Molecular phylogeography and paleodistribution modeling of the boreal tree species Ulmus lamellosa (T.Wang et S. L. Chang) (Ulmaceae) in China
- 251 Downloads
- 1 Citations
Abstract
The uplift of mountains and climatic oscillations are important for understanding of the demographic history and genetic structure of species. We investigated the biogeographic history of the boreal tree species Ulmus lamellosa (Ulmaceae) in China, by using a combined phylogeographic and paleodistribution modeling approach. In this study, 14 populations of endangered U. lamellosa were analyzed by using chloroplast DNA (cpDNA) sequences. A high level of genetic differentiation (Φ ST = 86.22%) among populations with a significant phylogeographic pattern (N ST > G ST, P < 0.05) was found in U. lamellosa. Ten haplotypes were detected by combining chloroplast DNA data, and haplotype 3 (H3) was found to be common and widespread. The intraspecific divergence of all U. lamellosa cpDNA haplotypes (9.27 Ma; 95% HPD 5.17–13.33 Ma) most probably began in the late Miocene. The pairwise difference among haplotypes and neutrality tests (Tajima’s D and Fu’s Fs statistic) indicated that populations of U. lamellosa, except group I, have not experienced recent sudden expansions. Multiple refuge areas were identified across the entire distribution ranges of U. lamellosa. The low level of gene flow (Nm = 0.14) among populations may have resulted from isolation resulting from distance and complex topography during climatic oscillations; this isolation was probably the major process that shaped the present distribution of haplotypes. These results support the hypothesis that U. lamellosa persisted in situ during glaciations and occupied multiple localized glacial refugia, contrary to the hypotheses of large-scale range contraction and long-distance southward migration.
Keywords
Ulmus lamellosa Phylogeography Climatic oscillation Paleodistribution modeling Chloroplast DNANotes
Acknowledgements
We are grateful to Feng Li (College of Life Sciences, Northwest University, Xi’an, China) for the insightful comments and assistance. This work was supported by the Natural Science Foundation of Shanxi Province, P.R. China (2015011069) and The University Innovation program of Science and Technology of Shanxi Province (20161109).
Data archiving statement
Sequence data obtained in this study has been submitted to GenBank (http://www.ncbi. nlm.nih.gov/genbank/). The accession numbers were KX671803–KX671806, KX671807–KX671813, KX671814–KX671818, and KX671819–KX671826 for matK, psbA-trnH, atpB-rbcL, and trnD-trnE, respectively.
Supplementary material
a–d Mismatch distribution for three groups and all populations of Ulmus lamellosa. The thin represents the expectation; The dotted line represents the observed value (GIF 50 kb)
References
- An ZS, Huang YS, Liu WG, Guo ZT, Steven C, Li L, Warren P, Ning YF, Cai YJ, Zhou WJ, Lin BH, Zhang QL, Cao YN, Qiang XK, Chang H, Wu ZK (2005) Multiple expansions of C-4 plant biomass in East Asia since 7 Ma coupled with strengthened monsoon circulation. Geology 33:705–708CrossRefGoogle Scholar
- 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 411:62–66CrossRefGoogle Scholar
- Anderson RP, Raza A (2010) The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela: effect of study region on models of distributions. J Biogeogr 37(7):1378–1393CrossRefGoogle Scholar
- Bai WN, Wang WT, Zhang DY (2016) Phylogeographic breaks within Asian butternuts indicate the existence of a phytogeographic divide in East Asia. New Phytol 209:1757–1772CrossRefPubMedGoogle Scholar
- Bartish IV, Kadereit JW, Comes HP (2006) Late Quaternary history of Hippophae rhamnoides L. (Elaeagnaceae) inferred from chalcone synthase intron (Chsi) sequences and chloroplast DNA variation. Mol Ecol 15:4065–4083CrossRefPubMedGoogle Scholar
- Bi RC, Yi WB, Li YN (2003) Study on niche of population of Ulmus lamellosa in the south area of Shanxi Province. Acta Bot Boreal –Occident Sin 23(7):1266–1271Google Scholar
- Bi RC, Zhang J, Su JX (2002) Ecological characters of rare-endangered plant Ulmus lamellosa in Shanxi Province. J Plant Res Environ 11:45–50Google Scholar
- Chen HR, Huang CJ (1998) Fagaceae, Ulmaceae and Rhoipteleaceae. Flora of China 22:334–350Google Scholar
