Skip to main content

Advertisement

SpringerLink
Log in

Chloroplast DNA phylogeographic analysis reveals significant spatial genetic structure of the relictual tree Davidia involucrata (Davidiaceae)

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The dove tree, Davidia involucrata Baill. (Davidiaceae), is a relict species endemic to China. Human activities and the strict requirements for seedling recruitments have led to the decline in number of individuals in extant natural populations of this species. In order to provide information for the design of conservation management strategies for D. involucrata, we investigated the phylogeographical pattern of this relict tree. Our sampling included 256 individuals from 32 natural populations of D. involucrata in China and we sequenced six chloroplast DNA (cpDNA) non-coding regions. We distinguished a total of 13 different cpDNA haplotypes. From the cpDNA variation in D. involucrata, we found a very high level of regional differentiation (F ST = 0.812) and a strong phylogeographical pattern (N ST = 0.996 > G ST = 0.981, P < 0.05). Phylogenetic analysis reveals three main cpDNA haplotype lineages and four population groups. The split between these geographical groups can be dated back from the late Pliocene to early Pleistocene. Non-overlapping distribution of chloroplast haplotypes and high genetic differentiation among four distinct geographical groups suggest that D. involucrata probably survives in four separate glacial refugia. Our findings have an important implication for conservation of its genetic diversity. The deduced glacial survival areas for D. involucrata should be recognized as four “evolutionary significant units” and be considered as separate targets in conserving its genetic diversity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Google Scholar 

  • Axelrod DI, Al-Shehba I, Raven PH (1996) History of the modern flora of China. In: Zhang AL, Wu SG (eds) Floristic characteristics and diversity of East Asian plants. Springer, New York, pp 43–55

    Google Scholar 

  • Bai WN, Liao WJ, Zhang DY (2010) Nuclear and chloroplast DNA phylogeography reveal two refuge areas with asymmetrical gene flow in a temperate walnut tree from East Asia. New Phytol 188:892–901

    Article  PubMed  Google Scholar 

  • Budantsev LY (2006) The western Kamchatka early Paleogene flora. Trans Bot Inst Russian Acad Sci 22:1–160

    Google Scholar 

  • Byrne M (2007) Phylogeography provides an evolutionary context for the conservation of a diverse and ancient flora. Aust J Bot 55:316–325

    Article  Google Scholar 

  • Chiang TY, Schaal BA (1999) Phylogeography of ten North American Hylocomium splendens based on nrDNA ITS sequences. Mol Ecol 8:1037–1042

    Article  CAS  Google Scholar 

  • Chou YW, Thomas PI, Ge XJ, LePage BA, Wang CN (2011) Refugia and phylogeography of Taiwania in East Asia. J Biogeogr 38:1992–2005

    Article  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–221

    Article  PubMed Central  PubMed  Google Scholar 

  • Du YJ (2012) Studies on population genetics and phylogeography of Davidia involucrata (Davidiaceae). PH.D. Dissertation, Zhejiang University, Hangzhou (in Chinese with English abstract)

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    Article  CAS  PubMed  Google Scholar 

  • Eiserhardt WL, Svenning JC, Kissling WD, Balslev H (2011) Geographical ecology of the palms (Arecaceae): determinants of diversity and distributions across spatial scales. Ann Bot 108:1391–1416

    Article  PubMed Central  PubMed  Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–259

    Article  Google Scholar 

  • Escuderoa A, Iriondob JM, Torres ME (2003) Spatial analysis of genetic diversity as a tool for plant conservation. Biol Conserv 113:351–365

    Article  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed Central  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2006) ARLEQUIN version 3.1: a software for population genetic data analysis. Computational and molecular population genetics laboratory, Institute of Zoology, University of Berne, Switzerland

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitch-hiking, and background selection. Genetics 147:915–925

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fu DZ, Endress PK (2001) Cercidiphyllaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol. 6. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis, MO, p 126

  • Fu LK, Jin JM (1992) China plant red data book. Science Press, Beijing

    Google 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 16:4684–4698

    Article  CAS  PubMed  Google Scholar 

  • Ge XJ, Chiang YC, Chou CH, Chiang TY (2002) Nested clade analysis of Dunnia sinensis, a monotypic genus of the Rubiaceae, from China based on organelle DNA sequences. Conserv Genet 3:351–362

    Article  CAS  Google Scholar 

  • Gladenkov YB, Sinel’nikova VN, Chelebaeva AI, Shantser AE (2005) Biosphere–Ecosystem–Biota during the Earth’s past. Ecosystems in the Cenozoic of the Northern Pacific. Eocene–Oligocene of western Kamchatka and adjacent regions (Contribution to Academician V.V. Menner’s 100th Birthday)

