Abstract
Zygophyllum xanthoxylon, a desert species, displaying a broad east–west continuous distribution pattern in arid Northwestern China, can be considered as a model species to investigate the biogeographical history of this region. We sequenced two chloroplast DNA spacers (psbK-psbI and rpl32-trnL) in 226 individuals from 31 populations to explore the phylogeographical structure. Median-joining network was constructed and analysis of AMOVA, SMOVA, neutrality tests and distribution analysis were used to examine genetic structure and potential range expansion. Using species distribution modeling, the geographical distribution of Z. xanthoxylon was modeled during the present and at the Last Glacial Maximum (LGM). Among 26 haplotypes, one was widely distributed, but most was restricted to either the eastern or western region. The populations with the highest levels of haplotype diversity were found in the Tianshan Mountains and its surroundings in the west, and the Helan Mountains and Alxa Plateau in the east. AMOVA and SAMOVA showed that over all populations, the species lacks phylogeographical structure, which is speculated to be the result of its specific biology. Neutrality tests and mismatch distribution analysis support past range expansions of the species. Comparing the current distribution to those cold and dry conditions in LGM, Z. xanthoxylon had a shrunken and more fragmented range during LGM. Based on the evidences from phylogeographical patterns, distribution of genetic variability, and paleodistribution modeling, Z. xanthoxylon is speculated most likely to have originated from the east and migrated westward via the Hexi Corridor.
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Abbott RJ, Smith LC, Milne RI, Crawford RM, Wolff K, Balfour J (2000) Molecular analysis of plant migration and refugia in the Arctic. Science 289:1343–1346
Alsos IG, Alm T, Normand S, Brochmann C (2009) Past and future range shifts and loss of diversity in dwarf willow (Salix herbacea L.) inferred from genetics, fossils and modelling. Glob Ecol Biogeogr 18:223–239
An JX, Wang Q, Yang J, Liu JQ (2012) Phylogeographic analyses of Phragmites australisin China: native distribution and habitat preference of the haplotype that invaded North America. J Syst Evol 10:1–7
Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol 13:494–504
Avise JC (1987) Identification and interpretation of mitochondrial DNA stocks in marine species. In: Kumpf H, Nakamura EL (eds) Proceedings of the stock identification workshop. National Oceanographic and Atmospheric Administration, Panama City, pp 105–136
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bellstedt DU, Van Zyl L, Marais EM, Bytebier B, De Villiers CA, Makwarela AM, Dreyer LL (2008) Phylogenetic relationships, character evolution and biogeography of southern African members of Zygophyllum (Zygophyllaceae) based on three plastid regions. Mol Phylogenet Evol 47:932–949
Burban C, Petit R, Carcreff E, Jactel H (1999) Rangewide variation of the maritime pine bast scale Matsucoccus feytaudi Duc. (Homoptera: Matsucoccidae) in relation to the genetic structure of its host. Mol Ecol 8:1593–1602
Bush ABG, Little EC, Rokosh D, White D, Rutter NW (2004) Investigation of the spatio-temporal variability in Eurasian Late Quaternary loess-paleosol sequences using a coupled atmosphere-ocean general circulation model. Quat Sci Rev 23:481–498
Carstens BC, Richards CL (2007) Integrating coalescent and ecological niche modeling in comparative phylogeography. Evolution 61:1439–1454
Chen JM, Du ZY, Sun SS, Robert WG, Wang QF (2013) Chloroplast DNA phylogeography reveals repeated range expansion in a widespread aquatic herb Hippuris vulgaris in the Qinghai–Tibetan Plateau and adjacent areas. PLoS One 8:e60948. doi:10.1371/journal.pone.0060948
Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, Chang P, Doney SC, Hack JJ, Henderson TB (2006) The community climate system model version 3 (CCSM3). J Clim 19:2122–2143
Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438
Cordellier M, Pfenninger M (2009) Inferring the past to predict the future: climate modelling predictions and phylogeography for the freshwater gastropod Radix balthica (Pulmonata, Basommatophora). Mol Ecol 18:534–544
Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969
Cruzan MB, Templeton AR (2000) Paleoecology and coalescence: phylogeographic analysis of hypotheses from the fossil record. Trends Ecol Evol 15:491–496
Cullings K (1992) Design and testing of a plant-specific PCR primer for ecological and evolutionary studies. Mol Ecol 1:233–240
Donnelly P, Tavaré S (1986) The ages of alleles and a coalescent. Adv Appl Probab:1–19
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47
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
Ge XJ, Chiang YC, Chou CH, Chiang TY (2002) Nested clade analysis of Dunnia sinensis (Rubiaceae), a monotypic genus from China based on organelle DNA sequences. Conserv Genet 3:351–362
Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792
Guan QY, Pan BT, Li N, Zhang JD, Xue LJ (2011) Timing and significance of the initiation of present day deserts in the northeastern Hexi Corridor, China. Palaeogeogr Palaeoclim Palaeoecol 306:70–74
Guo 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
Hamrick J, Godt M (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B Biol Sci 351:1291–1298
Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Harrison S, Yu G, Takahara H, Prentice I (2001) Palaeovegetation (communications arising): diversity of temperate plants in East Asia. Nature 413:129–130
Hasumi H, Emori S (2004) K-1 coupled GCM (MIROC) description. Center for climate system research. University of Tokyo, Tokyo
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
Hodgins KA, Barrett SCH (2007) Population structure and genetic diversity in tristylous Narcissus triandrus: insights from microsatellite and chloroplast DNA variation. Mol Ecol 16:2317–2332
Hu J, Xie JR, Wang SM (2012) Cloning and sequence analysis of 18S rRNA gene fragment from succulent xerophyte Zygophyllum xanthoxylum. Pratac Sci 29:1369–1373 (in Chinese with English abstract)
Lahaye R, Savolainen V, Duthoit S, Maurin O, Van der Bank M (2008) A test of psbK-psbI and atpF-atpH as potential plant DNA barcodes using the flora of the Kruger National Park as a model system (South Africa). Nat Proc:hdl:10101
Li Y, Qu JJ, Dong ZB, Wang T, An LZ (2008a) Storage behavior of Zygophyllum xanthoxylon (Bge.) Maxim seeds at low moisture contents. Acta Physiol Plant 30:651–656
Li Y, Qu JJ, Yang XM, An LZ (2008b) A report on ultra-dry storage experiment of Zygophyllum xanthoxylon seeds. Bot Stud 49:243–251
Li ZH, Chen J, Zhao GF, Guo YP, Kou YX, Ma YZ, Wang G, Ma XF (2012) Response of a desert shrub to past geological and climatic change: a phylogeographic study of Reaumuria soongarica (Tamaricaceae) in western China. J Syst Evol 50:351–361
Liu YX (1995) A study on origin and formation of the Chines desert floras. Acta Phytotaxon Sin 33:131–143
Liu YF, Wang Y, Huang HW (2009) Species-level phylogeographical history of Myricaria plants in the mountain ranges of western China and the origin of M. laxiflora in the Three Gorges mountain region. Mol Ecol 18:2700–2712
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
Lorenz-Lemke AP, Togni PD, Maeder G, Kriedt RA, Stehmann JR, Salzano FM, Bonatto SL, Freitas LB (2010) Diversification of plant species in a subtropical region of eastern South American highlands: a phylogeographic perspective on native Petunia (Solanaceae). Mol Ecol 19:5240–5251