- Chiang TY, Schaal BA (1999) Phylogeography of ten North American Hylocomium splendens based on nrDNA ITS sequences. Mol Ecol 8:1037–1042CrossRefGoogle Scholar
- Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, Chang P, Doney SC, Hack JJ, Henderson TB, Kiehl JT, Large WG, McKenna DS, Santer BD, Smith RD (2006) The community climate system model version 3 (CCSM3). J Clim 19(11):2122–2143CrossRefGoogle Scholar
- Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3(11):432–438CrossRefGoogle Scholar
- Comes HP, Tribsch A, Bittkau C (2008) Plant speciation in continental island floras as exemplified by Nigella in the Aegean Archipelago. Philos T R Soc B 363:3083–3096CrossRefGoogle Scholar
- Cruzan MB, Templeton AR (2000) Paleoecology and coalescence: phylogeographic analysis of hypotheses from the fossil record. Trends Ecol Evol 15:491–496CrossRefPubMedGoogle Scholar
- Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedPubMedCentralGoogle Scholar
- Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
- Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
- Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distance among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
- Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 47(2):915–925Google Scholar
- Fu ZZ, Li YH, Zhang KM, Li Y (2014) Molecular data and ecological niche modeling reveal population dynamics of widespread shrub Forsythia suspensa (Oleaceae) in China’s warm-temperate zone in response to climate change during the Pleistocene. BMC Evol Biol 14:114CrossRefPubMedPubMedCentralGoogle Scholar
- Gao LM, Moller M, Zhang XM, Hollingsworth ML, Liu J, Mill RR, Gibby M, Li DZ (2007) High variation and strong phylogeographic pattern among cpDNA haplotypes in Taxus wallichiana (Taxaceae) in China and North Vietnam. Mol Ecol 16(22):4684–4698CrossRefPubMedGoogle Scholar
- Gavin DG, Fitzpatrick MC, Gugger PF, Heath KD, Rodríguez-Sánchez F, Dobrowski SZ, Hampe A, Hu FS, Ashcroft MB, Bartlein PJ et al (2014) Climate refugia: joint inference from fossil records, species distribution models and phylogeography. New Phytol 204:37–54CrossRefPubMedGoogle Scholar
- Godbout J, Jaramillo-Correa JP, Beaulieu J, Bousquet J (2005) A mitochondrial DNA minisatellite reveals the postglacial history of jack pine (Pinus banksiana), a broad-range North American conifer. Mol Ecol 14:3497–3512CrossRefPubMedGoogle Scholar
- Gu S, Du G (1994) Relationships between geographica1 distribution of Ulmus lamellosa and climate in China. J Inner Mongolia For Coll 16(1):28–32Google Scholar
- Guo XD, Wang HF, Bao L, Wang TM, Bai WN, Ye JW, Ge JP (2014) Evolutionary history of a widespread tree species Acer mono in East Asia. Ecol Evol 4:4332–4345CrossRefPubMedPubMedCentralGoogle Scholar
- Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol Notes 8:513–525CrossRefGoogle Scholar
- Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Phil Trans Roy Soc Lond B Biol Sci 351:1291–1298CrossRefGoogle Scholar
- Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
- Harrison SP, Yu G, Takahara H, Prentice IC (2001) Palaeovegetation: diversity of temperate plants in East Asia. Nature 413(6852):129–130CrossRefPubMedGoogle Scholar
- Hewitt GM (1999) Post-glacial recolonisation of European biota. Biol J Linnean Soc 68:87–112CrossRefGoogle Scholar
- Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405(6789):907–913CrossRefPubMedGoogle Scholar
- Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH (2010) Phylogeography’s past, present, and future: 10 years after Avise, 2000. Mol Phylogenet Evol 54:291–301CrossRefPubMedGoogle Scholar
- Huang S, Chiang YC, Schaal BA, Chou CH, Chiang TY (2001) Organelle DNA phylogeography of Cycas taitungensis, a relict species in Taiwan. Mol Ecol 10:2669–2681CrossRefPubMedGoogle Scholar
- Jacques FMB, Go SX, Xing YW, Huang YJ, Liu YS, Ferguson DK, Zhou ZK (2011) Quantitative reconstruction of the Late Miocene monsoon climates of southwest China: a case study of the Lincang flora from Yunnan Province. Palaeogeography 304:318–327CrossRefGoogle Scholar
- Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13 Version 3.16, http://ibdws.sdsu.edu/
