Genetic diversity patterns in an endangered desert shrub from north-western China: implications for conservation
Zhihao Su A B F , Liuqiang Wang C F , Li Zhuo D , Xiaolong Jiang E and Wenjun Li A
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China.
B University Chinese Academy of Sciences, Beijing, 100049, China.
C State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China.
D Library, Xinjiang Normal University, Urumqi 830054, China.
E Shanghai Chenshan Plant Science Research Centre, Shanghai Chenshan Botanical Garden, Chinese Academy of Sciences, Shanghai 201602, China.
F Corresponding authors. Email: suzh@ms.xjb.ac.cn; wanglq@caf.ca.cn
Australian Journal of Botany 67(7) 571-584 https://doi.org/10.1071/BT18192
Submitted: 18 October 2018 Accepted: 23 October 2019 Published: 20 December 2019
Abstract
Tamarix taklamakanensis is an endangered shrub endemic to the Tarim Basin and adjacent Kumtag Desert in north-western China. Here, we used two chloroplast DNA sequences, namely, psbA-trnH and trnS-trnG, to examine the genetic diversity patterns of this species across its entire covered range. A total of nineteen haplotypes were detected. The total gene diversity within the species is high. Genetic variation mainly occurred among populations, SAMOVA groups, and geographic regions. The test for isolation-by-distance showed a significant correlation between genetic and geographical distances, and the genetic landscape shape analysis showed a significant genetic divergence between the Tarim Basin and Kumtag Desert. T. taklamakanensis likely had a potential geographic range during the Last Glacial Maximum period that was much smaller than the present range predicted by ecological niche modelling. The cold and dry climate during the glacial periods of the Quaternary might be a driver of the genetic isolation and divergence detected within T. taklamakanensis, and climatic oscillations might account for the habitat fragmentation of the species. Within the inner of the basin, populations have a higher level of genetic diversity and harbor most of this genetic diversity, thus a nature reserves should be set up in this area for the in situ conservation. In addition, five genetically distinct groups within T. taklamakanensis should be treated as different management units (MUs) when implementing conservation activities.
Additional keywords: aridification, genetic differentiation, hydrochory, Tamarix taklamakanensis, Tarim Basin.
References
Alvarez NC, Thiel-Egenter A, Tribsch R, Holderegger S, Manel P, Schönswetter P, Taberlet P, Brodbeck S, Gaudeul M, Gielly L, Kupfer P, Mansion G, Negrini R, Paun O, Pellecchia M, Rioux D, Schupfer F, Van Loo M, Winkler M, Gugerli F, IntraBioDiv Consortium (2009) History or ecology? Substrate type as a major driver of spatial genetic structure in alpine plants. Ecology Letters 12, 632–640.| History or ecology? Substrate type as a major driver of spatial genetic structure in alpine plants.Crossref | GoogleScholarGoogle Scholar |
Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Molecular Biology and Evolution 13, 494–504.
| The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism.Crossref | GoogleScholarGoogle Scholar | 8742638PubMed |
Avise JC (2000) ‘Phylogeography: the history and formation of species.’ (Harvard University Press: Cambridge, MA, USA)
Brouns G, De Wulf A, Constales D (2003) Delaunay triangulation algorithms useful for multibeam echosounding. Journal of Surveying Engineering 129, 79–84.
| Delaunay triangulation algorithms useful for multibeam echosounding.Crossref | GoogleScholarGoogle Scholar |
Byrne M (2008) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Science Reviews 27, 2576–2585.
| Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography.Crossref | GoogleScholarGoogle Scholar |
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 11050560PubMed |
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). Journal of Climate 19, 2122–2143.
| The Community Climate System Model version 3 (CCSM3).Crossref | GoogleScholarGoogle Scholar |
Dang RL, Pan XL, Gu XF (2002) Floristic analysis of spermatophyte genera in the arid deserts area in north-west China. Guihaia 22, 121–128.
Dong GR, Chen HZ, Wang GY, Li XZ, Shao YJ, Jin J (1997) The evolution of deserts with climatic changes in China since 150 ka BP. Science in China. Series D, Earth Sciences 40, 370–382.
| The evolution of deserts with climatic changes in China since 150 ka BP.Crossref | GoogleScholarGoogle Scholar |
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochemical Bulletin 19, 11–15.
Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161, 1307–1320.