  • Gong W, Chen C, Dobes C, Fu CX, Koch MA (2008) Phylogeography of a living fossil, Pleistocene glaciations forced Ginkgo biloba L. (Ginkgoaceae) into two refuge areas in China with limited subsequent postglacial expansion. Mol Phylogenet Evol 48:1094–1105

    Article  PubMed  Google Scholar 

  • Guan BC, Fu CX, Qiu YX, Zhou SL, Comes HP (2010) Genetic structure and breeding system of a rare understory herb, Dysosma versipellis (Berberidaceae), from temperate deciduous forests in China. Am J Bot 97:111–122

    Article  CAS  PubMed  Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  • Harrison SP, Yu G, Takahara H, Prentice IC (2001) Palaeovegetation: diversity of temperate plants in East Asia. Nature 413:129–130

    Article  CAS  PubMed  Google Scholar 

  • He JS, Lin H, Chen WL (1995) The current status of endemic and endangered species Davidia involucrata and the preserving strategies. Chin Biodivers 3:213–221

    Google Scholar 

  • Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, Rascaria-Lacoste N, Hardy OJ, Vekemans X, Vendramin GG (2004) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Mol Ecol 13:3437–3452

    Article  CAS  PubMed  Google 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 10:2669–2681

    Article  CAS  PubMed  Google Scholar 

  • Kokawa S (1965) Fossil endocarp of Davidia in Japan. J Biol, Osaka City University 16: 45–51

  • Lei M, Wang Q, Wu ZJ, Lopez-Pujol J, Li DZ, Zhang ZY (2012) Molecular phylogeography of Fagus engleriana (Fagaceae) in subtropical China: limited admixture among multiple refugia. Tree Genet Genomes 8:1203–1212

    Article  Google Scholar 

  • Li XW, Li J (1993) A preliminary floristic study on the seed plants from the region of Hengduan Mountain. Acta Bot Yunnan 15:217–231 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Li JQ, Zhang MH, Huang HW, Cai Q (2000) On the allozymic loci variation of Davidia involucrata. J Wuhan Bot Res 18:247–249 (in Chinese with English abstract)

    Google Scholar 

  • Li XP, He ZQ, Chen FJ, Liang HW, Li FL (2006) RAPD analysis for the genetic diversity of four populations of Davidia involucrata Baill. in Shennongjia area, Hubei Province. J Beijing For Univ 28:66–70 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Li AX, Yi S, Qiu YX, Guo JT, Comes HP, Fu CX (2008) Phylogeography of two East Asian species in Croomia (Stemonaceae) inferred from chloroplast DNA and ISSR fingerprinting variation. Mol Phylogenet Evol 49:702–714

    Article  CAS  PubMed  Google Scholar 

  • Li XP, Li ZL, He CL, Zhu WY, Gao SP (2012a) Genetic diversity of the endangered Davidia involucrata by AFLP analysis. Acta Hortic Sin 39:992–998 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Li XP, Zheng X, Zhu WY, He CL, Gao SP (2012b) Genetic diversity and genetic structure analysis of the endangered Davidia involucrata Baill. by ISSR. Guangdong Agric Sci 6:121–123 (in Chinese with English abstract)

    Google Scholar 

  • Luo SJ, He YH, Ning GG, Zhang JQ, Ma GY, Bao MZ (2011) Genetic diversity and genetic structure of different populations of the endangered species Davidia involucrata in China detected by inter-simple sequence repeat analysis. Trees 25:1063–1071

    Article  Google Scholar 

  • Mancheste SR, Chen ZD, Lu AM, Uemura K (2009) Eastern Asian endemic seed plant genera and their paleogeographic history throughout the Northern Hemisphere. J Syst Evol 47:1–42

    Article  Google Scholar 

  • Manchester SR (2002) Leaves and fruits of Davidia (Cornales) from the Paleocene of North America. Syst Bot 27:368–382

    Google Scholar 

  • Moritz C (1994) Defining significant units for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Pavlyutkin BI (2009) Leaf and fruit remains of Davidia (Cornales) from the Nezhino flora (Miocene of Primorye). Paleontol J 43:339–344