- Liu CP, Tsuda Y, Shen HL, Hu LJ, Saito Y, Ide Y (2014) Genetic structure and hierarchical population diversity history of Acer mono var. mono in south and northeast China. PLoS One 9(1):e87187CrossRefPubMedPubMedCentralGoogle Scholar
- 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(4):267–275CrossRefGoogle Scholar
- Liu L, Chen W, Zheng X, Li J, Yan DT, Liu L, Liu X, Wang YL (2016) Genetic diversity of Ulmus lamellosa by morphological traits and sequence-related amplified polymorphism (SRAP) markers. Biochem Syst Ecol 66:272–280CrossRefGoogle Scholar
- Li XH, Shao JW, Lu C, Zhang XP, Qiu YX (2012) Chloroplast phylogeography of a temperate tree Pteroceltis tatarinowii (Ulmaceae) in China. J Syst Evol 50(4):325–333CrossRefGoogle Scholar
- Mashayekhi S, Columbus JT (2015) Genetic diversity of Allium munzii (Amaryllidaceae), a rare southern California species and implication for its conservation. Biochem Syst Ecol 59:91–99CrossRefGoogle Scholar
- Ma SM, Zhang ML, Sanderson SC (2012) Phylogeography of the rare Gymnocarpos przewalskii (Caryophyllaceae): indications of multiple glacial refugia in north-western China. Aust J Bot 60(1):20–31CrossRefGoogle Scholar
- Mayol M, Riba M, Gonzalez-Martinez S, Bagnoli F, de Beaulieu JL, Berganzo E, Burgarella C, Dubreuil M, Krajmerova D, Paule L et al (2015) Adapting through glacial cycles: insights from a long-lived tree (Taxus baccata). New Phytol 208:973–986CrossRefPubMedGoogle Scholar
- 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 112:155–172CrossRefGoogle Scholar
- Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325CrossRefPubMedPubMedCentralGoogle Scholar
- Peterson AT, Soberón J, Sánchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285(5431):1265–1267CrossRefPubMedGoogle Scholar
- Petit RJ, Aguinagalde I, Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565CrossRefPubMedGoogle Scholar
- Petit RJ, Duminil J, Fineschi S, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14(3):689–701CrossRefPubMedGoogle Scholar
- Petit RJ, Hu FS, Dick CW (2008) Forests of the past: a window to future changes. Science 320(5882):1450–1452CrossRefPubMedGoogle Scholar
- Petit RJ, Vendramin GG (2007) Phylogeography of organelle DNA in plants: an introduction. In: Weiss S, Ferrand N (eds) Phylogeography of southern European refugia. Springer, New York , pp 23–972007CrossRefGoogle Scholar
- Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190(3–4):231–259CrossRefGoogle Scholar
- Polzin T, Daneshmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20CrossRefGoogle Scholar
- Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245PubMedPubMedCentralGoogle Scholar
- Printzen C, Ekman S, Tonsberg T (2003) Phylogeography of Cavernularia hultenii: evidence of slow genetic drift in a widely disjunct lichen. Mol Ecol 12(6):1473–1486CrossRefPubMedGoogle Scholar
- Qi XS, Chen C, Comes HP, Sakaguchi S, Liu YH, Tanaka N, Sakio H, Qiu YX (2012) Molecular data and ecological niche modelling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphyllum (Cercidiphyllaceae). New Phytol 196:617–630CrossRefPubMedGoogle Scholar
- Qiu YX, Fu CX, Comes HP (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Mol Phylogenet Evol 59(1):225–244CrossRefPubMedGoogle Scholar
- Rambaut A (2014) FigTree v1.4.2: tree figure drawing tool. [WWW document] URL http://tree.bio.ed.ac.uk/software/figtree
- Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. [WWW document] URL http://beast.bio.ed.ac.uk/Tracer
- Richardson JE, Pennington RT, Pennington TD, Hollingsworth PM (2001) Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293:2242–2245CrossRefPubMedGoogle Scholar
- Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615CrossRefGoogle Scholar
- Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
- Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
- Ru WM, Zhang GP, Bi RC, Zhang JT (2007) Population structure and pattern of endangered Ulmus lamellosa in Shanxi. Chin J Appl Environ Biol 13:14–17Google Scholar
- Sambrook J, Russell D (2001) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
