Phylogeography of a rare orchid, Vexillabium yakushimense: comparison of populations in central Honshu and the Nansei Island chain, Japan

Abstract

Vexillabium yakushimense is a rare, terrestrial orchid which occurs in east and southeast Asia. In spite of its inconspicuous appearance, several new populations were discovered in central Honshu, Japan. Because these populations are geographically isolated at its northern range limit of distribution, they were suspected to have distinctive genetic characteristics. Given this hypothesis, we quantified the genetic variation of V. yakushimense for populations of central Honshu, and the Nansei Island chain, which represent the most southern locality in Japan. Leaves were collected from nine populations in central Honshu (n = 48) and two populations from the Nansei Island chain (n = 29). We examined genetic variation using cpDNA (1,205 bp) and ITS (511 bp) markers. Based on the cpDNA variation, a total of seven haplotypes were recovered; populations in central Honshu were clearly differentiated from those in the Nansei Island chain. Relatively high allelic richness and haplotype diversity were found in the pooled population of central Honshu. These populations likely maintained an adequate population size for a long period despite a markedly different ecological niche compared to that in the Nansei Island chain. In contrast to cpDNA, little variation was detected in ITS. Further studies on geographic occurrences, reproductive biology and mycorrhizal association are encouraged for its conservation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alexander C, Alexander IJ, Hadley G (1984) Phosphate-uptake by Goodyera repens in relation to mycorrhizal infection. New Phytol 97(3):401–411

    CAS  Article  Google Scholar 

  2. Arditti J, Ghani AKA (2000) Numerical and physical properties of orchid seeds and their biological implications. New Phytol 146(3):569

    Article  Google Scholar 

  3. Cameron DD, Leake JR, Read DJ (2006) Mutualistic mycorrhiza in orchids: evidence from plant–fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytol 171(2):405–416

    CAS  PubMed  Article  Google Scholar 

  4. Cribb PJ, Kell SP, Dixon KW, Barrett RL (2003) Orchid conservation: a global perspective. In: Dixon KW, Kell SP, Barrett RL, Cribb PJ (eds) Orchid conservation. Natural History Publications, Kota Kinabalu, pp 1–24

    Google Scholar 

  5. Dearnaley JDW (2007) Further advances in orchid mycorrhizal research. Mycorrhiza 17(6):475–486

    PubMed  Article  Google Scholar 

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

    Google Scholar 

  7. Dressler RL (1993) Phylogeny and classification of the orchid family. Dioscorides Press, Portland

    Google Scholar 

  8. Duffy KJ, Scopece G, Cozzolino S, Fay MF, Smith RJ, Stout JC (2009) Ecology and genetic diversity of the dense-flowered orchid, Neotinea maculata, at the centre and edge of its range. Ann Bot 104(3):507–516

    CAS  PubMed  Article  Google Scholar 

  9. Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17(5):1170–1188

    CAS  PubMed  Article  Google Scholar 

  10. Ehime Prefecture (2003) Red data book Ehime. Ehime Prefecture, Japan

  11. Ek RC, Ter Steege H, Biesmeijer KC (1997) Vertical distribution and association of vascular epiphytes in four different forest types in the Guianas. In: Ek RC (ed) Botanical diversity in the tropical rain forest of Guyana, Ph.D. thesis. Utrecht University, The Netherlands, pp 65–89

  12. El Mousadik A, Petit RJ (1996) Chloroplast DNA phylogeography of the argan tree of Morocco. Mol Ecol 5(4):547–555

    PubMed  Article  Google Scholar 

  13. 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(2):479–491

    CAS  PubMed  Google Scholar 

  14. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  15. Forrest AD, Hollingsworth ML, Hollingsworth PM, Sydes C, Bateman RM (2004) Population genetic structure in European populations of Spiranthes romanzoffiana set in the context of other genetic studies on orchids. Heredity 92(3):218–227

    Google Scholar 

  16. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    PubMed  Article  Google Scholar 