    Article  Google Scholar 

  • Peng YL, Hu YQ, Sun H (2003) Allozyme analysis of Davidia involucrata var. vilmoriniana and its biogeography significance. Acta Bot Yunnan 25:55–62 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    Article  CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Qi XS, Chen C, Comes HP, Sakaguchi S, Liu YH, Tanaka N, Sakio H, Qiu YX (2012) Molecular data and ecological niche modeling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphyllum (Cercidiphyllaceae). New Phytol 196:617–630

    Article  CAS  PubMed  Google Scholar 

  • Qiu YX, Guan BC, Fu CX, Comes HP (2009a) Did glacials and/or interglacials promote allopatric incipient speciation in East Asian temperate plants? Phylogeographic and coalescent analyses on refugial isolation and divergence in Dysosma versipellis. Mol Phylogenet Evol 51:281–293

    Article  CAS  PubMed  Google Scholar 

  • Qiu YX, Qi XS, Jin XF, Tao XY, Fu CX, Naiki A, Comes HP (2009b) Population genetic structure, phylogeography, and demographic history of Platycrater arguta (Hydrangeaceae) endemic to East China and South Japan, inferred from chloroplast DNA sequence variation. Taxon 58:1226–1241

    Google Scholar 

  • Qiu YX, Sun Y, Zong M, Zhang XP, Lee J, Murata J, Fu CX, Comes HP (2009c) Molecular phylogeography of East Asian Kirengeshoma in relation to quaternary climate change and land-bridge configurations. New Phytol 183:480–495

    Article  CAS  PubMed  Google 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 59:225–244

    Article  PubMed  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer

  • Ray N, Adams JM (2001) A GIS-based vegetation map of the world at the last glacial maximum (25,000–15,000 BP). Internet archaeology, 11. Available from: http://www.ncdc.noaa.gov/paleo/pubs/ray2001/ray_adams_2001.pdf/

  • Ren G, Beug HJ (2002) Mapping holocene pollen data and vegetation of northern China. Quat Sci Rev 21:1395–1422

    Article  Google Scholar 

  • Rivera-Ocasio E, Aide TM, McMillan WO (2006) The influence of spatial scale on the genetic structure of a widespread tropical wetland tree, Pterocarpus officinalis (Fabaceae). Conserv Genet 7:251–266

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Saeki I, Murakami N (2009) Chloroplast DNA phylogeography of the endangered Japanese red maple (Acer pycnanthum): the spatial configuration of wetlands shapes genetic diversity. Divers Distrib 15:917–927

    Article  Google 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 152:1079–1089

    PubMed Central  CAS  PubMed  Google Scholar 

  • Song CW, Bao MZ (2006) Genetic diversity of RAPD mark for natural Davidia involucrata populations. Front China 1:95–99

    Article  Google Scholar 

  • Sun JF, Gong YB, Renner SS, Huang SQ (2008) Multifunctional bracts in the dove tree Davidia involucrata (Nyssaceae: Cornales): rain protection and pollinator attraction. Am Nat 171:119–124

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 Res 22:4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tian B, Liu RR, Wang LY, Qiu Q, Chen KM, Liu JQ (2009) Phylogeographic analyses suggests that a deciduous species (Ostryopsis davidiana Decne., Betulaceae) survived in northern China during the Last Glacial Maximum. J Biogeogr 36:2148–2155

    Article  Google Scholar 

  • Tsukagosmh I, Ono Y, Hashimot T (1997) Fossil endocarp of Davidia from the early Pleistocene sediments of the Tokai group in Gifu prefecture, central Japan. Bull Osaka Mus Nat Hist 51:13–23

    Google Scholar 

  • Wang HS (1992) Floristic geography. Science Press, Beijing (in Chinese)

    Google Scholar 

  • Wang HW, Ge S (2006) Phylogeography of the endangered Cathaya argyrophylla (Pinaceae) inferred from sequence variation of mitochondrial and nuclear DNA. Mol Ecol 15:4109–4122

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Gao PX, Kang M, Lowe AJ, Huang HW (2009) Refugia within refugia: the case study of a canopy tree Eurycorymbus cavaleriei in subtropical China. J Biogeogr 36:2156–2164

    Article  Google Scholar 

  • Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu ZY, Wu SG (1996) A proposal for a new floristic kingdom (realm)—the E. Asiatic kingdom, its delimitation and characteristics. In: Zhang AL, Wu SG (eds) Proceedings of the first international symposium on floristic characteristics and diversity of East Asian plants. China Higher Education Press/Springer-Verlag, Beijing, China/Berlin, Heidelberg, Germany, pp 3–42

