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Patterns of Genetic Diversity in Rare and Common Orchids Focusing on the Korean Peninsula: Implications for Conservation

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Abstract

To provide basic information for orchid conservation, we surveyed the plant allozyme literature to summarize genetic diversity and structure data for (i) rare orchids native to the Korean Peninsula, and (ii) their congeners irrespective of being common and rare or Korean or not. A total of 68 taxa (32 taxa in Korea and 37 outside Korea; Goodyera repens being included in both datasets) were considered in this study. Overall, rare Korean orchid species had significantly lower levels of genetic diversity than their common congeners and common orchids in general at both population and species levels. However, mean values of G ST (or F ST) for rare and common orchids (Korean or not) did not differ significantly from each other. We found patterns of both low and high genetic diversity in rare Korean orchids. Many rare orchids harbored a complete lack of allozyme variation or extremely low within-population variation, perhaps due to rarity associated with random genetic drift and/or, for the case of warm-temperate orchids, to founder effects during post-glacial re-colonization. In contrast, high levels of genetic variation were found for a few orchids that have become recently rare (due to over-collection during the past several decades), probably because there have not been sufficient generations for the initial diversity to be substantially eroded. In addition, several orchids occurring in the main mountain system of the Korean Peninsula (the Baekdudaegan), that served as a glacial refugium, maintained moderate to high levels of within-population genetic diversity. Based on our genetic data, conservation priority should be given to rare orchid species. Particularly, urgent measures should be implemented on Jeju Island, a popular vacation spot, because it also a hotspot for threatened orchids with low levels of genetic diversity.

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Literature Cited

  • Aagaard, J. E., R. J. Harrod & K. L. Shea. 1999. Genetic variation among populations of the rare clustered lady-slipper orchid (Cypripedium fasciculatum) from Washington state, USA. Natural Areas Journal 19: 234–238.

    Google Scholar 

  • Aguinagalde, I., A. Hampe, A. Mohanty, J. P. Martín, J. Duminil, J. & R. J. Petit. 2005. Effects of life-history traits and species distribution on genetic structure at maternally inherited markers in European trees and shrubs. Journal of Biogeography 32: 329–339.

  • Azevedo, M. T. A., E. L. Borba, J. Semir & V. N. Solferini. 2007. High genetic variability in Neotropical myophilous orchids. Botanical Journal of the Linnean Society 153: 33–40.

    Article  Google Scholar 

  • Barrett, S. C. H. & J. R. Kohn. 1991. Genetic and evolutionary consequences of small population size in plants: implications for conservation. Pp. 3–30. In: D. A. Falk & K. E. Holsinger (eds). Genetics and conservation of rare plants. Oxford University Press, New York.

    Google Scholar 

  • Berg, E. E. & J. L. Hamrick. 1997. Quantification of genetic diversity at allozyme loci. Canadian Journal of Forest research 27: 415–424.

    Article  CAS  Google Scholar 

  • Bridger, R. 2016. Jeju Islanders resist airport megaproject. Save Jeju - Now No War Base on the Island of Peace. http://savejejunow.org/jeju-islanders-resist-airport-megaproject/. [Accessed March, 2017].

  • Bronstein, J. L., W. S. Armbruster & J. N. Thompson. 2014. Understanding evolution and the complexity of species interactions using orchids as a model system. New Phytologist 202: 373–375.

    Article  PubMed  Google Scholar 

  • Brzosko, E. & A. Wróblewska. 2013. Genetic diversity of nectar-rewarding Platanthera chlorantha and nectarless Cephalanthera rubra. Botanical Journal of the Linnean Society 171: 751–763.

    Article  Google Scholar 

  • ———, A. Wróblewska & I. Tałałaj. 2004. Genetic variation and genotypic diversity in Epipactis helleborine populations from NE Poland. Plant Systematics and Evolution 248: 57–69.

  • ———, I. Tałałaj, & A. Wróblewska. 2006. Genetic structure of rare Epipactis atrorubens populations from two national parks in northeastern Poland. Polish Botanical Studies 22: 1–10.

  • ———, A. Wróblewska, I. Tałałaj & W. Adamowski. 2009. Patterns of genetic diversity in Platanthera bifolia (Orchidaceae) with respect to life history traits and recent range expansion. Folia Geobotanica 44: 131–144.

