Skip to main content

Advertisement

SpringerLink
Log in

Conservation genetics of rare trees restricted to subtropical montane cloud forests in southern China: a case study from Quercus arbutifolia (Fagaceae)

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Montane cloud forests (MCFs), with their isolated nature, offer excellent opportunities to study the long-term effects of habitat fragmentation and the impacts of climate change. Quercus arbutifolia is a rare oak in MCFs of southern China and Vietnam. Its isolated populations, small population size and unique ecological niche make this species vulnerable to climate change and habitat loss. In this study, we used chloroplast (cpDNA) and nuclear (ITS) DNA sequences to investigate genetic divergence patterns and demographic history of five of the six known populations of Q. arbutifolia. Considering its small population size and fragmentation, Q. arbutifolia has unexpectedly high genetic diversity. The time since the most recent common ancestor of all cpDNA haplotypes was c. 10.25 Ma, and the rapid diversification of haplotypes occurred during the Quaternary. The maximum clade credibility chronogram of cpDNA haplotypes suggests that the DM population (Daming Mountain, Guangxi province) diverged early and rapidly became isolated from other populations. The Pearl River drainage system may have been the main geographic barrier between DM and other populations since the late Miocene. ITS data suggests that population expansion occurred during the last interglacial of the Quaternary. The combined effects of pre-Quaternary and Quaternary climatic and geological changes were the main drivers to the current genetic diversity and distribution pattern of Q. arbutifolia. Because of the high between-population genetic differentiation and high within-population genetic diversity of Q. arbutifolia, conservation efforts should be implemented for all populations, but if conservation resources are limited, populations DM, YZ (Mang Mountain, Hunan province) and ZZ (Daqin Mountain, Fujian province) should have priority.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 411:62–66

  • An ZS, Huang YS, Liu WG, Guo ZT, Clemens S, Li L, Prell W, 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 33:705–708. doi:10.1130/g21423.1

    Article  Google Scholar 

  • Anderson RS, Ashe JS (2000) Leaf litter inhabiting beetles as surrogates for establishing priorities for conservation of selected tropical montane cloud forests in Honduras, central America (Coleoptera; Staphylinidae, Curculionidae). Biodivers Conserv 9:617–653. doi:10.1023/a:1008937017058

  • Anderson RP, Gutierrez EE, Ochoa-G J, Garcia FJ, Aguilera M (2012) Faunal nestedness and species-area relationship for small non-volant mammals in "sky islands" of northern Venezuela. Stud Neotropical Fauna Environ 47:157–170. doi:10.1080/01650521.2012.745295

    Article  Google Scholar 

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

    Google Scholar 

  • Axelrod DI, Al-Shehbaz I, Raven PH (1996) History of the modern flora of China. In: Zhang AL, SG W (eds) Floristic characteristics and diversity of East Asian plants: proceedings of the first international symposium of floristic characteristics and diversity of East Asian plants. Springer Verlag and China Higher Education Press, Berlin and Beijing, pp. 43–55

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Barbara T, Martinelli G, Fay MF, Mayo SJ, Lexer C (2007) Population differentiation and species cohesion in two closely related plants adapted to neotropical high-altitude ‘inselbergs’, Alcantarea imperialis and Alcantarea geniculata (Bromeliaceae). Mol Ecol 16:1981–1992. doi:10.1111/j.1365-294X.2007.03272.x

    Article  CAS  PubMed  Google Scholar 

  • Barbara T, Lexer C, Martinelli G, Mayo S, Fay MF, Heuertz M (2008) Within-population spatial genetic structure in four naturally fragmented species of a neotropical inselberg radiation, Alcantarea imperialis, A. geniculata, A. glaziouana and A. regina (Bromeliaceae). Heredity 101:285–296. doi:10.1038/hdy.2008.65

    Article  CAS  PubMed  Google Scholar 

  • Bellarosa R, Simeone MC, Papini A, Schirone B (2005) Utility of ITS sequence data for phylogenetic reconstruction of Italian Quercus spp. Mol Phylogenet Evol 34:355–370. doi:10.1016/j.ympev.2004.10.014

    Article  CAS  PubMed  Google Scholar 

  • Bradford J, Jaffre T (2004) Plant species microendemism and conservation of montane maquis in New Caledonia: two new species of Pancheria (Cunoniaceae) from the Roche Ouaieme. Biodivers Conserv 13:2253–2273. doi:10.1023/B:BIOC.0000047901.33761.3c

