Soc London, Ser B, Biol Sci 268:1–10
Williams MAJ, Dunkerley DL, De Dekker P, Kershaw AP, Stokes T (1993) Quaternary environments. Edward Arnold, London
Xu XK, Kleidon A, Miller L, Wang SQ, Wang LQ, Dong GC (2010) Late Quaternary glaciation in the Tianshan and implications for palaeoclimatic change: a review. Boreas 39:215–232. https://doi.org/10.1111/j.1502-3885.2009.00118.x
Xu Z, Zhang ML, Cohen JI (2016) Phylogeographic history of Atraphaxis Plants in arid Northern China and the origin of A. bracteata in the Loess Plateau. PLoS ONE 11:243. https://doi.org/10.1371/journal.pone.0163243
Yang XP (2006) Desert research in Northwestern China-a brief review. Geomorphologie 4:275–283 (in Chinese)
Yao H, Tan DY (2005) Size-dependent reproductive output and life-history strategies in four ephemeral species of Trigonella. Acta Phytoecol Sin 29:954–960 (in Chinese)
Yoder JB, Stanton-Geddes J, Zhou P, Briskine R, Young ND, Tiffin P (2014) Genomic signature of adaptation to climate in Medicago truncatula. Genetics 196:1263–1275. https://doi.org/10.1534/genetics.113.159319
Yu XF, Li J (1997) A study of the biological characteristics and the anatomical vegetative organs of the ephemeral plant in Cancrinia discoidea (Idb.) Pok. Acta Bot Boreal-Occid Sin 17:123–126 (in Chinese)
Yu HB, Zhang YL, Liu LS, Qi W, Li SC, Hu ZJ (2015) Combining the least cost path method with population genetic data and species distribution models to identify landscape connectivity during the late Quaternary in Himalayan hemlock. Ecol Evol 5:S781–S791. https://doi.org/10.1002/ece3.1840
Zeng YF, Zhang JG, Abuduhamiti B, Wang WT, Jia ZQ (2018) Phylogeographic patterns of the desert poplar in Northwest China shaped by both geology and climatic oscillations. BMC Evol Biol 18:75. https://doi.org/10.1186/s12862-018-1194-1
Zhang HX, Zhang ML (2012) Genetic structure of the Delphinium naviculare species group tracks Pleistocene climatic oscillations in the Tianshan Mountains, arid Central Asia. Palaeogeogr Paleoclimatol Palaeoecol 353:93–103. https://doi.org/10.1016/j.palaeo.2012.07.013
Zhang HX, Zhang ML (2014) Insight into distribution patterns and conservation planning in relation to woody species diversity in Xinjiang, arid Northwestern China. Biol Conservation 177:165–173. https://doi.org/10.1016/j.biocon.2014.07.005
Zhang HX, Zhang ML, Williams DM (2014) Genetic evidence and species distribution modelling reveal the response of Larix sibirica and its related species to Quaternary climatic and ancient historical events. Biochem Syst Ecol 54:316–325. https://doi.org/10.1016/j.bse.2014.02.017
Zhang HX, Zhang ML, Wang LN (2015) Genetic structure and historical demography of Malus sieversii in the Yili Valley and the western mountains of the Junggar Basin, Xinjiang, China. J Arid Land 7:264–271. https://doi.org/10.1007/s40333-014-0044-2
Zhang YH, Wang IJ, Comes HP, Peng H, Qiu YX (2016) Contributions of historical and contemporary geographic and environmental factors to phylogeographic structure in a Tertiary relict species, Emmenopterys henryi (Rubiaceae). Sci Rep 6:24041. https://doi.org/10.1038/srep24041
Zhang YH, Yu QS, Zhang Q, Hu XK, Hu J, Fan BL (2017) Regional-scale differentiation and phylogeography of a desert plant Allium mongolicum (Liliaceae) inferred from chloroplast DNA sequence variation. Pl Syst Evol 303:451–466. https://doi.org/10.1007/s00606-016-1383-6
Acknowledgements
We thank Dr. Hongxiang Zhang and Zhibin Wen at Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences for their review and comments on the manuscript. We would also like to thank Elizabeth Tokarz at the Yale University for her assistance with English language and grammatical editing of the manuscript. This work was financially supported by the National Natural Science Foundation of China (Nos. 31500309, 31560131) and the Scientific Research Fund for Doctors of Xinjiang University (BS150259).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict interest.
Ethical approval
We are clear about the rules of COPE and comply with all the guidelines. This research does not involve any human participants or animals. All authors consent the submission of this manuscript to PSE.
Additional information
Handling Editor: Pablo Vargas.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Information on electronic supplementary material
Information on electronic supplementary material
Online resource 1. Detailed sample locations of 15 Ixiolirion songaricum populations.
Online resource 2. Sequence polymorphisms detected in nITS regions identifying 8 ribotypes.
Online resource 3. Sequence polymorphisms detected in ptDNA regions identifying 11 chlorotypes.
Online resource 4. Bayesian phylogenetic relationship and age estimation of ribotypes of Ixiolirion songaricum using nITS sequences. Nodes indicate mean age estimates and 95% confidence intervals (light blue bars). The posterior probabilities were indicated below branches. Node a was used as calibration point for the estimates of divergence analysis. The scale bar represents million years ago (Mya).
Online resource 5. Bayesian phylogenetic tree constructed by ptDNA matK sequences showing the sister relationship of Ixiolirion songaricum and Ixiolirion tataricum. The posterior probabilities were indicated below branches. Nodes indicate mean age estimates and 95% confidence intervals (light blue bars). Node a was used as calibration point for the estimates of divergence time of I. songaricum and I. tataricum. The scale bar represents million years ago (Mya).
Rights and permissions
About this article
Cite this article
Li, Y., Zhang, XN. & Lv, GH. Phylogeography of Ixiolirion songaricum, a spring ephemeral species endemic to Northwest China. Plant Syst Evol 305, 205–221 (2019). https://doi.org/10.1007/s00606-018-1563-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-018-1563-7