  • ———, A. Wróblewska, I. Tałałaj & E. Wasilewska. 2011. Genetic diversity of Cypripedium calceolus in Poland. Plant Systematics and Evolution 295: 83–96.

  • ———, A. Wróblewska, E. Jermakowicz & A. Hermaniuk. 2013. High level of genetic variation within clonal orchid Goodyera repens. Plant Systematics and Evolution 299: 1537–1548.

  • Cardillo, M., G. M. Mace, J. L. Gittleman, K. E. Jones, J. Bielby & A. Purvis. 2008. The predictability of extinction: biological and external correlates of decline in mammals. Proceedings of the Royal Society B – Biological Sciences 275: 1441–1448.

    Article  PubMed  PubMed Central  Google Scholar 

  • Case, M. A. 1994. Extensive variation in the levels of genetic diversity and degree of relatedness among five species of Cypripedium (Orchidaceae). American Journal of Botany 81: 175–184.

    Article  Google Scholar 

  • ———. 2002. Evolutionary patterns in Cypripedium: inferences from allozyme analyses. Pp. 192–202. In: J. Clark, W. M. Elliott, G. Tingley & J. Biro (eds). Proceedings of the 16th world conference, Vancouver, 1999. Vancouver Orchid Society, Canada.

    Google Scholar 

  • ———, H. T. Mlodozeniec, L. E. Wallace & T. W. Weldy. 1998. Conservation genetics and taxonomic status of the rare Kentucky lady’s slipper: Cypripedium kentuckiense (Orchidaceae). American Journal of Botany 85: 1779–1786.

  • Catling, P. M. & B. Kostiuk. 2011. Some wild Canadian orchids benefit from woodland hiking trails – and the implications. The Canadian Field-Naturalist 125: 105–115.

    Article  Google Scholar 

  • Chase, M. W., K. M. Cameron, J. V. Freudenstein, et al. 2015. An updated classification of Orchidaceae. Botanical Journal of the Linnean Society 177: 151–174.

    Article  Google Scholar 

  • Chen, Q., K. Lang, S. W. Gale, P. J. Cribb & P. Ormerod. 2001. Goodyera repens (Linnaeus) R. Brown in W. T. Aiton. Pp. 48. In: Z.-Y. Wu, P. H. Raven & D. Y. Hong (eds). Flora of China, vol. 25, Orchidaceae. Science Press, Beijing and Missouri Botanical Garden Press, St. Louis.

    Google Scholar 

  • Chung, G. S. & K.-S. Hwang. 2015. Suggestions for efficient management of the protected areas with multiple international designations on Jeju Island. World Environment and Island Studies 5: 43–52.

    Google Scholar 

  • Chung, J. M., K. W. Park, C.-S. Park, S.-H. Lee, M. G. Chung & M. Y. Chung. 2009. Contrasting levels of genetic diversity between the historically rare orchid Cypripedium japonicum and the historically common orchid Cypripedium macranthos in South Korea. Botanical Journal of the Linnean Society 160: 119–129.

    Article  Google Scholar 

  • Chung, M. Y. 2009a. Low levels of genetic variation within populations of the four rare orchids Gymnadenia cucullata, Gymnadenia camtschatica, Amitostigma gracile, and Pogonia minor in South Korea: indication of genetic drift and implications for conservation. Plant Systematics and Evolution 281: 65–76.

    Article  Google Scholar 

  • ———. 2009b. Lack of allozyme diversity in populations of the rare, endangered terrestrial orchids Tipularia japonica and Epipactis papillosa in Korea. Plant Systematics and Evolution 278: 203–209.

    Article  CAS  Google Scholar 

  • ——— & M. G. Chung. 1999. Allozyme diversity and population structure in Korean populations of Cymbidium goeringii (Orchidaceae). Journal of Plant Research 112: 139–144.

  • ——— & ———. 2000. Allozyme diversity in populations of Cymbidium goeringii (Orchidaceae). Plant Biology 2: 77–82.

    Article  CAS  Google Scholar 

  • ——— & ———. 2007. Extremely low levels of genetic diversity in the terrestrial orchid Epipactis thunbergii (Orchidaceae) in South Korea: implications for conservation. Botanical Journal of Linnean Society 155: 161–169.