    Article  Google Scholar 

  • Browne RA, Ferree PM (2007) Genetic structure of southern Appalachian “sky island” populations of the southern red-backed vole (Myodes gapperi). J Mammal 88:759–768

    Article  Google Scholar 

  • Carstens BC, Knowles LL (2007) Shifting distributions and speciation: species divergence during rapid climate change. Mol Ecol 16:619–627. doi:10.1111/j.1365-294X.2006.03167.x

    Article  PubMed  Google Scholar 

  • Cayuela L, Golicher DJ, Rey-Benayas JM (2006) The extent, distribution, and fragmentation of vanishing montane cloud forest in the highlands of Chiapas, Mexico. Biotropica 38:544–554. doi:10.1111/j.1744-7429.2006.00160.x

    Article  Google Scholar 

  • Chen DM, Zhang XX, Kang HZ, Sun X, Yin S, Du HM, Yamanaka N, Gapare W, Wu HX, Liu CJ (2012) Phylogeography of Quercus variabilis based on chloroplast DNA sequence in East Asia: multiple glacial refugia and mainland-migrated island populations. PLoS ONE 7:e47268. doi:10.1371/journal.pone.0047268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu HS, Chang SC, Klemm O, Lai CW, Lin YZ, Wu CC, Lin JY, Jiang JY, Chen JQ, Gottgens JF, Hsia YJ (2014) Does canopy wetness matter? Evapotranspiration from a subtropical montane cloud forest in Taiwan. Hydrol Process 28:1190–1214. doi:10.1002/hyp.9662

    Article  Google Scholar 

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843

    Article  PubMed  Google Scholar 

  • Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129

    Article  Google Scholar 

  • Corrander J, Marttinen P, Mäntyniemi S (2006) A Bayesian method for identification of stock mixtures from molecular marker data. Fish Bull 104:550–558

    Google Scholar 

  • Crepet WL, Nixon KC (1989) Extinct transitional Fagaceae from the Oligocene and their phylogenetic implications. Am J Bot 76:1493–1505

    Article  Google Scholar 

  • Cruz-Cardenas G, Luis Villasenor J, Lopez-Mata L, Ortiz E (2012) Potential distribution of humid mountain forest in Mexico. Bot Sci 90:331–340

    Article  Google Scholar 

  • DeChaine EG, Martin AP (2004) Historic cycles of fragmentation and expansion in Parnassius smintheus (Papilionidae) inferred using mitochondrial DNA. Evolution 58:113–127. doi:10.1111/j.0014-3820.2004.tb01578.x

    Article  PubMed  Google Scholar 

  • DeChaine EG, Martin AP (2005) Marked genetic divergence among sky island populations of Sedum lanceolatum (Crassulaceae) in the rocky mountains. Am J Bot 92:477–486. doi:10.3732/ajb.92.3.477

    Article  CAS  PubMed  Google Scholar 

  • Deng M, Cao M, Xi SL, Cao XY (2011a) Quercus arbutifolia, a new record species of Fagaceae in Guangxi. Guihaia 31:575–577

    Google Scholar 

  • Deng M, Coombes A, Li QS (2011b) Lectotypification of Quercus arbutifolia (Fagaceae) and the taxonomic treatment of Quercus subsect. Chrysotrichae. Nord J Bot 29:208–214

    Article  Google Scholar 

  • Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Fan ZX, Liu SY, Liu Y, Liao LH, Zhang XY, Yue BS (2012) Phylogeography of the South China field mouse (Apodemus draco) on the southeastern Tibetan Plateau reveals high genetic diversity and glacial refugia. PLoS ONE 7. doi:10.1371/journal.pone.0038184

  • Fan DM, Yue JP, Nie ZL, Li ZM, Comes HP, Sun H (2013) Phylogeography of Sophora davidii (Leguminosae) across the ‘Tanaka-Kaiyong Line’, an important phytogeographic boundary in southwest China. Mol Ecol 22:4270–4288

  • Foster P (2001) The potential negative impacts of global climate change on tropical montane cloud forests. Earth-Sci Rev 55:73–106. doi:10.1016/s0012-8252(01)00056-3