  17. GBIF (2012) Global Biodiversity Information Facility. Available via http://www.gbif.org/ Accessed 2012.8.1

  18. Gentry AH, Dodson CH (1987) Diversity and biogeography of neotropical vascular epiphytes. Ann Mo Bot Gard 74(2):205–233

    Article  Google Scholar 

  19. Gravendeel B, Smithson A, Slik FJ, Schuiteman A (2004) Epiphytism and pollinator specialization: drivers for orchid diversity? Philos Trans R Soc London Ser B Biol Sci 359(1450):1523–1535

    Article  Google Scholar 

  20. Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8(5):461–467

    PubMed  Article  Google Scholar 

  21. Hatsushima S (1971) Flora of the Ryukyus: including Amami islands, Okinawa islands, and Sakishima archipelago. Okinawa-seibutsu-kyouiku-kenkyuukai, Okinawa

    Google Scholar 

  22. Inoue K (1996) Present status and conservation of orchids in Japan. Jap J Conserv Ecol 1:115–129 (in Japanese with English abstract)

    Google Scholar 

  23. Ishikawa N, Yokoyama J, Ikeda H, Takabe E, Tsukaya H (2006) Evaluation of morphological and molecular variation in Plantago asiatica var. densiuscula, with special reference to the systematic treatment of Plantago asiatica var. yakusimensis. J Plant Res 119(4):385–395

    PubMed  Article  Google Scholar 

  24. Johansson DR (1974) Ecology of vascular epiphytes in West African rain forests. Acta Phytogeographica Suecica 59:1–136

    Google Scholar 

  25. Kew Royal Botanic Gardens (2013) World check list of selected plant families. Available via Kew Royal botanic Gardens. 2012. http://apps.kew.org/wcsp/advanced.do. Accessed January 22, 2013

  26. Kitazawa A (2009) Discovery of endangered plants in wetlands dominated by Acer pycnanthum. Bull Bot Soc Nagano 42:63–64

    Google Scholar 

  27. Kitazawa A (2010) Discovery of endangered plants in wetlands dominated by Acer pycnanthum No. 2. Bull Bot Soc Nagano 43:55–58

    Google Scholar 

  28. Kitazawa A (2011) Discovery of endangered plants in wetlands dominated by Acer pycnanthum No. 3. Bull Bot Soc Nagano 44:31–32

    Google Scholar 

  29. Kitazawa A (2012) Discovery of endangered plants in wetlands dominated by Acer pycnanthum No. 3. Bull Bot Soc Nagano 45:39–41

    Google Scholar 

  30. Kochi Prefecture (2009) Flora of Kochi. Kochi Prefecture, Japan

  31. Lawton JH (1993) Range, population abundance and conservation. Trends Ecol Evol 8(11):409–413

    CAS  PubMed  Article  Google Scholar 

  32. Lesica P, McCune B (2004) Decline of arctic-alpine plants at the southern margin of their range following a decade of climatic warming. J Veg Sci 15(5):679–690

    Article  Google Scholar 

  33. Mabberley DJ (1997) The plant book. A portable dictionary of the vascular plants. 2nd edn. Cambridge University Press, Cambridge

  34. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2):209–220

    CAS  PubMed  Google Scholar 

  35. Matsushima N (1995) Morphogenetic history of the Ina Basin. Research Report of the Iida City Museum 3:1–145

    Google Scholar 

  36. McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. MjM Software Design, Gleneden Beach

    Google Scholar 

  37. McLachlan JS, Clark JS, Manos PS (2005) Molecular indicators of tree migration capacity under rapid climate change. Ecology 86(8):2088–2098

    Article  Google Scholar 

  38. Micheneau C, Duffy KJ, Smith RJ, Stevens LJ, Stout JC, Civeyrel L, Cowan RS, Fay MF (2010) Plastid microsatellites for the study of genetic variability in the widespread Cephalanthera longifolia, C. damasonium and C. rubra (Neottieae, Orchidaceae), and cross-amplification in other Cephalanthera species. Bot J Linn Soc 163(2):181–193