    Article  Google Scholar 

  • ——— & ———. 2010. Population genetic diversity and structure in Goodyera rosulacea (Orchidaceae), endemic in Korea, and implications for conservation. Annales Botanici Fennici 47: 460–470.

    Article  Google Scholar 

  • ——— & ———. 2014. Large effective population sizes and high levels of gene flow between subpopulations of Lilium cernuum (Liliaceae). Biochemical Systematics and Ecology 54: 354–361.

    Article  CAS  Google Scholar 

  • ———, J. D. Nason & M. G. Chung. 2004a. Implications of clonal structure for effective population size and genetic drift in a rare terrestrial orchid, Cremastra appendiculata (Orchidaceae). Conservation Biology 18: 1515–1524.

  • ———, ——— & ———. 2004b. Spatial genetic structure in populations of the terrestrial orchid Cephalanthera longibracteata (Orchidaceae). American Journal of Botany 91: 52–57.

    Article  PubMed  Google Scholar 

  • ———, ——— & ———. 2005a. Spatial genetic structure in populations of the terrestrial orchid Orchis cyclochila (Orchidaceae). Plant Systematics and Evolution 254: 209–219.

    Article  Google Scholar 

  • ———, ——— & ———. 2005b. Patterns of hybridization and population genetic structure in the terrestrial orchids Liparis kumokiri and Liparis makinoana (Orchidaceae) in sympatric populations. Molecular Ecology 14: 4389–4402.

    Article  CAS  PubMed  Google Scholar 

  • ———, C.-W. Park & M. G. Chung. 2007a. Extremely low levels of allozyme variation of the two rare and endangered lithophytes or epiphytes Bulbophyllum drymoglossum and Sarcanthus scolopendrifolius (Orchidaceae). Biodiversity and Conservation 16: 775–786.

  • ———, ———, E. R. Myers & M. G. Chung. 2007b. Contrasting levels of genetic diversity between the common, self-compatible Liparis kumokiri and rare, self-incompatible Liparis makinoana (Orchidaceae) in South Korea. Botanical Journal of Linnean Society 153: 41–48.

    Article  Google Scholar 

  • ———, J. López-Pujol, M. Maki, K.-J. Kim, J. M. Chung, B.-Y. Sun & M. G. Chung. 2012. Genetic diversity in the common terrestrial orchid Oreorchis patens and its rare congener Oreorchis coreana: inference of species evolutionary history and implications for conservation. Journal of Heredity 103: 692–702.

  • ———, M.-O. Moon, J. López-Pujol, M. Maki, T. Yamashiro, T. Yukawa, N. Sugiura, Y.-I. Lee & M. G. Chung. 2013a. Was Jeju Island a glacial refugium for East Asian warm-temperate plants? Insights from the homosporous fern Selliguea hastata (Polypodiaceae). American Journal of Botany 100: 2240–2249.

  • ———, J. López-Pujol & M. G. Chung. 2013b. Low genetic diversity in marginal populations of Bletilla striata (Orchidaceae) in southern Korea: Insights into population history and implications for conservation. Biochemical Systematics and Ecology 46: 88–96.

  • ———, ———, M. Maki, M.-O. Moon, J. O. Hyun & M. G. Chung. 2013c. Genetic variation and structure within 3 endangered Calanthe species (Orchidaceae) from Korea: Inference of population-establishment history and implications for conservation. Journal of Heredity 102: 248–262.

  • ———, ———, M.-O. Moon, M. Maki, T. Yukawa, N. Sugiura & M. G. Chung. 2013d. Population history of the terrestrial orchid Cremastra appendiculata var. variabilis from Korea, inferred from levels and distribution of genetic diversity. Botanical Journal of the Linnean Society 173: 721–732.

    Article  Google Scholar 

  • ———, J. D. Nason, J. López-Pujol, T. Yamashiro, B.-Y. Yang, Y.-B. Luo & M. G. Chung. 2014. Genetic consequences of fragmentation on populations of the terrestrial orchid Cymbidium goeringii. Biological Conservation 170: 222–231.