    Article  Google Scholar 

  • Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Frascaria N, Maggia L, Michaud M, Bousquet J (1993) The rbcL gene sequence from chestnut indicates a slow rate of evolution in the Fagaceae. Genome 36:668–671. doi:10.1139/g93-089

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao LM, Moeller 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. doi:10.1111/j.1365-294X.2007.03537.x

    Article  CAS  PubMed  Google Scholar 

  • Graur D, Li WH (2000) Fundamentals of molecular evolution, 2nd edn. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Grivet D, Heinze B, Vendramin GG, Petit RJ (2001) Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes 1:345–349. doi:10.1046/j.1471-8278.2001.00107.x

    Article  CAS  Google Scholar 

  • Guo ZT, Ruddiman WF, Hao QZ, Wu HB, Qiao YS, Zhu RX, Peng SZ, Wei JJ, Yuan BY, Liu TS (2002) Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature 416:159–163. doi:10.1038/416159a

    Article  CAS  PubMed  Google Scholar 

  • Harpending H (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 (Communications arising): diversity of temperate plants in East Asia. Nature 413:129–130

    Article  CAS  PubMed  Google Scholar 

  • He K, Jiang X (2014) Sky islands of southwest China. I: an overview of phylogeographic patterns. Chin Sci Bull 59:585–597

    Article  Google Scholar 

  • Hedrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding, and genetic resources. Sinauer Associates, Sunderland

    Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Huang CC, Zhang YT, Bartholomew B (1999) Fagaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 4. Science Press and Missouri Botanical Garden Press, Beijing and St. Louis, pp. 314–400

    Google Scholar 

  • Huang SSF, Hwang SY, Lin TP (2002) Spatial pattern of chloroplast DNA variation of Cyclobalanopsis glauca in Taiwan and East Asia. Mol Ecol 11:2349–2358. doi:10.1046/j.1365-294X.2002.01624.x

    Article  CAS  PubMed  Google Scholar 

  • Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci USA 103:10334–10339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914. doi:10.2307/2640449

    Article  Google Scholar 

  • IUCN (2011) IUCN Red list categories and criteria, Version 3.1. IUCN Species survival commission, Gland and Gambridge

  • Kay KM, Whittall JB, Hodges SA (2006) A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol 6:36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Knowles LL (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshopprers. Mol Ecol 10:691–701

    Article  CAS  PubMed  Google Scholar 

  • Kvacek Z, Teodoridis V (2007) Tertiary macrofloras of the Bohemian Massif: a review with correlations within Boreal and Central Europe. Bull Geosci 82:383–408

  • Li FJ, Rousseau D-D, Wu NQ, Hao QZ, Pei YP (2008) Late Neogene evolution of the East Asian monsoon revealed by terrestrial mollusk record in western Chinese Loess Plateau: from winter to summer dominated sub-regime. Earth Planet Sci Lett 274:439–447

  • Liao PC, Havanond S, Huang S (2007) Phylogeography of Ceriops tagal (Rhizophoraceae) in southeast Asia: the land barrier of the Malay Peninsula has caused population differentiation between the Indian Ocean and South China Sea. Conserv Genet 8:89–98

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu HZ, Takeichi Y, Kamiya K, Harada K (2012a) Phylogeography of Quercus phillyraeoides (Fagaceae) in Japan as revealed by chloroplast DNA variation. J For Res 18(4):361–370. doi:10.1007/s10310-012-0357-y

    Article  CAS  Google Scholar 

  • Liu JQ, Sun YS, Ge XJ, Gao LM, Qiu YX (2012b) Phylogeographic studies of plants in China: advances in the past and directions in the future. J Syst Evol 50:267–275. doi:10.1111/j.1759-6831.2012.00214.x

    Article  Google Scholar 

  • Liu Q, Chen P, He K, Kilpatrick CW, Liu SY, Yu FH, Jiang XL (2012c) Phylogeographic study of Apodemus ilex (Rodentia: Muridae) in southwest China. PLoS ONE 7:e31453. doi:10.1371/journal.pone.0031453

  • Lu HY, Yi SW, Liu ZY, Mason JA, Jiang DB, Cheng J, Stevens T, Xu ZW, Zhang EL, Jin LY (2013) Variation of East Asian monsoon precipitation during the past 21 ky and potential CO2 forcing. Geology 41:1023–1026