    Article  Google Scholar 

  39. Ministry of Environment (2012) Red list of vascular plants in Japan. Available via Ministry of Environment. http://www.biodic.go.jp/rdb/rdb_f.html. Accessed Sept 30, 2012

  40. Nakajima M (2012) Illustrations of Japanese Orchids. Bun-ichi Sogo Shuppan Co., Tokyo

    Google Scholar 

  41. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  42. Nieder J (2004) Distribution patterns of epiphytic orchids—present research, past causes and future consequences. In: Hermans J, Cribb P (ed) The European Orchid Conference and Show, London, London, 2003. The British Orchid Council and the Royal Horticultural Society, London, pp 241–258

  43. Nishizawa T, Watano Y (2000) Primer pairs suitable for PCR-SSCP analysis of chloroplast DNA in angiosperms. J Phytogeog Taxon 48:63–66

    Google Scholar 

  44. Otero JT, Flanagan NS, Herre EA, Ackerman JD, Bayman P (2007) Widespread mycorrhizal specificity correlates to mycorrhizal function in the neotropical, epiphytic orchid Ionopsis utricularioides (Orchidaceae). Am J Bot 94(12):1944–1950

    PubMed  Article  Google Scholar 

  45. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295

    Article  Google Scholar 

  46. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12(4):844–855

    Article  Google Scholar 

  47. Pillon Y, Chase MW (2007) Taxonomic exaggeration and its effects on orchid conservation. Conserv Biol 21(1):263–265

    PubMed  Article  Google Scholar 

  48. Ramirez SR, Eltz T, Fujiwara MK, Gerlach G, Goldman-Huertas B, Tsutsui ND, Pierce NE (2011) Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333(6050):1742–1746

    CAS  PubMed  Article  Google Scholar 

  49. Roberts DL (2003) Pollination biology: the role of sexual reproduction in orchid conservation. In: Dixon KW, Kell SP, Barrett RL, Cribb PJ (eds) Orchid conservation. Natural History Publications, Kota Kinabalu

    Google Scholar 

  50. 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 

  51. Sagarin RD, Gaines SD (2002) The ‘abundant centre’ distribution: to what extent is it a biogeographical rule? Ecol Lett 5:137–147

    Article  Google Scholar 

  52. Sagarin RD, Gaines SD, Gaylord B (2006) Moving beyond assumptions to understand abundance distributions across the ranges of species. Trends Ecol Evol 21:524–530

    PubMed  Article  Google Scholar 

  53. Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am J Bot 84(8):1120–1136

    CAS  PubMed  Article  Google Scholar 

  54. Satake Y, Ohwi J, Kitamura S, Watari S, Tominari T (1985) Wild flowers of Japan, herbs. Heibonsha, Tokyo

    Google Scholar 

  55. Search System of Japanese Red Data (2012) Search System of Japanese Red Data. Available via http://jpnrdb.com/index.html. Accessed 1 Aug 2012 (in Japanese)

  56. Shimizu T (1997) Flora of Nagano prefecture. Shinano Mainichi Shinbun, Nagano

    Google Scholar 

  57. Stone JL, Crystal PA, Devlin EE, Downer RH, Cameron DS (2012) Highest genetic diversity at the northern range limit of the rare orchid Isotria medeoloides. Heredity 109:215–221

    CAS  PubMed  Article  Google Scholar 

  58. Suetsugu K, Honda T (2012) New record of Vexillabium yakushimense from Kinki district. Bunrui 12(1):59–61

    Google Scholar 

  59. Swarts ND, Dixon KW (2009a) Perspectives on orchid conservation in botanic gardens. Trends Plant Sci 14(11):590–598

    CAS  PubMed  Article  Google Scholar 

  60. Swarts ND, Dixon KW (2009b) Terrestrial orchid conservation in the age of extinction. Ann Bot 104(3):543–556

    PubMed  Article  Google Scholar 

  61. Takahashi S, Furukawa T, Asano T, Terajima Y, Shimada H, Sugimoto A, Kadowaki K (2005) Very close relationship of the chloroplast genomes among Saccharum species. Theor Appl Genet 110(8):1523–1529