  • ———, J. López-Pujol & M. G. Chung. 2016. Is the Baekdudaegan “the Southern Appalachians of the East”? A comparison between these mountain systems, focusing on their role as glacial refugia. Korean Journal of Plant Taxonomy 46: 337–347.

  • ———, ——— & ———. 2017. The role of the Baekdudaegan (Korean Peninsula) as a major glacial refugium for plant species: A priority for conservation. Biological Conservation 206: 236–248.

    Article  Google Scholar 

  • Cole, C. T. 2003. Genetic variation in rare and common plants. Annual Review of Ecology and Systematics 34: 213–237.

    Article  Google Scholar 

  • Cozzolino, S. & A. Widmer. 2005. Orchid diversity: an evolutionary consequence of deception? Trends in Ecology & Evolution 20: 487–494.

    Article  Google Scholar 

  • Dolezal, J., J. Altman, M. Kopecky, T. Cerny, S. Janecek, et al. 2012. Plant diversity changes during the postglacial in East Asia: Insights from forest refugia on Halla Volcano, Jeju Island. PLoS ONE 7: e33065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • EAJ (Environment Agency of Japan). 2000. Red data book 1997. Threatened wildlife of Japan 8: Vascular plants. Japan Wildlife Research Center, Tokyo [in Japanese].

    Google Scholar 

  • EAJ (Environment Agency of Japan). 2015. Red data book 2014.Threatened wildlife of Japan 8: Vascular plants. Japan Wildlife Research Center, Tokyo [in Japanese].

    Google Scholar 

  • Ehlers, B. K. & H. E. Pedersen. 2000. Genetic variation in three species of Epipactis (Orchidaceae): geographic scale and evolutionary inferences. Biological Journal of the Linnean Society 69: 411–430.

    Article  Google Scholar 

  • Ellstrand, N. C. & D. R. Elam. 1993. Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24: 217–242.

    Article  Google Scholar 

  • Eum, S. M., S. Gale, T. Yukawa & N. S. Lee. 2011. Phylogenetic and conservation status of the endangered terrestrial orchid Nervilia nipponica (Orchidaceae) in Korea. Biochemical Systematics and Ecology 39: 635–642.

    Article  CAS  Google Scholar 

  • Fay, M. F., T. Pailler & K. W. Dixon. 2015. Orchid conservation: making the links. Annals of Botany 116: 377–379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125: 1–15.

    Article  Google Scholar 

  • Fenster, C. B. & M. R. Dudash. 1994. Genetic considerations for plant population restoration and conservation. Pp. 34–62. In: Bowles, M. L. & C. J. Whelan (eds.), Restoration of endangered species: Conceptual issues, planning and implementation. Cambridge University Press, Cambridge.

    Chapter  Google Scholar 

  • Forrest, A. D., M. L. Hollingsworth, P. M. Hollingsworth, C. Sydes & R. M. Bateman. 2004. Population genetic structure in European populations of Spiranthes romanzoffiana set in the context of other genetic studies on orchids. Heredity 92: 218–227.

    Article  CAS  PubMed  Google Scholar 

  • Frankham, R., J. D. Ballou & D. A. Briscoe. 2002. Introduction to conservation genetics. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Gaston, K. J. & R. A. Fuller. 2009. The sizes of species’ geographic ranges. Journal of Applied Ecology 46: 1–9.

    Article  Google Scholar 

  • Ghorbani, A., B. Gravendeel, F. Naghibi & H. de Boer. 2014. Wild orchid tuber collection in Iran: a wake-up call for conservation. Biodiversity and Conservation 23: 2749–2760.

    Article  Google Scholar 

  • Gitzendanner, M. A. & P. S. Soltis. 2000. Patterns of genetic variation in rare and widespread congeners. American Journal of Botany 87: 783–792.

    Article  CAS  PubMed  Google Scholar 

  • Godt, M. J. W. & J. L. Hamrick. 2001. Genetic diversity in rare southeastern plants. Natural Areas Journal 21: 61–70.

    Google Scholar 

  • Gravendeel, B., A. Smithson, F. J. W. Slik & A. Schuiteman. 2004. Epiphytism and pollinator specialisation: drivers for orchid diversity? Philosophical Transactions of the Royal Society of London B 359: 1523–1535.