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |
Dubreuil M, Riba M, Gonzalez-Martinez SC, Vendramin GG, Sebastiani F, Mayol M (2010) Genetic effects of chronic habitat fragmentation revisited: strong genetic structure in a temperate tree, Taxus baccata (Taxaceae), with great dispersal capability. American Journal of Botany 97, 303–310.
| Genetic effects of chronic habitat fragmentation revisited: strong genetic structure in a temperate tree, Taxus baccata (Taxaceae), with great dispersal capability.Crossref | GoogleScholarGoogle Scholar | 21622391PubMed |
Dupanloup I, Schneider S, Excoffier L (2002) Assimilated annealing approach to define the genetic structure of populations. Molecular Ecology 11, 2571–2581.
| Assimilated annealing approach to define the genetic structure of populations.Crossref | GoogleScholarGoogle Scholar | 12453240PubMed |
Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 131, 479–491.
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
| Arlequin (version 3.0): an integrated software package for population genetics data analysis.Crossref | GoogleScholarGoogle Scholar |
Fischer M, Matthies D (1997) Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae). American Journal of Botany 84, 1685–1692.
| Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae).Crossref | GoogleScholarGoogle Scholar | 21708572PubMed |
Frankel OH (1983) The place of management in conservation. In ‘Genetics and conservation’. (Eds CM Schonewald-Cox, SM Chambers, B MacBryde, L Thomas) pp. 1–14. (Benjamin-Cummings: Menlo Park, CA, USA)
Frankham R (2005) Genetics and extinction. Biological Conservation 126, 131–140.
| Genetics and extinction.Crossref | GoogleScholarGoogle Scholar |
Frankham R, Kingsolver JG (2004) Response to environmental change: adaptation or extinction. In ‘Evolutionary conservation biology’. (Eds R Ferrier, U Dieckman, D Couvet) pp. 85–100. (Cambridge University Press: Cambridge, UK)
Frankham R, Ballou JD, Briscoe DA (2002) ‘Introduction to conservation genetics.’ (Cambridge University Press: Cambridge, UK)
Fu LG (1992) ‘Rare and endangered plants in China.’ pp. 368–370. (Science Press: Beijing)
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147, 915–925.
Guo ZT, Peng SZ, Hao QZ, Chen XH, Liu TS (1999) Late Tertiary development of aridification in northwestern China: link with the arctic ice-sheet formation and Tibetan uplifts. Quaternary Science 6, 556–566. [in Chinese with English abstract]
Hamrick J, Godt MJW (1989Allozyme diversity in plant species. In ‘Plant population genetics, breeding and genetic resources’. (Eds AHD Brown, .) (Sinauer Assoc.))
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of The Royal Society of London Series B. Biological Sciences 351, 1291–1298.
| Effects of life history traits on genetic diversity in plant species.Crossref | GoogleScholarGoogle Scholar |
Harle KJ, Heijnis H, Chisari AP, Kershaw AP, Zoppi U, Jacobsen G (2002) A chronology for the long pollen record from Lake Wangoom, western Victoria (Australia) as delivered from uranium/thorium disequilibrium dating. Journal of Quaternary Science 17, 707–720.
| A chronology for the long pollen record from Lake Wangoom, western Victoria (Australia) as delivered from uranium/thorium disequilibrium dating.Crossref | GoogleScholarGoogle Scholar |
Hasumi H, Emori S (2004) ‘K-1 coupled GCM (MIROC) description.’ (Centre for Climate System Research, University of Tokyo: Tokyo)
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society. Linnean Society of London 58, 247–276.
| Some genetic consequences of ice ages, and their role in divergence and speciation.Crossref | GoogleScholarGoogle Scholar |
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.
| The genetic legacy of the Quaternary ice ages.Crossref | GoogleScholarGoogle Scholar | 10879524PubMed |
Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of The Royal Society of London Series B. Biological Sciences 359, 183–195.
| Genetic consequences of climatic oscillations in the Quaternary.Crossref | GoogleScholarGoogle Scholar | 15101575PubMed |
Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH, Johnson JB, Rissler L, Victoriano PF, Yoder AD (2010) Phylogeography’s past, present, and future: 10 years after. Molecular Phylogenetics and Evolution 54, 291–301.
| Phylogeography’s past, present, and future: 10 years after.Crossref | GoogleScholarGoogle Scholar | 19755165PubMed |
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
| Very high resolution interpolated climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |
Jia DR, Abbott RJ, Liu TL, Mao KS, Bartish IV, Liu JQ (2012) Out of the Qinghai–Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophaë rhamnoides (Elaeagnaceae). New Phytologist 194, 1123–1133.
