Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Phylogeography of the rare Gymnocarpos przewalskii (Caryophyllaceae): indications of multiple glacial refugia in north-western China

S. M. Ma A B , M. L. Zhang A C E and S. C. Sanderson D
+ 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 Graduate University of the Chinese Academy of Sciences, Beijing 100049, China.

C Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.

D Shrub Sciences Laboratory, Intermountain Research Station, Forest Service, U.S. Department of Agriculture, Utah 84606, USA.

E Corresponding author. Email: zhangml@ibcas.ac.cn

Australian Journal of Botany 60(1) 20-31 https://doi.org/10.1071/BT11055
Submitted: 16 February 2011  Accepted: 12 December 2011   Published: 3 February 2012

Abstract

We investigated the phylogeography of Gymnocarpos przewalskii Maxim. (Caryophyllaceae), a rare relictual shrub restricted to north-western China, in the context of Quaternary climate oscillations. Three cpDNA regions (psbA–trnH, ycf6–psbM and rpl32–trnL (UAG)) were sequenced for 160 individuals from 16 populations. High genetic diversity (hT = 0.930, hS = 0.425) and a significant phylogeographic structure (NST > GST, P < 0.01) were identified; 31 different cpDNA haplotypes were detected. Phylogenetic analyses showed that the haplotypes were clustered into five clades, consistent with their distributions in the following four geographic regions: the Tarim Basin, Hami Basin, the western Yumen of Gansu Province and an easternmost region, consisting of populations in the Wulate Rear Banner region in Inner Mongolia, the Jinta and Jingyuan regions in Gansu Province and the Zhongwei region in Ningxia. The existence of regional divergence was supported by AMOVA, which revealed that ~63% of variation was due to differences among the four geographic regions. Four independent glacial refugia were inferred, in the western Tarim Basin, Hami Basin, the Liuyuan region in western Gansu and the easternmost region mentioned. Population bottlenecks and postglacial recolonisation were identified in the northern Tarim Basin, western Yumen and the Jinta region in Gansu Province.


References

Avise JC (2000) ‘Phylogeography: the history and formation of species.’ (Harvard University Press: Cambridge, MA)

Bandelt HJ, Forster P, Röhl A (1999) Median joining networks for inferring intraespecific phylogenies. Molecular Biology and Evolution 16, 37–48.

Barker JS, Frydenberg J, González J, Davies HI, Ruiz A, Sørensen JG, Loeschcke V (2009) Bottlenecks, population differentiation and apparent selection at microsatellite loci in Australian Drosophila buzzatii. Heredity 102, 389–401.
Bottlenecks, population differentiation and apparent selection at microsatellite loci in Australian Drosophila buzzatii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1Kjs7w%3D&md5=3fca3a6d956afb85f6c70f31dfa2266eCAS |

Chang ZY, Xu LR, Wu ZH (2004) Comparative morphology, ecology and geographical distribution of Calophaca sinica and C. soongorica. Acta Botanica Boreali Occidentalia Sinica 24, 2312–2320. [in Chinese, with English abstract]

Chai YQ, Chao ZZ, Cai ZS (2010) A study on species diversity of a Gymnocarpos przewalskii community in the Subei desert. Acta Prataculturae Sinica 19, 21–27. [in Chinese, with English abstract]

Chen GQ, Huang HW, Ge XJ (2005) Allozyme diversity and population differentiation in an endangered plant, Ammopiptanthus nanus (Leguminosae). Journal of Wuhan Botanical Research 23, 131–137. [in Chinese, with English abstract]

Chen GQ, Huang HW, Crawford DJ, Pan BR, Ge XJ (2009) Mating system and genetic diversity of a rare desert legume Ammopiptanthus nanus (Leguminosae). Journal of Systematics and Evolution 47, 57–66.
Mating system and genetic diversity of a rare desert legume Ammopiptanthus nanus (Leguminosae).Crossref | GoogleScholarGoogle Scholar |

Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends in Plant Science 3, 432–438.

Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134, 959–969.

Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11–15.

Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11, 2571–2581.
A simulated annealing approach to define the genetic structure of populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nptlaksw%3D%3D&md5=48f25549155d62dcec4cae2e461e31eeCAS |

Dutech C, Maggia L, Joly HI (2000) Chloroplast diversity in Vouacapoua Americana (Caesalpiniaceae), a neotropical forest tree. Molecular Ecology 9, 1427–1432.
Chloroplast diversity in Vouacapoua Americana (Caesalpiniaceae), a neotropical forest tree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFCmu7c%3D&md5=6835d4402f3ff2eedc2fb9b3c6ed35b1CAS |

Excoffier L, Smouse PE, Quattro JM (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 1, 47–50.

Falchi A, Paolini J, Desjobert JM, Melis A, Costa J, Varesi L (2009) Phylogeography of Cistus creticus L. on Corsica and Sardinia inferred by the trnL–F and pl32–trnL sequences of cpDNA. Molecular Phylogenetics and Evolution 52, 538–543.
Phylogeography of Cistus creticus L. on Corsica and Sardinia inferred by the trnL–F and pl32–trnL sequences of cpDNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms12htro%3D&md5=5ba3b5b723b565d99c40c8cb6c58f53eCAS |

Fang XM, Lu LQ, Yang SL, Li JJ, An ZS, Jiang P, Chen XL (2002) Loess in Kunlun Mountains and its implications on desert development and Tibetan Plateau uplift in west China. Science China Earth Sciences 45, 289–299.
Loess in Kunlun Mountains and its implications on desert development and Tibetan Plateau uplift in west China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFWitb4%3D&md5=91d1875ad855dd2b3809134896155677CAS | [Science in China Series D]

Fan ZL (1993) A study on the formation and evolution of oases in Tarim Basin. Acta Geographica Sinica 5, 421–427. [in Chinese, with English abstract]

Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |

Fu LG (1992) ‘China plant red data book.’ (Science Press: Beijing) [in Chinese].

Fu XY (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.

Ge XJ, Yu Y, Yuan YM, Huang HW, Yan C (2005) Genetic diversity and geographic differentiation in endangered Ammopiptanthus (Leguminosae) populations in desert regions of northwest China as revealed by ISSR analysis. Annals of Botany 95, 843–851.
Genetic diversity and geographic differentiation in endangered Ammopiptanthus (Leguminosae) populations in desert regions of northwest China as revealed by ISSR analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFOrtrw%3D&md5=70f370f42e7d870fdf5985bbce407bfcCAS |

Ge XJ, Hwang CC, Liu ZH, Huang CC, Huang WH, Huang KH, Wang WK, Chiang TY (2011) Conservation genetics and phylogeography of endangered and endemic shrub Tetraena mongolica (Zygophyllaceae) in Inner Mongolia, China. BMC Genetics 12, 1–12.
Conservation genetics and phylogeography of endangered and endemic shrub Tetraena mongolica (Zygophyllaceae) in Inner Mongolia, China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosVOjsw%3D%3D&md5=700358682e75484de5daafe6fe799034CAS |

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 Sciences 6, 556–566. [in Chinese, with English abstract]

Guo YP, Zhang R, Chen CY, Zhou DW, Liu JQ (2010) Allopatric divergence and regional range expansion of Juniperus sabina in China. Journal of Systematics and Evolution 48, 153–160.
Allopatric divergence and regional range expansion of Juniperus sabina in China.Crossref | GoogleScholarGoogle Scholar |

Hamilton M (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molecular Ecology 8, 521–523.

Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.
The genetic legacy of the Quaternary ice ages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXks1Wmu78%3D&md5=eea8c2586ae45c6cf90b99bd59ca1af2CAS |

Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=0a978b6b632b2af37310c5afba9775e4CAS |

Li N, Fu L (1997) Notes on gymnosperms I. Taxonomic treatment of some Chinese conifers. Novon 7, 261–264.
Notes on gymnosperms I. Taxonomic treatment of some Chinese conifers.Crossref | GoogleScholarGoogle Scholar |

Li WC (1998) ‘The Chinese Quaternary vegetation and environment.’ (Science Press: Beijing) [in Chinese].