    Article  CAS  Google Scholar 

  • Lu ZQ, Chen P, Bai XT, Xu JM, He XD, Niu ZM, Wan DS (2015) Initial diversification, glacial survival, and continuous range expansion of Gentiana straminea (Gentianaceae) in the Qinghai–Tibet Plateau. Biochem Syst Ecol 62:219–228. doi:10.1016/j.bse.2015.09.005

    Article  CAS  Google Scholar 

  • Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563

    Article  CAS  PubMed  Google Scholar 

  • Masta SE (2000) Phylogeography of the jumping spider Habronattus pugillis (Araneae: Salticidae): recent vicariance of sky island populations? Evolution 54:1699–1711

    Article  CAS  PubMed  Google Scholar 

  • Matthews SD, Meehan LJ, Onyabe DY, Vineis J, Nock I, Ndams I, Conn JE (2007) Evidence for late Pleistocene population expansion of the malarial mosquitoes, Anopheles arabiensis and Anopheles gambiae in Nigeria. Med Vet Entomol 21:358–369

    Article  CAS  PubMed  Google Scholar 

  • McCormack JE, Bowen BS, Smith TB (2008) Integrating paleoecology and genetics of bird populations in two sky island archipelagos. BMC Biol 6. doi:10.1186/1741-7007-6-28

  • McCormack JE, Huang H, Knowles LL (2009) Sky islands. In: Gillespie RG, Clague DA (eds) Encyclopedia of islands. University of California Press, Berkeley, CA, pp. 841–843

    Google 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 112:155–172

  • Morris AB, Graham CH, Soltis DE, Soltis PS (2010) Reassessment of phylogeographical structure in an eastern North American tree using Monmonier’s algorithm and ecological niche modelling. J Biogeogr 37:1657–1667

    Article  Google Scholar 

  • Ojeda AA (2010) Phylogeography and genetic variation in the South American rodent Tympanoctomys barrerae (Rodentia: Octodontidae). J Mammal 91:302–313. doi:10.1644/09-MAMM-A-177.1

    Article  Google Scholar 

  • Oliveira RS, Eller CB, Bittencourt PRL, Mulligan M (2014) The hydroclimatic and ecophysiological basis of cloud forest distributions under current and projected climates. Ann Bot 113:909–920. doi:10.1093/aob/mcu060

    Article  PubMed  PubMed Central  Google Scholar 

  • Otto-Bliesner BL, Marshall SJ, Overpeck JT, Miller GH, Hu A, members CLIP (2006) Simulating Arctic climate warmth and Icefield retreat in the last interglaciation. Science 311:1751–1753. doi:10.1126/science.1120808

    Article  CAS  PubMed  Google Scholar 

  • Patterson BD, Stotz DF, Solari S, Fitzpatrick JW, Pacheco V (1998) Contrasting patterns of elevational zonation for birds and mammals in the Andes of southeastern Peru. J Biogeogr 25:593–607. doi:10.1046/j.1365-2699.1998.2530593.x

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2003) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pons J, Pausas JG (2007) Not only size matters: acorn selection by the European jay (Garrulus glandarius). Acta Oecol 31:353–360. doi:10.1016/j.actao.2007.01.004

    Article  Google Scholar 

  • Pons O, Petit R (1996) Measwring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Porembski S, Barthlott W (2000) Inselbergs. Biotic diversity of isolated rock outcrops in tropical and temperate regions. Springer-Verlag, Berlin, Heidelberg, New York

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  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 modelling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphyllum (Cercidiphyllaceae). New Phytol 196:617–630

  • Qiu YX, Luo YP, Comes HP, Ouyang ZQ, Fu CX (2007) Population genetic diversity and structure of Dipteronia dyerana (Sapindaceae), a rare endemic from Yunnan province, China, with implications for conservation. Taxon 56:427–437

    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

  • Ramos-Palacios CR, Badano EI, Flores J, Flores-Cano JA, Flores-Flores JL (2014) Distribution patterns of acorns after primary dispersion in a fragmented oak forest and their consequences on predators and dispersers. Eur J For Res 133:391–404. doi:10.1007/s10342-013-0771-5

    Article  Google Scholar 

  • Robin VV, Sinha A, Ramakrishnan U (2010) Ancient geographical gaps and paleo-climate shape the phylogeography of an endemic bird in the sky islands of southern India. PLoS ONE 5:e13321. doi:10.1371/journal.pone.0013321