| Out of the Qinghai–Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophaë rhamnoides (Elaeagnaceae).Crossref | GoogleScholarGoogle Scholar | 22432741PubMed |
Kershaw AP, Dcosta DM, Mason J, Wagstaff BE (1991) Palynological evidence for Quaternary vegetation and environments of mainland southeastern Australia. Quaternary Science Reviews 10, 391–404.
| Palynological evidence for Quaternary vegetation and environments of mainland southeastern Australia.Crossref | GoogleScholarGoogle Scholar |
Kool A, de Boer HJ, Krügerü Å, Rydberg A, Abbad A, Björk L, Martin G (2012) Molecular identification of commercialized medicinal plants in southern Morocco. PLoS One 7, e39459
| Molecular identification of commercialized medicinal plants in southern Morocco.Crossref | GoogleScholarGoogle Scholar | 22761800PubMed |
Leipold M, Tausch S, Poschlod P, Reisch C (2017) Species distribution modeling and molecular markers suggest longitudinal range shifts and cryptic northern refugia of the typical calcareous grassland species Hippocrepis comosa (horseshoe vetch). Ecology and Evolution 7, 1919–1935.
| Species distribution modeling and molecular markers suggest longitudinal range shifts and cryptic northern refugia of the typical calcareous grassland species Hippocrepis comosa (horseshoe vetch).Crossref | GoogleScholarGoogle Scholar | 28331599PubMed |
Li XW (1990) ‘Flora of China. Vol. 50.’ (Science Press: Beijing)
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. Journal of Systematics and Evolution 50, 351–361.
| Response of a desert shrub to past geological and climatic change: a phylogeographic study of Reaumuria soongarica (Tamaricaceae) in western China.Crossref | GoogleScholarGoogle Scholar |
Lima JS, Telles MPC, Chaves LJ, Lima-Ribeiro MS, Collevatti RG (2017) Demographic stability and high historical connectivity explain the diversity of a savanna tree species in the Quaternary. Annals of Botany 119, 645–657.
| Demographic stability and high historical connectivity explain the diversity of a savanna tree species in the Quaternary.Crossref | GoogleScholarGoogle Scholar | 28115317PubMed |
Liu YX (1982) Observations on the formation of Chinese desert floras. Acta Phytotaxonomica Sinica 20, 131–140.
Liu YX (1987) ‘Desert flora of China. Vol. 2.’ (Science Press: Beijing)
Liu YX (1995) A study on origin and formation of the Chinese desert flora. Journal of Systematics and Evolution 33, 131–143.
Liu JQ, Qin XG (2005) Evolution of the environmental framework and oasis in the Tarim Basin. Quaternary Sciences 25, 533–539. [in Chinese with English abstract]
Liu SL, Wang LD, Gao ZH, Zhong SJ (1996) Cuttage experiment of Tamarix taklamakanensis. Journal of Gansu Forestry Science and Technology 3, 36–38.
Luo C, Peng ZC, Yang D, Liu WG, Zhang ZF, He JF, Chou CL (2009) A lacustrine record from Lop Nur, Xinjiang, China: implications for paleoclimate change during Late Pleistocene. Journal of Asian Earth Sciences 34, 38–45.
| A lacustrine record from Lop Nur, Xinjiang, China: implications for paleoclimate change during Late Pleistocene.Crossref | GoogleScholarGoogle Scholar |
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Human Biology 76, 173–190.
| Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm.Crossref | GoogleScholarGoogle Scholar | 15359530PubMed |
Miller M (2005) Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. The Journal of Heredity 96, 722–724.
| Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information.Crossref | GoogleScholarGoogle Scholar | 16251514PubMed |
Monmonier MS (1973) Maximum‐difference barriers: an alternative numerical regionalization method. Geographical Analysis 5, 245–261.
| Maximum‐difference barriers: an alternative numerical regionalization method.Crossref | GoogleScholarGoogle Scholar |
Mu GJ (1994) On the age and evolution of the Taklimakan desert. Arid Land Geography 17, 1–9. [in Chinese with English abstract]
Nei M (1987) ‘Molecular evolutionary genetics.’ (Columbia University Press: New York)
Ossa PG, Armesto JJ, Pérez F (2017) Assessing the influence of life form and life cycle on the response of desert plants to past climate change: genetic diversity patterns of an herbaceous lineage of Nolana along western South America. American Journal of Botany 104, 1533–1545.