Ma SM, Zhang ML, Zhang HX, Meng HH, Chen X (2010) Predicting potential geographical distributions and patterns of the relic plant Gymnocarpos przewalskii using maximum entropy and genetic algorithm for rule-set prediction. Chinese Journal of Plant Ecology 34, 1327–1335. [in Chinese, with English abstract]

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)

Oxelman B, Ahlgren B, Thulin M (2002) Circumscription and phylogenetic relationships of Gymnocarpos (Caryophyllaceae–Paronychioideae). Edinburgh Journal of Botany 59, 221–237.
Circumscription and phylogenetic relationships of Gymnocarpos (Caryophyllaceae–Paronychioideae).Crossref | GoogleScholarGoogle Scholar |

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 P, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300, 1563–1565.
Glacial refugia: hotspots but not melting pots of genetic diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlKruro%3D&md5=56f48fc265b264f6e610ab550badabeaCAS |

Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237–1245.

Printzen C, Ekman S, Tonsberg T (2003) Phylogeography of Cavernularia hultenii: evidence of slow genetic drift in a widely disjunct lichen. Molecular Ecology 12, 1473–1486.
Phylogeography of Cavernularia hultenii: evidence of slow genetic drift in a widely disjunct lichen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3jsVWluw%3D%3D&md5=c0534e22c443fa2f30371b1fd259c533CAS |

Raspé O, Saumitou-Laprade P, Cuguen J, Jacquemart AL (2000) Chloroplast DNA haplotype variation and population differentiation in Sorbus aucuparia L. (Rosaceae: Maloideae). Molecular Ecology 9, 1113–1122.
Chloroplast DNA haplotype variation and population differentiation in Sorbus aucuparia L. (Rosaceae: Maloideae).Crossref | GoogleScholarGoogle Scholar |

Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.
DnaSP, DNA polymorphism analyses by the coalescent and other methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVSisLo%3D&md5=0617c6a6e994b961cc3584cdc63073f5CAS |

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 | 1:CAS:528:DyaK2sXlvFejuro%3D&md5=13496d28438605a52d68b15ccca4bc07CAS |

Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152, 1079–1089.

Shackleton NJ, Opdyke ND (1973) Oxygen isotope and palaeomagnetic stratigraphy of equatorial Pacific core v28–238 isotope temperatures and ice volumes on a 105 year and 106 year scale. Quaternary Research 3, 39–55.
Oxygen isotope and palaeomagnetic stratigraphy of equatorial Pacific core v28–238 isotope temperatures and ice volumes on a 105 year and 106 year scale.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXkvVWrtrc%3D&md5=889a3ce03e5627d6219c1168277ce218CAS |

Shan WJ, Liu J, Yu L, Robert WM, Mahmut H, Zhang YP (2011) Genetic consequences of postglacial colonization by the endemic Yarkand hare (Lepus yarkandensis) of the arid Tarim Basin. Chinese Science Bulletin 56, 1370–1382.
Genetic consequences of postglacial colonization by the endemic Yarkand hare (Lepus yarkandensis) of the arid Tarim Basin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltVygtrs%3D&md5=04f94774801ce08e84550aefe2b46db6CAS |

Shaw J, Lickey E, Schilling E, Small R (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms, the tortoise and the hare III. American Journal of Botany 94, 275–288.
Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms, the tortoise and the hare III.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFOjsLg%3D&md5=eb08d32a392ba8ca394a3226c0836872CAS |

Shaw J, Small RL (2005) Chloroplast DNA phylogeny and phylogeography of the North American plums (Prunus subgenus Prunus section Prunocerasus, Rosaceae). American Journal of Botany 92, 2011–2030.