    CAS  PubMed  Article  Google Scholar 

  62. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    CAS  PubMed  Article  Google Scholar 

  63. Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. Syst Bot 28(4):723–737

    Google Scholar 

  64. Taylor DL, Bruns TD, Szaro TM, Hodges SA (2003) Divergence in mycorrhizal specialization within Hexalectris spicata (Orchidaceae), a nonphotosynthetic desert orchid. Am J Bot 90(8):1168–1179

    CAS  PubMed  Article  Google Scholar 

  65. The Environment Agency (2000) Threatened Wildlife of Japan, Red Data Book, Vascular Plants, vol 8. 2nd edn. Japan Wildlife Research Center, Tokyo

  66. Tomaru N, Takahashi M, Tsumura Y, Uchida K, Ohba K (1997) Genetic diversity in Fagus crenata (Japanese beech): influence of the distributional shift during the late-quaternary. Heredity 78(3):241–251

    Article  Google Scholar 

  67. Tremblay RL (1992) Trends in the pollination ecology of the Orchidaceae—evolution and systematics. Can J Bot 70(3):642–650

    Article  Google Scholar 

  68. Ueda K (1989) Phytogeography of Tokai hilly land element I. Definition. Acta Phytotaxonomica Geobotanica 40:190–202

    Google Scholar 

  69. Ueda K (1994) The origin and evolution of the Tokai hilly land element. In: Okada H, Ueda K, Kadono Y (eds) Natural history of plants: evolutionary studies of diversity. Hokkaido University Press, Sapporo, pp 3–18

    Google Scholar 

  70. Urbatsch LE, Baldwin BG, Donoghue MJ (2000) Phylogeny of the coneflowers and relatives (Heliantheae: Asteraceae) based on nuclear rDNA internal transcribed spacer (ITS) sequences and chloroplast DNA restriction site data. Syst Bot 25(3):539–565

    Article  Google Scholar 

  71. Vucetich JA, Waite TA (2003) Spatial patterns of demography and genetic processes across the species’ range: null hypotheses for landscape conservation genetics. Conserv Genet 4(5):639–645

    Article  Google Scholar 

  72. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  73. 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(24):9054–9058

    CAS  PubMed  Article  Google Scholar 

  74. Yamamoto Y (1924) Eine neue Art von Anoectochilus. Bot Mag 38:131–133

    Google Scholar 

  75. Yoder JA, Zettler LW, Stewart SL (2000) Water requirements of terrestrial and epiphytic orchid seeds and seedlings, and evidence for water uptake by means of mycotrophy. Plant Sci 156(2):145–150

    CAS  PubMed  Article  Google Scholar 

  76. Yonekura K (2012) An enumeration of the vascular plants of Japan. Hokuryukan, Tokyo

    Google Scholar 

Download references

Acknowledgments

We sincerely thank Mr. T. Watanabe, Mr. A. Tono, Mr. S. Yamaguchi, Mrs. Y. Yamaguchi, Mr. K. Watanabe and Makino Herbarium (Dr. N. Murakami, Dr. T. Sugawara, Dr. H. Kato) for their support in field collection, examination of herbarium specimens and DNA analyses. Comments on an early draft by Dr. B.V. Barnes (Professor Emeritus of the University of Michigan) were very helpful. Two refrees provided useful suggestions. This research was funded by the Yokohama National University-National Environment Research Institute Global COE program from April 2010 to March 2012 and the Pro Natura Fund from October 2011 to September 2012.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ikuyo Saeki.

Appendix 1

Appendix 1

See Table 3.

Table 3 GenBank accession numbers of sequenced individuals of Vexillabium yakushimense

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Saeki, I., Kitazawa, A., Abe, A. et al. Phylogeography of a rare orchid, Vexillabium yakushimense: comparison of populations in central Honshu and the Nansei Island chain, Japan. Plant Syst Evol 300, 1–12 (2014). https://doi.org/10.1007/s00606-013-0854-2

Download citation

Keywords

  • Biogeography
  • Chloroplast DNA
  • Disjunct distribution
  • Endangered species
  • Genetic diversity