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Sauquet H, Ho SY, Gandolfo MA, Jordan GJ, Wilf P, Cantrill DJ, Bayly MJ, Bromham L, Brown GK, Carpenter RJ (2012) Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales). Syst Biol 61:289–313

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555

    Article  PubMed  CAS  Google Scholar 

  • Scofield DG, Sork VL, Smouse PE (2010) Influence of acorn woodpecker social behaviour on transport of coast live oak (Quercus agrifolia) acorns in a southern California oak savanna. J Ecol 98:561–572. doi:10.1111/j.1365-2745.2010.01649.x

    Article  Google Scholar 

  • Scofield DG, Alfaro VR, Sork VL, Grivet D, Martinez E, Papp J, Pluess AR, Koenig WD, Smouse PE (2011) Foraging patterns of acorn woodpeckers (Melanerpes formicivorus) on valley oak (Quercus lobata Née) in two California oak savanna-woodlands. Oecologia 166:187–196. doi:10.1007/s00442-010-1828-5

    Article  PubMed  Google Scholar 

  • Shao L, Pang X, Qiao PJ, Chen CM, Li QY, Miao WL (2008) Sedimentary filling of the Pear River Mouth Basin response to the evolution of the Pear River. Acta Sedment Sin 26:179–185

    CAS  Google Scholar 

  • Shi MM, Michalski SG, Welk E, Chen XY, Durka W (2014) Phylogeography of a widespread Asian subtropical tree: genetic east-west differentiation and climate envelope modelling suggest multiple glacial refugia. J Biogeogr 41:1710–1720. doi:10.1111/jbi.12322

    Article  Google Scholar 

  • Simeone MC, Piredda R, Papini A, Vessella F, Schirone B (2013) Application of plastid and nuclear markers to DNA barcoding of Euro-Mediterranean oaks (Quercus, Fagaceae): problems, prospects and phylogenetic implications. Bot J Linn Soc 172:478–499

    Article  Google Scholar 

  • Simeone MC, Grimm GW, Papini A, Vessella F, Cardoni S, Tordoni E, Piredda R, Franc A, Denk T (2016) Plastome data reveal multiple geographic origins of Quercus Group Ilex. PeerJ 4:e1897. doi:10.7717/peerj.1897

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Small RL, Ryburn JA, Cronn RC, Seelanan T, Wendel JF (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear Adh sequences for phylogeny reconstruction in a recently diverged plant group. Am J Bot 85:1301–1315

    Article  CAS  PubMed  Google Scholar 

  • Smith CI, Farrell BD (2005) Phylogeography of the longhorn cactus beetle Moneilema appressum LeConte (Coleoptera: Cerambycidae): was the differentiation of the Madrean sky islands driven by Pleistocene climate changes? Mol Ecol 14:3049–3065

    Article  CAS  PubMed  Google Scholar 

  • Song SY, Krajewska K, Wang YF (2000) The first occurrence of the Quercus section Cerris Spach fruits in the Miocene of China. Acta Palaeobotanica 40:153–163

    Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264

  • Steele MA, Turner G, Smallwood PD, Wolff JO, Radillo J (2001) Cache management by small mammals: experimental evidence for the significance of acorn-embryo excision. J Mammal 82:35–42. doi:10.1644/1545-1542(2001)082<0035:cmbsme>2.0.co;2

    Article  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Still CJ, Foster PN, Schneider SH (1999) Simulating the effects of climate change on tropical montane cloud forests. Nature 398:608–610

    Article  CAS  Google Scholar 

  • Sullivan RM (1994) Micro-evolutionary differentiation and biogeographic structure among coniferous forest populations of the Mexican woodrat (Neotoma mexicana) in the American southwest: a test of the vicariance hypothesis. J Biogeogr 21:369–389. doi:10.2307/2845756

  • Sun XJ, Chen YS (1991) Palynological records of the last 11,000 years in China. Quat Sci Rev 10:537–544. doi:10.1016/0277-3791(91)90047-X

    Article  Google Scholar 

  • Sun Y, Hu HQ, Huang HW, Vargas-Mendoza CF (2014a) Chloroplast diversity and population differentiation of Castanopsis fargesii (Fagaceae): a dominant tree species in evergreen broad-leaved forest of subtropical China. Tree Genet Genomes 10:1531–1539. doi:10.1007/s11295-014-0776-3

