Genetic diversity of the extremely rare Habenaria dentata and the rare Habenaria linearifolia (Orchidaceae) in South Korea: implications for population history and conservation
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Keywords

conservation
genetic diversity
Habenaria
historical events
population history

How to Cite

Chung, M. Y., Quynh Le, H. T., Son, S., Tian, H. Z. and Chung, M. G. (2018) “Genetic diversity of the extremely rare Habenaria dentata and the rare Habenaria linearifolia (Orchidaceae) in South Korea: implications for population history and conservation”, Plant Ecology and Evolution, 151(1), pp. 48-60. doi: 10.5091/plecevo.2018.1366.

Abstract

Background and aims – Since historical events often leave an indelible mark on levels of genetic diversity of plant populations, one may indirectly infer their evolutionary history with the help of current patterns of genetic diversity. The terrestrial orchid Habenaria dentata, an element of warm-temperate/subtropical vegetation, reaches its northernmost limits in the Korean Peninsula, and thus it is extremely rare there. As H. dentata was absent from the Peninsula during the Last Glacial Maximum (LGM), it is likely to be of post-glacial origin having arrived from either a single refugium or multiple refugia. However, its rare, temperate/boreal congener H. linearifolia might have persisted in situ in either macrorefugia or microrefugia on the Peninsula during the LGM.
Methods – To test which hypothesis is most appropriate for each species, we investigated levels of allozyme-based (17 loci) genetic diversity and population genetic structure in the two only known populations of H. dentata and in 12 populations of H. linearifolia.
Key results – No allozyme diversity was found in H. dentata (He = 0.000), whereas H. linearifolia exhibited low within-population variation (He = 0.060) and high among-population differentiation (FST = 0.237). We found little association between populations in relation to their geographic location; several populations presented individuals belonging to different clusters.
Conclusions – Our results suggest that H. dentata likely originated from a single ancestral population (perhaps from southern Japan or southern China) through post-glacial dispersal, whereas H. linearifolia probably survived the LGM in situ in microrefugia situated at low to mid-elevated regions. We further suggest that separate conservation strategies for each species should be employed, given that the two taxa have different ecological and demographic traits and harbour different levels of genetic diversity.

https://doi.org/10.5091/plecevo.2018.1366
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References

Arditti J., Ghani A.K.A. (2000) Numerical and physical properties of orchid seeds and their biological implications. New Phytologist 145: 367–421. https://doi.org/10.1046/j.1469-8137.2000.00587.x

Case M.A. (2002) Evolutionary patterns in Cypripedium: inferences from allozyme analysis. In: Clark J., Elliott W. M., Tingley G., Biro J. (eds) Proceedings of the 16th World Orchid Conference: 192–202. Vancouver, Vancouver Orchid Society.

Ceska J.F., Affolter J.M., Hamrick J.L. (1997) Developing a sampling strategy for Baptisia arachnifera based on allozyme diversity. Conservation Biology 11: 1131–1139. https://doi.org/10.1046/j.1523-1739.1997.95527.x

Charrier O., Dupont P., Pornon A., Escaravage N. (2014) Microsatellite marker analysis reveals the complex phylogeographic history of Rhododendron ferrugineum (Ericaceae) in the Pyrenees. PLoS ONE 9: e92976. https://doi.org/10.1371/journal.pone.0092976

Cheliak W.M., Pitel J.P. (1984) Technique for starch gel electrophoresis of enzyme from forest tree species. Information report PI-X-42. Chalk River, Ontario, Canada, Petawawa National Forestry Institute.

Chen X., Cribb P.J. (2009) Habenaria Willdenow. In: Wu Z.Y., Raven P.H., Hong D.Y. (eds) Flora of China, vol. 25 (Orchidaceae): 144–160. Beijing, Science Press; St. Louis, Missouri Botanical Garden Press.

Choi K.R. (1998) The post-glacial vegetation history of the lowland in Korean Peninsula. The Korean Journal of Ecology 21: 169–174.

Chung C.-H., Lim H.S., Yoon H.I. (2006) Vegetation and climate changes during the Late Pleistocene to Holocene inferred from pollen record in Jinju area, South Korea. Geosciences Journal 10: 423–431. https://doi.org/10.1007/BF02910436

Chung C.-H., Lim H.S., Lee H.J. (2010) Vegetation and climate history during the late Pleistocene and early Holocene inferred from pollen record in Gwangju area, South Korea. Quaternary International 227: 61–67. https://doi.org/10.1016/j.quaint.2010.06.002

Chung J.M., Park K.W., Park C.-S., Lee S.-H., Chung M.G., Chung M.Y. (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. https://doi.org/10.1111/j.1095-8339.2009.00965.x

Chung M.G., Chung M.Y., Oh G.S., Epperson B.K. (2000) Spatial genetic structure in a Neolitsea sericea population (Lauraceae). Heredity 85: 490–497. https://doi.org/10.1046/j.1365-2540.2000.00781.x

Chung M.Y., Chung M.G. (1999) Allozyme diversity and population structure in Korean populations of Cymbidium goeringii (Orchidaceae). Journal of Plant Research 112: 139–144. https://doi.org/10.1007/PL00013868

Chung M.Y., Nason J.D., Chung M.G. (2005a) Spatial genetic structure in populations of the terrestrial orchid Orchis cyclochila (Orchidaceae). Plant Systematics and Evolution 254: 209–219. https://doi.org/10.1007/s00606-005-0341-5

Chung M.Y., Nason J.D., Chung M.G. (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. https://doi.org/10.1111/j.1365-294X.2005.02738.x

Chung M.Y. (2009) 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. https://doi.org/10.1007/s00606-008-0140-x