- Sakaguchi S, Qiu YX, Liu YH, Qi XS, Kim SH, Han J, Takeuchi Y, Worth JR, Yamasaki M, Sakurai S, Isagi Y (2012) Climate oscillation during the Quaternary associated with landscape heterogeneity promoted allopatric lineage divergence of a temperate tree Kalopanax septemlobus (Araliaceae) in East Asia. Mol Ecol 21:3823–3838CrossRefPubMedGoogle Scholar
- Sakai A (1971) Freezing resistance of relicts from the Arcto-Tertiary flora. New Phytol 70:1199–1205CrossRefGoogle Scholar
- Mao K, Liu J (2012) Current ‘relicts’ more dynamic in history than previously thought. New Phytol 196:329–331CrossRefPubMedGoogle Scholar
- Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedPubMedCentralGoogle Scholar
- Shaw J, Small RL (2005) Chloroplast DNA phylogeny and phylogeography of the North American plums (prunus subgenus prunus section Prunocerasus, Rosaceae). Am J Bot 92:2011–2030CrossRefPubMedGoogle Scholar
- Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381CrossRefPubMedGoogle Scholar
- Soltis PS, Gitzendanner MA (1999) Molecular systematics and the conservation of rare species. Conserv Biol 13:471–483CrossRefGoogle Scholar
- Sun Y, Moore MJ, Yue L, Feng T, Chu H, Chen S, Ji Y, Wang H, Li J (2014) Chloroplast phylogeography of the East Asian Arcto-Tertiary relict Tetracentron sinense (Trochodendraceae). J Biogeogr 41:1721–1732CrossRefGoogle Scholar
- Taberlet P (1998) Biodiversity at the intraspecific level: the comparative phylogeographic approach. J Biotechnol 64:91–100CrossRefGoogle Scholar
- Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595PubMedPubMedCentralGoogle Scholar
- Tang ZH, Ding Z, White PD, Dong X, Ji J, Jiang H, Luo P, Wang X (2011) Late Cenozoic central Asian drying inferred from a palynological record from the northern Tian Shan. Earth Planet Sci Lett 302:439–447CrossRefGoogle Scholar
- Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploidy species. Syst Bot 28:723–737Google Scholar
- Teixeira H, Rodríguez-Echeverría S, Nabais C (2014) Genetic diversity and differentiation of Juniperus thurifera in Spain and Morocco as determined by SSR. PLoS One 9:e88996CrossRefPubMedPubMedCentralGoogle Scholar
- Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedPubMedCentralGoogle Scholar
- VanDerWal J, Shoo LP, Graham G, Williams SE (2009) Selecting pseudo-absence data for presence-only distribution modeling: how far should you stray from what you know? Ecol Model 220(4):589–594CrossRefGoogle Scholar
- Wan SM, Li AC, Clift PD, Stuut JBW (2007) Development of the East Asian monsoon: mineralogical and sedimentologic records in the northern South China Sea since 20 Ma. Palaeogeography 254:561–582CrossRefGoogle Scholar
- Wang HW, Ge S (2006) Phylogeography of the endangered Cathaya argyrophylla (Pinaceae) inferred from sequence variation of mitochondrial and nuclear DNA. Mol Ecol 15(13):4109–4122CrossRefPubMedGoogle Scholar
- Wang J, Gao P, Kang M, Lowe AJ, Huang H (2009) Refugia within refugia: the case study of a canopy tree Eurycorymbus cavalerieiin subtropical China. J Biogeogr 36(11):2156–2164CrossRefGoogle Scholar
- Wang Y, Yan G (2014) Molecular phylogeography and population genetic structure of O. longilobus and O. taihangensis (Opisthopappus) on the Taihang Mountains. PLoS One 9(8):e104773. doi: 10.1371/journal.pone.0104773 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 60:56–62CrossRefGoogle Scholar
- Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondria, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A 84:9054–9058CrossRefPubMedPubMedCentralGoogle Scholar
- Wu HZ, Xu SW, Cui SC (1999) The four new records of plant species in Shanxi Province. Shanxi For Sci Tech 2:20–21Google Scholar
- Yu G, Chen X, Ni J, Cheddadi R, Guiot J, Han H, Harrison SP, Huang C, Ke M, Kong Z, Li S, Li W, Liew P, Liu G, Liu J, Liu Q, Liu KB, Prentice IC, Qui W, Ren G, Song C, Sugita S, Sun X, Tang L, van Campo E, Xia Y, Xu Q, Yan S, Yang X, Zhao J et al (2000) Palaeovegetation of China: a pollen data based synthesis for the mid-Holocene and last glacial maximum. J Biogeogr 27(3):635–664CrossRefGoogle Scholar
- Zhao C, Wang CB, Ma XG, Liang QL, He XJ (2013) Phylogeographic analysis of a temperate-deciduous forest restricted plant (Bupleurum longiradiatum Turcz.) reveals two refuge areas in China with subsequent refugial isolation promoting speciation. Mol Phylogenet Evol 68:628–643CrossRefPubMedGoogle Scholar