Ma Q, Wang SM (2012) Construction of RNAi expression vector of the plasma membrane Na+/H+ antiporter gene in succulent xerophyte Zygophyllum xanthoxylum. Pratacultural Science 29:549–553 (in Chinese with English abstract)
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 60:20
Marske KA, Leschen RA, Buckley TR (2011) Reconciling phylogeography and ecological niche models for New Zealand beetles: looking beyond glacial refugia. Mol Phylogenet Evol 59:89–102
Meng HH, Zhang ML (2011) Phylogeography of Lagochilus ilicifolius (Lamiaceae) in relation to Quaternary climatic oscillation and aridification in northern China. Biochem Syst Ecol 39:787–796
Meng HH, Zhang ML (2013) Diversification of plant species in arid Northwest China: species-level phylogeographical history of Lagochilus Bunge ex Bentham (Lamiaceae). Mol Phylogenet Evol 68:398–409
Meng LH, Yang R, Abbott RJ, Miehe G, Hu TH, Liu JQ (2007) Mitochondrial and chloroplast phylogeography of Picea crassifolia Kom. (Pinaceae) in the Qinghai–Tibetan Plateau and adjacent highlands. Mol Ecol 16:4128–4137
Meng HH, Gao XY, Huang JF, Zhang ML (2014) Plant phylogeography in arid Northwest China: retrospectives and perspectives. J Syst Evol. doi:10.1111/jse.12088
Ni J, Harrison SP, Colin Prentice I, Kutzbach JE, Sitch S (2006) Impact of climate variability on present and Holocene vegetation: a model-based study. Ecol Model 191:469–486
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Nybom H, Bartish IV (2000) Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect Plant Ecol 3:93–114
Orive ME, Asmussen MA (2000) The effects of pollen and seed migration on nuclear-dicytoplasmic systems. II. A new method for estimating plant gene flow from joint nuclear-cytoplasmic data. Genetics 155:833–854
Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A (1997) Chloroplast DNA footprints of postglacial recolonization by oaks. P Natl Acad Sci USA 94:9996–10001
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
Pons O, Petit R (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245
Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45
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 59:225–244
Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Song BH, Wang XQ, Wang XR, Sun LJ, Hong DY, Peng PH (2002) Maternal lineages of Pinus densata, a diploid hybrid. Mol Ecol 11:1057–1063
Su ZH, Zhang ML (2013) Evolutionary response to Quaternary climate aridification and oscillations in north-western China revealed by chloroplast phylogeography of the desert shrub Nitraria sphaerocarpa (Nitrariaceae). Biol J Linn Soc 109:757–770
Sun JM, Liu TS (2006) The age of the Taklimakan Desert. Science 312:1621
Sun JM, Ding ZL, Liu TS (1998) Desert distributions during the glacial maximum and climatic optimum: example of China. Epis Newsmag Int Union Geol Sci 21:28–31 (in Chinese with English abstract)
Sun JM, Zhang ZQ, Zhang LY (2009a) New evidence on the age of the Taklimakan Desert. Geology 37:159–162
Sun LD, Guan LP, Zhang YC, Wu DL, Zhang YP, Hou SW (2009b) High-efficiency plant regeneration of Zygophyllum xanthoxylon (Bunge) Maxim, an endangering desert plant. J Desert Res 29:312–315 (in Chinese with English abstract)
Taberlet P, Fumagalli L, Wust-saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tang YC (2000) On the affinities and the role of the Chinese Flora. Acta Botanica Yunnanica 22:2–26 (in Chinese with English abstract)
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Timme RE, Kuehl JV, Boore JL, Jansen RK (2007) A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats. Am J Bot 94:302–312
Waltari E, Hijmans RJ, Peterson AT, Nyári ÁS, Perkins SL, Guralnick RP (2007) Locating Pleistocene refugia: comparing phylogeographic and ecological niche model predictions. PLoS One 2:e563