| Assessing the influence of life form and life cycle on the response of desert plants to past climate change: genetic diversity patterns of an herbaceous lineage of Nolana along western South America.Crossref | GoogleScholarGoogle Scholar | 29885223PubMed |
Pan XL (1994) The study on Tarim basin flora. Journal of Xinjiang University 11, 77–83. [Natural Science Edition]
Pan BR (1998) The diversity of the Tamaricaceae in China and its conservation strategy. In ‘Biodiversity and the future of human beings. Proceedings of the Second National Symposium on the conservation and sustainable use of biological Diversity’. (Eds Biodiversity Committee of the Chinese Academy of Sciences, Department for Wildlife and Forest Plants Protection of the Ministry of Forestry, Department of Natural Conservation of the National Environmental Protection Agency, Chinese Academy of Agricultural Sciences, Department of Science and Technology of the State Education Commission) pp. 114–121. (China Forestry Publishing House: Beijing)
Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31, 161–175.
| Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation.Crossref | GoogleScholarGoogle Scholar |
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, 231–259.
| Maximum entropy modeling of species geographic distributions.Crossref | GoogleScholarGoogle Scholar |
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237–1245.
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conservation Biology 17, 230–237.
| Correlation between fitness and genetic diversity.Crossref | GoogleScholarGoogle Scholar |
Rebernig CA, Schneeweiss GM, Bardy KE, Schonswetter P, Villasenor JL, Obermayer R, Stuessy TF, Weiss-Schneeweiss H (2010) Multiple Pleistocene refugia and Holocene range expansion of an abundant southwestern American desert plant species (Melampodium leucanthum, Asteraceae). Molecular Ecology 19, 3421–3443.
| Multiple Pleistocene refugia and Holocene range expansion of an abundant southwestern American desert plant species (Melampodium leucanthum, Asteraceae).Crossref | GoogleScholarGoogle Scholar | 20670366PubMed |
Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.
Rosenberg MS (2001) PASSAGE: pattern analysis, spatial statistics and geographic exegesis. Ver. 1.1. (Department of Biology, Arizona State University: Tucson, AZ, USA)
Sampson J, Tapper S, Coates D, Hankinson M, Mcarthur S, Byrne M (2018) Persistence with episodic range expansion from the early Pleistocene: the distribution of genetic variation in the forest tree Corymbia calophylla (Myrtaceae) in south-western Australia. Biological Journal of the Linnean Society. Linnean Society of London 123, 545–560.
| Persistence with episodic range expansion from the early Pleistocene: the distribution of genetic variation in the forest tree Corymbia calophylla (Myrtaceae) in south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84, 1120–1136.
| Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae).Crossref | GoogleScholarGoogle Scholar | 21708667PubMed |
Schönswetter P, Popp M, Brochmann C (2006) Rare arctic-alpine plants of the European alps have different immigration histories: the snow bed species Minuartia biflora and Ranunculus pygmaeus. Molecular Ecology 15, 709–720.
| Rare arctic-alpine plants of the European alps have different immigration histories: the snow bed species Minuartia biflora and Ranunculus pygmaeus.Crossref | GoogleScholarGoogle Scholar | 16499696PubMed |
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends in Ecology & Evolution 22, 25–33.
| Genetic monitoring as a promising tool for conservation and management.Crossref | GoogleScholarGoogle Scholar |
Shaw J, Lickey E, Beck JT, Farmer SB, Liu W, 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. American Journal of Botany 92, 142–166.
| The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 21652394PubMed |
Shi YF, Cui ZJ, Su Z (2005) ‘The Quaternary glaciations and environmental variations in China.’ pp. 99–100. (Hebei Science and Technology Publishing House: Hebei, China)
Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49, 369–381.
| Gaps as characters in sequence-based phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 12118412PubMed |
Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555–562.