    Article  Google Scholar 

  • Gray, A. 1996. Genetic diversity and its conservation in natural populations of plants. Biodiversity Letters 3: 71–80.

    Article  Google Scholar 

  • Hamrick, J. L. & M. J. W. Godt. 1989. Allozyme diversity in plant species. Pp 43–63. In: A. H. D. Brown, M. T. Clegg, A. L. Kahler & B. S. Weir (eds). Plant population genetics: breeding and germplasm resources. Sinauer, Sunderland.

    Google Scholar 

  • ——— & M. J. W. Godt. 1996. Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society B: Biological Sciences 351: 1291–1298.

  • Harris, S. A. & R. J. Abbott. 1997. Isozyme analysis of the reported origin of a new hybrid orchid species, Epipactis youngiana (Young’s helleborine), in the British Isles. Heredity 79: 402–407.

    Article  CAS  Google Scholar 

  • Hewitt, G. M. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58: 247–276.

    Article  Google Scholar 

  • ——— 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.

    Article  CAS  PubMed  Google Scholar 

  • Hollingsworth, P. M. & J. H. Dickson. 1997. Genetic variation in rural and urban populations of Epipactis helleborine (L.) Crantz. (Orchidaceae). Botanical Journal of the Linnean Society 123: 321–331.

    Google Scholar 

  • Izawa, T., T. Kawahara & H. Takahashi. 2007. Genetic diversity of an endangered plant, Cypripedium macranthos var. rebunense (Orchidaceae): background genetic research for future conservation. Conservation Genetics 8: 1369–1376.

    Article  Google Scholar 

  • Jin, W.-T., X.-H. Jin, A. Schuiteman, D.-Z. Li, X.-G. Xiang, W.-C. Huang, J.-W. Li & L.-Q. Huang. 2014. Molecular systematics of subtribe Orchidinae and Asian taxa of Habenariinae (Orchideae, Orchidaceae) based on plastid matK, rbcL and nuclear ITS. Molecular Phylogenetics and Evolution 77: 41–53.

    Article  PubMed  Google Scholar 

  • Kallunki, J. 1976. Population studies in Goodyera (Orchidaceae) with emphasis on the hybrid origin of G. tesselata. Brittonia 28: 53–75.

    Article  Google Scholar 

  • Kang, H.-G., C.-S. Kim & E.-S. Kim. 2013. Human influence, regeneration, and conservation of the Gotjawal forests in Jeju Island, Korea. Journal of Marine and Island Cultures 2: 85–92.

    Article  Google Scholar 

  • Karron, J. D. 1987. A comparison of levels of genetic polymorphism and self-compatibility in geographically restricted and widespread plant congeners. Evolutionary Ecology 1: 47–58.

    Article  Google Scholar 

  • Kennedy, A. H. & G. L. Walker. 2007. The population genetic structure of the showy lady’s slipper orchid (Cypripedium reginae Walter) in its glaciated and unglaciated ranges. Castanea 72: 248–261.

    Article  Google Scholar 

  • Kim, C.-S. 2009. Vascular plant diversity of Jeju Island, Korea. Korean Journal of Plant Resources 22: 558–570.

    Google Scholar 

  • ———, M.-O. Mun & J.-G. Koh. 2009. A new record for the Korean flora: Nervilia nipponica Makino (Orchidaceae). Korean Journal of Plant Taxonomy 39: 229–232.

  • KNA (Korea National Arboretum). 2012. Rare plants in Korea. Korea National Arboretum, Pocheon [in Korean].

    Google Scholar 

  • Kong, W. S. & D. Watts. 1993. The plant geography of Korea with the emphasis on the alpine zones. Series Geobotany 19. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Lee, N. S. 2011. Illustrated flora of Korean orchids. Ewha Womans University Press, Seoul, p. 345 [in Korean].

    Google Scholar 

  • Lee, J.-S. & B.-H. Choi. 2006. Distributions and red data of wild orchids in the Korean Peninsula. Korean Journal of Plant Taxonomy 36: 335–360 [in Korean with English abstract].

    Article  Google Scholar 

  • ———, W. B. Lee, B. H. Choi & K. H. Tae. 2007. Orchidaceae Juss. Pp 1339–1376. In: C. W. Park (ed). The genera of vascular plants of Korea. Flora of Korea Editorial Committee, Academy Publishing Co., Seoul.