Wan T, Yan L, Shi XS, Yi WD, Zhang XM (2006) Comparative analysis of genetic diversity of Zygophyllum L. and its related Congener Sarcozygium xanthoxylon Bunge in Inner Mongolia. J Arid Land Resour Environ 20:199–203 (in Chinese with English abstract)
Wang LY, Abbott RJ, Zhang W, Chen P, Wang YJ, Liu JQ (2009a) History and evolution of alpine plants endemic to the Qinghai–Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae). Mol Ecol 18:709–721
Wang LY, Hiroshi I, Liu TL, Wang YJ, Liu JQ (2009b) Repeated range expansion and glacial endurance of Potentilla glabra (Rosaceae) in the Qinghai–Tibetan Plateau. J Integr Plant Biol 51(7):698–706
Wu JF, Guo F (2012) Geomorphological patterns in a linear dune field and ages of the linear dunes in the northern Kumtagh Desert, northwest China. Environ Earth Sci 66:2449–2457
Wu ZY, Wang HS (1983) Chinese physical geography. Phytogeography (I). Science Press, Beijing
Wu LL, Cui XK, Milne RJ, Sun YS, Liu JQ (2010) Multiple autopolyploidizations and range expansion of Allium przewalskianum Regel. (Alliaceae) in the Qinghai–Tibetan Plateau. Mol Ecol 19:1691–1704
Xi JJ, Wu GQ, Bao AK, Wang SM (2011) Cloning and sequence analysis of a vacuolar H+-PPase gene fragment from Zygophyllum xanthoxylum. Pratacult Sci 20:119–124 (in Chinese with English abstract)
Yang D, Fang XM, Dong GR, Peng ZC, Li JJ (2006) Aeolian deposit evidence for formation and evolution of the Tengger desert in the north of China since early Pleistocene. Mar Geol Quat Geol 26:93–100 (in Chinese with English abstract)
Yu G, Chen XD, Ni J, Cheddadi R, Guiot J, Han H, Harrison SP, Huang C, Ke M, Kong Z (2000) Palaeovegetation of China: a pollen data-based synthesis for the mid-Holocene and last glacial maximum. J Biogeogr 27:635–664
Zeng YJ, Wang YR, Zhuang GH, Yang ZS (2004) Seed germination responses of Reaumuria soongorica and Zygophyllum xanthoxylum to drought stress and sowing depth. Acta Ecol Sinica 24:1629–1634 (in Chinese with English abstract)
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 Palaeoclim Palaeoecol 353:93–103
Zhang CB, Shi XS, W T, C YW, Z XM (2006) Studies on the genetic relationships of 7 species of Zygophyllum in Inner Mongolia based on random amplified polymorphic DNA (RAPD). Chin J Grass land 28:86–90
Zhao YZ, Zhu ZY (2003) The endemic genera of desert region in the centre of Asia. Acta Botanica Yunnanica 25:113 (in Chinese with English abstract)
Zhou XR, Zhou ZY, Wu CX (2006) The research of the breeding characters of Zygophyllum xanthoxylum. Pratacult Sci 23:38–41 (in Chinese with English abstract)
Zurawski G, Clegg MT, Brown AH (1984) The nature of nucleotide sequence divergence between barley and maize chloroplast DNA. Genetics 106:735–749
Acknowledgments
We thank Jian Zhang and Hong-Hu Meng for help of the field collection, to Zhi-Hao Su and Hong-Xiang Zhang (Xinjiang Institute of Ecology and Geography, CAS) for their kindly help about molecular data analyses. We also thank Stewart C. Sanderson (Shrub Sciences Laboratory, Intermountain Research Station, Forest Service, US Department of Agriculture, Utah) for his useful suggestion and English correction to the manuscript. This study is financially supported by Innovation Research Group Program of Chinese Academy of Sciences and State Administration of Foreign Experts Affairs of China (KZCX2-YW-T09), National Basic Research Special Program of China (2012FY111500), State International Science and Technology Cooperation Program of China (2010DFA92720), and Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences.
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Shi, XJ., Zhang, ML. Phylogeographical structure inferred from cpDNA sequence variation of Zygophyllum xanthoxylon across north-west China. J Plant Res 128, 269–282 (2015). https://doi.org/10.1007/s10265-014-0699-y
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DOI: https://doi.org/10.1007/s10265-014-0699-y