Su ZH, Zhang ML (2013) Evolutionary response to Quaternary climate aridification and oscillations in northwestern China revealed by chloroplast phylogeography of Nitraria sphaerocarpa (Nitrariaceae). Biological Journal of the Linnean Society. Linnean Society of London 109, 757–770.
| Evolutionary response to Quaternary climate aridification and oscillations in northwestern China revealed by chloroplast phylogeography of Nitraria sphaerocarpa (Nitrariaceae).Crossref | GoogleScholarGoogle Scholar |
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
| Evolutionary history of a desert shrub Ephedra przewalskii (Ephedraceae): allopatric divergence and range shifts in northwestern China.Crossref | GoogleScholarGoogle Scholar | 27351630PubMed |
Su ZH, Pan BR, Zhang ML, Shi W (2016) Conservation genetics and geographic patterns of genetic variation of endangered shrub Ammopiptanthus (Fabaceae) in northwestern China. Conservation Genetics 17, 485–496.
| Conservation genetics and geographic patterns of genetic variation of endangered shrub Ammopiptanthus (Fabaceae) in northwestern China.Crossref | GoogleScholarGoogle Scholar |
Su ZH, Richardson BA, Zhuo L, Jiang XL, Li WJ, Kang XS (2017) Genetic diversity and structure of an endangered desert shrub and the implications for conservation. AoB Plants 9, plx016
| Genetic diversity and structure of an endangered desert shrub and the implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Sun JM, Zhang LY, Deng CL, Zhu RX (2008) Evidence for enhanced aridity in the Tarim Basin of China since 5.3 Ma. Quaternary Science Reviews 27, 1012–1023.
| Evidence for enhanced aridity in the Tarim Basin of China since 5.3 Ma.Crossref | GoogleScholarGoogle Scholar |
Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240, 1285–1293.
| Measuring the accuracy of diagnostic systems.Crossref | GoogleScholarGoogle Scholar | 3287615PubMed |
Taberlet P, Cheddadi R (2002) Quaternary refugia and persistence of biodiversity. Science 297, 2009–2010.
| Quaternary refugia and persistence of biodiversity.Crossref | GoogleScholarGoogle Scholar | 12242431PubMed |
Tajima F (1983) Evolutionary relationships of DNA sequences in finite populations. Genetics 105, 437–460.
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143, 1457–1465.
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |
Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
Wang Q, Abbott RJ, Yu QS, Lin K, Liu JQ (2013) Pleistocene climate change and the origin of two desert plant species, Pugionium cornutum and Pugionium dolabratum (Brassicaceae), in northwest China. New Phytologist 199, 277–287.
| Pleistocene climate change and the origin of two desert plant species, Pugionium cornutum and Pugionium dolabratum (Brassicaceae), in northwest China.Crossref | GoogleScholarGoogle Scholar | 23550542PubMed |
Williams MAJ, Dunkerley DL, De Dekker P, Kershaw AP, Stokes T (1993) ‘Quaternary environments.’ (Edward Arnold: London)
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAS. Proceedings of the National Academy of Sciences of the United States of America 84, 9054–9058.
Xu X, 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.
| Late Quaternary glaciation in the Tianshan and implications for palaeoclimatic change: a review.Crossref | GoogleScholarGoogle Scholar |
Yang QE, Gaskin J (2007) Tamaricaceae. In ‘Flora of China. Vol. 13’. (Eds ZY Wu, PH Raven) pp. 60–64. (Science Press: Beijing)
Yang YJ, Yuan HB, Liu SJ, Zhang JC, Tang JN, Ding F (2013) Tamarix taklamakanensis populations and their environmental factors in the Kumtag Desert. Arid Zone Research 30, 827–831.
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends in Ecology & Evolution 11, 413–418.
| The population genetic consequences of habitat fragmentation for plants.Crossref | GoogleScholarGoogle Scholar |
Yuan HB, Zhang JC, Chu JM, Liu SJ, Tang JN, Ding F (2011) Characteristics of the age plant populations structures of three typical in Kumtag Desert. Acta Botanica Boreali-Occidentalia 31, 2301–2309.
Zhang H, Wu JW, Zheng QH, Yu YJ (2003) A preliminary study of oasis evolution in the Tarim Basin, Xinjiang, China. Journal of Arid Environments 55, 545–553.
| A preliminary study of oasis evolution in the Tarim Basin, Xinjiang, China.Crossref | GoogleScholarGoogle Scholar |
Zheng HB, Powell CM, Butcher K, Cao JJ (2003) Late Neogene loess deposition in southern Tarim Basin: tectonic and palaeoenvironmental implications. Tectonophysics 375, 49–59.
| Late Neogene loess deposition in southern Tarim Basin: tectonic and palaeoenvironmental implications.Crossref | GoogleScholarGoogle Scholar |
Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology 17, 2107–2121.
| Mitochondrial DNA under siege in avian phylogeography.Crossref | GoogleScholarGoogle Scholar | 18397219PubMed |