  • Lee, C. S., C. Tsutsumi, T. Yukawa & N. S. Lee. 2010. Two new species of the genus Liparis (Orchidaceae) from Korea based on morphological and molecular data. Journal of Plant Biology 53: 190–200.

    Article  CAS  Google Scholar 

  • Lee, H.-J., J.-C. Yang, Y.-M. Lee & H. H. Yang. 2013a. A new record of Habenaria (Orchidaceae) to Korean flora: H. dentata (Sw.) Schltr. Korean Journal of Plant Taxonomy 43: 223–226 [in Korean with English abstract].

    Article  CAS  Google Scholar 

  • Lee, J.-H., D.-H. Lee & B.-H. Choi. 2013b. Phylogeography and genetic diversity of East Asian Neolitsea sericea (Lauraceae) based on variations in chloroplast DNA sequences. Journal of Plant Research 126: 193–202.

    Article  PubMed  Google Scholar 

  • ———, ———, I.-S. Choi & B.-H. Choi. 2014. Genetic diversity and historical migration patterns of an endemic evergreen oak, Quercus acuta, across Korea and Japan, inferred from nuclear microsatellites. Plant Systematics and Evolution 300: 1913–1923.

    Article  Google Scholar 

  • Lim, D.-O. 2003. Vascular plants of mountain ridge from Cheonwangbong-Hyangjeokbong section in the Baekdudaegan. Korean Journal of Environment and Ecology 16: 359–386 [in Korean with English abstract].

    Google Scholar 

  • Liu, H., C.–L. Feng, Y.-B. Luo, B.–S. Chen, Z.–S. Wang & H.–Y. Gu. 2010. Potential challenges of climate change to orchid conservation in a wild orchid hotspot in southwestern China. Botanical Review 76: 174–192.

  • ———, Y.–B. Luo, J. Heinen, M. Bhat & Z.–J. Liu. 2014. Eat your orchid and have it too: a new conservation model for the Chinese medicinal orchids. Biodiversity and Conservation 23: 1215–1228.

  • Liu, Q., J. Chen, R. T. Corlett, X. Fan, D. Yu, H. Yang & J. Gao. 2015. Orchid conservation in the biodiversity hotspot of southwestern China. Conservation Biology 29: 1563–1572.

    Article  CAS  PubMed  Google Scholar 

  • López-Pujol, J., M. Bosch, J. Simon & C. Blanché. 2009. Patterns of genetic diversity in the highly threatened vascular flora of the Mediterranean Basin. Pp 45–79. In: A. Columbus & L. Kuznetsov (eds). Endangered species: new research. Nova Science Publishers, New York.

    Google Scholar 

  • Losos, J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11: 995–1007.

    Article  PubMed  Google Scholar 

  • McCormick, M. K. & H. Jacquemyn. 2014. What constrains the distribution of orchid populations? New Phytologist 202: 392–400.

    Article  Google Scholar 

  • MOE (Ministry of Environment, Republic of Korea). 2012. Red data book of endangered vascular plants in Korea. National Institute of Biological Resources, Incheon [in Korean].

    Google Scholar 

  • MOE (Ministry of Environment, Republic of Korea). 2014. Korean red list of threatened species. Second edition. National Institute of Biological Resources, Incheon.

    Google Scholar 

  • Morales, E. 2000. Estimating phylogenetic inertia in Tithonia (Asteraceae): A comparative approach. Evolution 54: 475–484.

    Article  CAS  PubMed  Google Scholar 

  • Nybom, H. 2004. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology 13: 1143–1155.

    Article  CAS  PubMed  Google Scholar 

  • Oh, G. S., M. Y. Chung, S. G. Chung & M. G. Chung. 2001. Contrast breeding system between Liparis kumokiri and Liparis makinoana (Orchidaceae). Annales Botanici Fennici 38: 281–284.

    Google Scholar 

  • Payne, J. L. & S. Finnegan. 2007. The effect of geographic range on extinction risk during background and mass extinction. Proceedings of the National Academy of Sciences of the United States of America 104: 10506–10511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips, R. D., A. P. Brown, K. W. Dixon & S. D. Hopper. 2011. Orchid biogeography and factors associated with rarity in a biodiversity hotspot, the Southwest Australian Floristic Region. Journal of Biogeography 38: 487–501.