  • Wu G, Xiao H, Li J, Ma KM (2000) Relationship between human activities and survival of rare and endangered species Davidia involucrata. Chin J Appl Ecol 11:493–496 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Xiang QY, Thomas DT, Xiang QP (2011) Resolving and dating the phylogeny of Cornales—effects of taxon sampling, data partitions, and fossil calibrations. Mol Phylogenet Evol 59:123–138

    Article  PubMed  Google Scholar 

  • Xu GB, Yu YT, Shen XB (2007) Studies of genetic diversity of dove trees (Davidia involucrate) in west Hunan and Hubei by RAPD. J Central South Univ For Technol 27:5–9 (in Chinese with English abstract)

    Google Scholar 

  • Ying TS (2001) Species diversity and distribution pattern of seed plants in China. Biodivers Sci 9:393–398 (in Chinese with English abstract)

    Google Scholar 

  • Ying TS, Zhang YL, Boufford DE (1993) The endemic genera of seed plants of China. Science Press, Beijing (in Chinese)

    Google Scholar 

  • Yu YF (1999) A milestone of wild plant conservation in China. Plants 5:3–11 (in Chinese)

    Google Scholar 

  • Zhan YY, Liu YH, Xiong WJ (2010) Current situation and prospect of endangered reason of Davidia involucrate Baill. Hubei For Sci Technol 161:41–56 (in Chinese with English abstract)

    Google Scholar 

  • Zhang YM (2012) The research on genetic diversity and molecular phylogenetic population of Davidia involucrata. Master Dissertation, Central South University of Forestry Technology, Changsha (in Chinese with English abstract)

  • Zhang RZ, Zheng D, Yang QY, Liu YH (1997) Physical geography of Hengduan Mountains. Science Press, Beijing (in Chinese)

    Google Scholar 

Download references

Acknowledgments

The authors thank Ling-Yun Chen, Xiao-Li Yue, and Dan Yang for their help in fieldwork, Zhi-Yuan Du and Dun Wang for their assistance in the laboratory, and Hans Peter Comes for his useful comments and suggestions on an earlier draft of the manuscript. This study was supported by grants from One Hundred Person Project of the Chinese Academy of Sciences granted to WQF (KSCX2-YW-Z-0805), the strategic pilot science and technology projects of the Chinese Academy of Sciences (Grant No. XDAO5090305), and the National Natural Science Foundation of China (No. 31270278).

Author information

Authors and Affiliations

  1. Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, China

    Jin-Ming Chen, Shu-Ying Zhao, Andrew Wanyoike Gichira & Qing-Feng Wang

  2. Fairy Lake Botanical Garden, Shenzhen, Chinese Academy of Sciences, Shenzhen, 518004, China

    Yi-Ying Liao

  3. Botany Department, Jomo Kenyatta University of Agriculture and Technology, P. O. Box 62000-00200, Nairobi, Kenya

    Robert Wahiti Gituru

Authors
  1. Jin-Ming Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu-Ying Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi-Ying Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrew Wanyoike Gichira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert Wahiti Gituru
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qing-Feng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qing-Feng Wang.

Additional information

Jin-Ming Chen and Shu-Ying Zhao contributed equally to this paper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 47 kb) Table S1 Chloroplast DNA non-coding regions studied and PCR primer sequence

10592_2014_683_MOESM2_ESM.docx

Supplementary material 2 (DOCX 18 kb) Table S2 Chloroplast DNA sequence polymorphism detected in six non-coding regions of Davidia involucrata identifying 13 haplotypes (H1-13). Dot (.) shows a site with the same nucleotide variant to that of the sequence of haplotype H1, “-” indicates alignment gap

10592_2014_683_MOESM3_ESM.doc

Supplementary material 3 (DOC 53 kb) Table S3 GenBank accession numbers for each of the six non-coding regions of each chloroplast haplotype (H1-13) identified in Davidia involucrata

10592_2014_683_MOESM4_ESM.doc

Supplementary material 4 (DOC 43 kb) Fig. S1 Distribution of the number of pairwise nucleotide differences for six non-coding regions sequence data in Davidia involucrata. a The whole species; b The WLS mountain region (HPG I); c The western region of Sichuan Basin (HPG II + III). The dash line represents observed value whereas the solid line shows expected values under a sudden (stepwise) population expansion

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, JM., Zhao, SY., Liao, YY. et al. Chloroplast DNA phylogeographic analysis reveals significant spatial genetic structure of the relictual tree Davidia involucrata (Davidiaceae). Conserv Genet 16, 583–593 (2015). https://doi.org/10.1007/s10592-014-0683-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0683-z

Keywords

Search

Navigation