    Article  Google Scholar 

  • Sun YX, Moore MJ, Yue LL, Feng T, Chu HJ, Chen ST, Ji YH, Wang HC, Li JQ (2014b) Chloroplast phylogeography of the East Asian Arcto-Tertiary relict Tetracentron sinense (Trochodendraceae). J Biogeogr 41:1721–1732. doi:10.1111/jbi.12323

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (and other methods). Version 4.0 b10. Sinauer Associates, Sunderland

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi K, Sato K, Washitani I (2006) The role of the wood mouse in Quercus serrata acorn dispersal in abandoned cut-over land. For Ecol Manag 229:120–127. doi:10.1016/j.foreco.2006.03.015

    Article  Google Scholar 

  • Tang ZH, Ding ZL, White PD, Dong XX, Ji JL, Jiang HC, Luo P, Wang X (2011) Late Cenozoic central Asian drying inferred from a palynological record from the northern Tian Shan. Earth Planet Sci Lett 302:439–447

    Article  CAS  Google Scholar 

  • Teixeira S, Cambon-Bonavita MA, Serrão EA, Desbruyeres D, Arnaud-Haond S (2011) Recent population expansion and connectivity in the hydrothermal shrimp Rimicaris exoculata along the Mid-Atlantic ridge. J Biogeogr 38:564–574

  • Terachi T (1993) Structural alterations of chloroplast genome and their significance to the higher plant evolution. Bull Inst Natl Land Util Developm Kyoto Sangyo Univ 14:138–148

    Google Scholar 

  • van de Weg MJ, Meir P, Williams M, Girardin C, Malhi Y, Silva-Espejo J, Grace J (2014) Gross primary productivity of a high elevation tropical montane cloud forest. Ecosystems 17:751–764. doi:10.1007/s10021-014-9758-4

    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. doi:10.1111/j.1365-2699.2009.02165.x

    Article  Google Scholar 

  • Wang YH, Jiang WM, Comes HP, Hu FS, Qiu YX, Fu CX (2015) Molecular phylogeography and ecological niche modelling of a widespread herbaceous climber, Tetrastigma hemsleyanum (Vitaceae): insights into Plio-Pleistocene range dynamics of evergreen forest in subtropical China. New Phytol 206:852–867. doi:10.1111/nph.13261

    Article  PubMed  Google Scholar 

  • Wright S (1949) The genetical structure of populations. Ann Eugenics 15:323–354

    Article  Google Scholar 

  • Wu ZY (1980) China’s vegetation. Science Press, Beijing

    Google Scholar 

  • Wu LL, Cui XK, Milne RI, 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. doi:10.1111/j.1365-294X.2010.04613.x

  • Xiao ZS, Zhang ZB, Wang YS (2005) Effects of seed size on dispersal distance in five rodent-dispersed fagaceous species. Acta Oecol 28:221–229

    Article  Google Scholar 

  • Xu J, Deng M, Jiang XL, Westwood M, Song YG, Turkington R (2015) Phylogeography of Quercus glauca (Fagaceae), a dominant tree of East Asian subtropical evergreen forests, based on three chloroplast DNA interspace sequences. Tree Genet Genomes 11:805. doi:10.1007/s11295-014-0805-2

  • Yan HF, Zhang CY, Wang FY, Hu CM, Ge XJ, Hao G (2012) Population expanding with the phalanx model and lineages split by environmental heterogeneity: a case study of Primula obconica in subtropical China. PLoS ONE 7:e41315. doi:10.1371/journal.pone.0041315

  • Yao YF, Bruch AA, Mosbrugger V, Li CS (2011) Quantitative reconstruction of Miocene climate patterns and evolution in southern China based on plant fossils. Palaeogeogr Palaeoclimatol Palaeoecol 304:291–307

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

  • Yu GH, Zhang MW, Rao DQ, Yang JX (2013) Effect of Pleistocene climatic oscillations on the phylogeography and demography of red knobby newt (Tylototriton shanjing) from southwestern China. PLoS ONE 8. doi:10.1371/journal.pone.0056066

  • Zhang TS, Li K, Wang Q, Cai YL, Yang K, Chen LQ (2006) Seed predation and dispersal of Castanopsis fargesii by rodents in Tiantong Mountain, Zhejiang province. Chin J Ecol 25:161–165