    Article  Google Scholar 

  • ———, K. W. Dixon & R. Peakall. 2012. Low population genetic differentiation in the Orchidaceae: implications for the diversification of the family. Molecular Ecology 21: 5208–5220.

  • Pillon, Y. & M. W. Chase. 2007. Taxonomic exaggeration and its effects on orchid conservation. Conservation Biology 21: 263–265.

    Article  PubMed  Google Scholar 

  • Purvis, A., J. L. Gittleman, G. Cowlishaw & G. M. Mace. 2000. Predicting extinction risk in declining species. Proceedings of the Royal Society B - Biological Sciences 267: 1947–1952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu, Y.-X., C.-X. Fu & H. P. Comes. 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. Molecular Phylogenetic Evolution 59: 225–244.

    Article  Google Scholar 

  • Ribeiro, P. L., E. L. Borba, E. de Camargo, S. M. Lambert, A. S. Schnadelbach & C. van den Berg. 2008. Genetic and morphological variation in the Bulbophyllum exaltatum (Orchidaceae) complex occurring in the Brazilian “campos rupestres”: implications for taxonomy and biogeography. Plant Systematics and Evolution 270: 109–137.

    Article  Google Scholar 

  • Roberts, D. L. & K. W. Dixon. 2008. Orchids. Current Biology 18: R325–R329.

    Article  CAS  PubMed  Google Scholar 

  • Scacchi, R., P. Lanzara & G. De Angelis. 1987. Study of electrophoretic variability in Epipactis helleborine (L.) Crantz, E. palustris (L.) Crantz and E. microphylla (Ehrh.) Swartz (fam. Orchidaceae). Genetica 72: 217–224.

    Article  Google Scholar 

  • ———, G. De Angelis & R. M. Corbo. 1991. Effect of breeding system on the genetic structure in three Cephalanthera spp. (Orchidaceae). Plant Systematics and Evolution 176: 53–61.

  • Silvertown, J. & M. Dodd. 1996. Comparing plants and connecting traits. Philosophical Transactions of the Royal Society London B 351: 1233–1239.

    Article  Google Scholar 

  • Soltis, D. E., A. B. Morris, J. S. McLachlan, P. S. Manos & P. S. Soltis. 2006. Comparative phylogeography of unglaciated eastern North America. Molecular Ecology 15: 4261–4293.

    Article  PubMed  Google Scholar 

  • Son, O. & S.-W. Son. 2016. Development and characterization of EST-SSR markers for the endangered species Cypripedium japonicum. P. 373. In: Abstract book of the 7th EAFES International Congress “One Asia tied with ecosystems: living harmoniously with local people and nature”. Inter-Burgo Daegu, Daegu, South Korea.

  • Spielman, D., B. W. Brook & R. Frankham. 2004. Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the United States of America 101: 15261–15264.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squirrell, J., P. M. Hollingsworth, R. M. Bateman, J. H. Dickson, M. H. S. Light, M. MacConaill & M. C. Tebbitt. 2001. Partitioning and diversity of nuclear and organelle markers in native and introduced populations of Epipactis helleborine (Orchidaceae). American Journal of Botany 88: 1409–1418.

    Article  CAS  PubMed  Google Scholar 

  • Swarts, N. D. & K. W. Dixon. 2009. Terrestrial orchid conservation in the age of extinction. Annals of Botany 104: 543–556.

    Article  PubMed  PubMed Central  Google Scholar 

  • Takashima, M., J. Hasegawa & T. Yukawa. 2016. Oreorchis coreana (Orchidaceae), a new addition to the flora of Japan. Acta Phytotaxonomica et Geobatonica 67: 61–66.

    Google Scholar 

  • Tang, Y., T. Yukawa, R. M. Bateman, H. Jiang & H. Peng. 2015. Phylogeny and classification of the East Asian Amitostigma alliance (Orchidaceae: Orchideae) based on six DNA markers. BMC Evolutionary Biology 15: 96.

    Article  PubMed  PubMed Central  Google Scholar 

  • Templeton, A. R. 2006. Population genetics and microevolutionary theory. Wiley-Liss, Hoboken.