Shen L, Chen XY, Li YY (2002) Glacial refugia and postglacial recolonization patterns of organisms. Acta Ecologica Sinica 22, 1983–1990. [in Chinese, with English abstract]

Shen L, Chen XY, Zhang X, Li YY, Fu CX, Qiu YX (2005) Genetic variation of Ginkgo biloba L. (Ginkgoaceae) based on cpDNA PCR–RFLPs: inference of glacial refugia. Heredity 94, 396–401.
Genetic variation of Ginkgo biloba L. (Ginkgoaceae) based on cpDNA PCR–RFLPs: inference of glacial refugia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1Oru78%3D&md5=aeb72431d7fd26b42f6f0c5a8557aa5fCAS |

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.

Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=bd47fc55681f7cfb27c8dbaa3b3d2672CAS |

Thompson JDTJ, Gibson PF, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=2074c8485c32f38a18ac176dd31f6555CAS |

Van der Pijl L (1969) ‘Principles of dispersal in higher plants.’ (Springer Verlag Press: Berlin)

Vidal-Russell R, Souto CP, Premoli AC (2011) Multiple Pleistocene refugia in the widespread Patagonian tree Embothrium coccineum (Proteaceae). Australian Journal of Botany 59, 299–314.

Wang GH (2005) The western Ordos plateau as a biodiversity center of relic shrubs in arid areas of China. Biodiversity and Conservation 14, 3187–3200.
The western Ordos plateau as a biodiversity center of relic shrubs in arid areas of China.Crossref | GoogleScholarGoogle Scholar |

Wang HW, Ge S (2006) Phylogeography of the endangered Cathaya Argyrophylla (Pinaceae) inferred from sequence variation of mitochondrial and nuclear DNA. Molecular Ecology 15, 4109–4122.
Phylogeography of the endangered Cathaya Argyrophylla (Pinaceae) inferred from sequence variation of mitochondrial and nuclear DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlSmsrnJ&md5=6be51b197f7005e0862be289e6179105CAS |

Wang LY, Abbott RJ, Zheng W, Chen P, Wang YJ, Liu JQ (2009a) History and evolution of alpine plants endemic to the Qinghai–Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae). Molecular Ecology 18, 709–721.
History and evolution of alpine plants endemic to the Qinghai–Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae).Crossref | GoogleScholarGoogle Scholar |

Wang ZB, Gao QX, Sun JZ, Ma QL (2009b) Study on biological characteristics of rare endangered plant Gymnocarpos Przewalskii. Resource Development & Market 25, 481–509. [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. Marine Geology and Quaternary Geology 26, 93–100. [in Chinese, with English abstract]

Yang Y, Liu M (2002) Cenozoic deformation of the Tarim plate and the implications for mountain building in the Tibetan Plateau and the Tian Shan. Tectonics 21, 1059–1076.
Cenozoic deformation of the Tarim plate and the implications for mountain building in the Tibetan Plateau and the Tian Shan.Crossref | GoogleScholarGoogle Scholar |

Yuan QJ, Zhang ZY, Peng H, Ge S (2008) Chloroplast phylogeography of Dipentodon (Dipentodontaceae) in southwest China and northern Vietnam. Molecular Ecology 17, 1054–1065.
Chloroplast phylogeography of Dipentodon (Dipentodontaceae) in southwest China and northern Vietnam.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVajurY%3D&md5=0c27075ae42a22bd028bbb946d0e9cabCAS |

Zawko G, Krauss SL, Dixon KW, Sivasithamparam K (2001) Conservation genetics of the rare and endangered Leucopogon obtectus (Ericaceae). Molecular Ecology 10, 2389–2396.
Conservation genetics of the rare and endangered Leucopogon obtectus (Ericaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXot1Sqtrs%3D&md5=3eaee93af0cf238e28b3cc944cbe9a4fCAS |

Zhang DF, Fengquan L, Jianmin B (2000) Eco-environmental effects of the Qinghai–Tibet Plateau uplift during the Quaternary in China. Environmental Geology 39, 1352–1358.
Eco-environmental effects of the Qinghai–Tibet Plateau uplift during the Quaternary in China.Crossref | GoogleScholarGoogle Scholar |

Zhao YZ (1997) Endemic genera and their basic characteristics of the Mongolian Plateau plants. Acta Scientiarum Naturalium Universitatis NeiMongol 28, 547–552. [in Chinese, with English abstract]