  • Zhang ZY, Wu R, Wang Q, Zhang ZR, López-Pujol J, Fan DM, Li DZ (2013) Comparative phylogeography of two sympatric beeches in subtropical China: species-specific geographic mosaic of lineages. Ecol Evol 3:4461–4472. doi:10.1002/ece3.829

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao YY, Zhang YH, Li XC (2013) Molecular phylogeography and population genetic structure of an endangered species Pachyhynobius shangchengensis (hynobiid Salamander) in a fragmented habitat of southeastern China. PLoS ONE 8:e78064. doi:10.1371/journal.pone.0078064

  • Zheng YQ, Yu G, Wang SM, Xue B, Liu HQ, Zeng XM (2003) Simulations of LGM climate of East Asia by regional climate model. Sci China Ser D 46:753–764. doi:10.1007/bf02879520

    Article  Google Scholar 

  • Zhou Y, Qiu G, Guo D (1991) Changes of permafrost in China during Quaternary. In: Liu TS (ed) Quaternary geology and environment in China. Science Press, Beijing, pp. 86–94

    Google Scholar 

Download references

Acknowledgments

We thank the two anonymous reviewers for their insightful and valuable suggestions and comments for improving the manuscript. We also thank the editors and two anonymous reviewers of Axios Review for their help and suggestions on improving the manuscript. We are grateful to Mr. Allen Coombes (Benemerita Universidad Autónoma de Puebla) for helping in revising the early draft of the manuscript. This work was supported by grants from the National Natural Science Foundation of China (31500539, 31270267), the Shanghai Municipal Administration of Forestation and City Appearances (F132418, G142430, G142424), and Science and Technology Commission of Shanghai Municipality (14DZ2260400).

Author contributions

Conceived and designed the experiments: MD. Performed the experiments: JX, SSZ. Analyzed the data: JX, XLJ. Collected samples: MD, YGS, SSZ. Revised manuscript: JX, MD, MW. Wrote the paper: JX, XLJ, MD.

Data archiving statement

Sequence data obtained in this study has been submitted to Genebank (http://www.ncbi.nlm.nih.gov/genbank/). DNA sequences Genbank accessions for the different haplotypes sequenced are KM210618-KM210622 and KU312127-KU312189; Genbank accession numbers for each taxon sampled are listed in Table S2 (Supplementary material).

Author information

Authors and Affiliations

  1. Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai, 201602, China

    Jin Xu, Xiao-Long Jiang, Min Deng, Yi-Gang Song & Si-Si Zheng

  2. Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai, 201602, China

    Jin Xu, Xiao-Long Jiang, Min Deng, Yi-Gang Song & Si-Si Zheng

  3. The Morton Arboretum, 4100 Illinois Route 53, Lisle, IL, 60532-1293, USA

    Murphy Westwood

Authors
  1. Jin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-Long Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Murphy Westwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yi-Gang Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Si-Si Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Min Deng.

Additional information

Communicated by A. Kremer

Jin Xu and Xiao-Long Jiang contributed equally to this work

Electronic supplementary material

ESM 1

(DOCX 17 kb)

ESM 2

(DOCX 17 kb)

ESM 3

(DOCX 16 kb)

ESM 4

(DOCX 27 kb)

ESM 5

(DOCX 23 kb)

ESM 6

(DOCX 17 kb)

ESM 7

(DOCX 18 kb)

Fig. S1

The geographical distribution of the six known sites (populations) of Q. arbutifolia. Red dots represents the locations (GIF 995 kb)

High resolution image (TIFF 26381 kb)

Fig. S2

Results of Bayesian cluster analysis with BAPS for K = 4 based on (a) cpDNA data and (b) ITS data. Each individual is represented by a thin vertical line. Black line separate the 5 investigated populations of Q. arbutifolia (see Table 1 for population names) (GIF 2556 kb)

High resolution image (TIFF 25733 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, J., Jiang, XL., Deng, M. et al. Conservation genetics of rare trees restricted to subtropical montane cloud forests in southern China: a case study from Quercus arbutifolia (Fagaceae). Tree Genetics & Genomes 12, 90 (2016). https://doi.org/10.1007/s11295-016-1048-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-016-1048-1

Keywords

Search

Navigation