    Book  Google Scholar 

  • The Plant List. 2013. Version 1.1. Published on the Internet; http://www.theplantlist.org/ [accessed January 2016].

  • Tremblay, R. L., J. D. Ackerman, J. K. Zimmerman & R. N. Calvo. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of Linnean Society 84: 1–54.

    Article  Google Scholar 

  • Vásquez, R., P. L. Ibisch & B. Gerkmann. 2003. Diversity of Bolivian Orchidaceae – a challenge for taxonomic, floristic and conservation research. Organisms Diversity & Evolution 3: 93–102.

    Article  Google Scholar 

  • Vogt-Schilb, H., F. Munoz, F. Richard & B. Schatz. 2015. Recent declines and range changes of orchids in Western Europe (France, Belgium and Luxembourg). Biological Conservation 190: 133–141.

    Article  Google Scholar 

  • Wallace, L. E. 2002. Examining the effects of fragmentation on genetic variation in Platanthera leucophaea (Orchidaceae): Inferences from allozyme and random amplified polymorphic DNA markers. Plant Species Biology 17: 37–49.

    Article  Google Scholar 

  • ——— & M. A. Case. 2000. Contrasting allozyme diversity between northern and southern populations of Cypripedium parviflorum (Orchidaceae): implications for Pleistocene refugia and taxonomic boundaries. Systematics Botany 25: 281–296.

  • Waterman, R. J., M. I. Bidartondo, J. Stofberg, J. K. Combs, et al. 2011. The effects of above- and belowground mutualisms on orchid speciation and coexistence. The American Naturalist 177: E54–E68.

    Article  PubMed  Google Scholar 

  • Wong, K. C. & M. Sun. 1999. Reproductive biology and conservation genetics of Goodyera procera (Orchidaceae). American Journal of Botany 86: 1408–1413.

    Article  Google Scholar 

  • Yi, S. 2011. Holocene vegetation responses to East Asian monsoonal changes in South Korea. Pp. 157–178. In: J. Blanco & H. Kheradmand (eds). Climate change geophysical foundations and ecological effects. InTech, Rijeka.

    Google Scholar 

  • Zhang, Z., Y. Yan, Y. Tian, J. Li, J.-S. He & Z. Tang. 2015. Distribution and conservation of orchid species richness in China. Biological Conservation 181: 64–72.

    Article  Google Scholar 

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Acknowledgements

The authors thank all undergraduate and graduate students who were associated with the M. G. Chung’s laboratory since 1991. The two graduate students Hoa Thi Quynh Le and Son Hai Vu have helped to search for references in Table 1. Special thank goes to James Hamrick, John Nason, Rodney Peakall, Bryan Epperson, Mei Sun, James Ackerman, Raymond Tremblay, Dennis Whigham, Dorset Trapnell, Ken Cameron, Hans Jacquemyn, Chris Wilcock, and Mary Ruth Neiland, for their discussion on orchid conservation and pollination biology; Jae Min Chung, Jin Seok Kim, Jin O Hyun, Byung-Yun Sun, Chan-Soo Kim, Hyoung-Tak Im, Masayuki Maki, Naoto Sugiura, Tadashi Yamashiro, Takayuki Kawahara, Kenji Suetsugu, Kaoru Tsuji, Huai Zhen Tian, Chengxin Fu, Yi-Bo Luo, and Yung-I Lee for their help in locating wild orchids in Korea, Japan, China, and Taiwan or discussion on their breeding systems. This research was supported by Korea Research Foundation grants; KRF-2013R1A1A2063524 to M.Y. C. and NRF-2011-0017236, NRF-2013R1A1A3010892, and NRF-2017R1A2B4012215 to M. G. C. and was carried out as part of “Infrastructure for Conservation and Restoration of Rare and Endemic Plants in Korea National Arboretum” that supported to M. G. C. in 2015 to 2017.

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Chung, M.Y., López-Pujol, J., Son, S. et al. Patterns of Genetic Diversity in Rare and Common Orchids Focusing on the Korean Peninsula: Implications for Conservation. Bot. Rev. 84, 1–25 (2018). https://doi.org/10.1007/s12229-017-9190-5

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