Chung M.Y., Chung M.G. (2012) A review of the use of genetic markers in orchid systematics with emphasis on allozymes. Biochemical Systematics and Ecology 41: 62–73. https://doi.org/10.1016/j.bse.2011.12.012

Chung M.Y., López-Pujol J., Chung J.M., Kim K.-J., Chung M.G. (2012a) Low within population genetic variation and high among population differentiation in Cyrtomium falcatum (L.f.) C. Presl (Dryopteridaceae) in southern Korea: inference of population establishment history. American Fern Journal 102: 256–272. https://doi.org/10.1640/0002-8444-102.4.256

Chung M.Y., López-Pujol J., Maki M., Kim K.-J., Chung J.M., Sun B.-Y., Chung M.G. (2012b) 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. https://doi.org/10.1093/jhered/ess032

Chung M.Y., López-Pujol J., Chung M.G. (2013a) 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. https://doi.org/10.1016/j.bse.2012.09.019

Chung M.Y., López-Pujol J., Maki M., Moon M.-O., Hyun J.O., Chung M.G. (2013b) Genetic variation and structure within 3 endangered Calanthe species (Orchidaceae) from Korea: inference of population-establishment history and implications for conservation. Journal of Heredity 104: 248–262. https://doi.org/10.1093/jhered/ess088

Chung M.Y., López-Pujol J., Chung M.G. (2013c) Population history of the two carnivorous plants Drosera peltata var. nipponica and D. rotundifolia (Droseraceae) in Korea. American Journal of Botany 100: 2231–2239. https://doi.org/10.3732/ajb.1200486

Chung M.Y., Moon M.-O., López-Pujol J., Maki M., Yamashiro T., Yukawa T., Sugiura N., Lee Y.-I., Chung M.G. (2013d) 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. https://doi.org/10.3732/ajb.1300134

Chung M.Y., López-Pujol J., Moon M.-O., Maki M., Yukawa T., Sugiura N., Chung M.G. (2013e) 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. https://doi.org/10.1111/boj.12109

Chung M.Y., Chung M.G., López-Pujol J., Ren M.-X., Zhang Z.-Y., Park S.J. (2014a) Were the main mountain ranges in the Korean Peninsula a glacial refugium for plants? Insights from the congeneric pair Lilium cernuum – Lilium amabile. Biochemical Systematics and Ecology 53: 36–45. https://doi.org/10.1016/j.bse.2013.12.019

Chung M.Y., López-Pujol J., Chung M.G. (2014b) Genetic homogeneity between Korean and Japanese populations of the broad-leaved evergreen tree Machilus thunbergii (Lauraceae): a massive post-glacial immigration through the Korea Strait or something else? Biochemical Systematics and Ecology 53: 20–28. https://doi.org/10.1016/j.bse.2013.12.006

Chung M.Y., López-Pujol J., Chung M.G. (2014c) Comparative biogeography of the congener lilies Lilium distichum and Lilium tsingtauense in Korea. Flora 209: 435–445. https://doi.org/10.1016/j.flora.2014.04.005

Chung M.Y., López-Pujol J., Lee Y.M., Oh S.H., Chung M.G. (2015) Clonal and genetic structure of Iris odaesanensis and Iris rossii (Iridaceae): insights of the Baekdudaegan Mountains as a glacial refugium for boreal and temperate plants. Plant Systematics and Evolution 301: 1397–1409. https://doi.org/10.1007/s00606-014-1168-8

Chung M.Y., López-Pujol J., Chung M.G. (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. https://doi.org/10.1016/j.biocon.2016.11.040

Chung M.Y., López-Pujol J., Son S., Suh G.U., Yukawa T., Chung M.G. (in press) Patterns of genetic diversity in rare and common orchids focusing on the Korean Peninsula: implications for conservation. The Botanical Review. https://doi.org/10.1007/s12229-017-9190-5

Clayton J.W., Tretiak D.N. (1972) Amine citrate buffers for pH control in starch gel electrophoresis. Journal of the Fisheries Research Board of Canada 29: 1169–1172. https://doi.org/10.1139/f72-172

Comes H.P., Kadereit J.W. (2003) Spatial and temporal patterns in the evolution of the flora of the European Alpine System. Taxon 52: 451–462. https://doi.org/10.2307/3647445

Cornuet J.M., Luikart G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001–2014.

Daïnou K., Bizoux J.-P., Doucet J.-L., Mahy G., Hardy O.J., Heuertz M. (2010) Forest refugia revisited: SSRs and cpDNA sequence support historial isolation in a wide-spread African tree with high colonization capacity, Milicia excelsa (Moraceae). Molecular Ecology 19: 4462–4477. https://doi.org/10.1111/j.1365-294X.2010.04831.x

Davis M.B., Shaw R.G. (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292: 673–679. https://doi.org/10.1126/science.292.5517.673

Dressler R.L. (1981) The orchids: natural history and classification. Cambridge, USA, Harvard University Press.

Earl D.A., vonHoldt B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361. https://doi.org/10.1007/s12686-011-9548-7

El Mousadik A., Petit R.J. (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeeels] endemic to Morocco. Theoretical and Applied Genetics 92: 832–839. https://doi.org/10.1007/BF00221895

Evanno G., Regnaut S., Goudet J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

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

Fischer M.L., Hochkirch A., Heddergott M., Schulze C., Anheyer-Behmenburg H.E., Lang J., Michler F.-W., Hohmann U., Ansorge H., Hoffmann L., Klein R., Frantz A.C. (2015) Historical invasion records can be misleading: genetic evidence for multiple introductions of invasive raccoons (Procyon lotor) in Germany. PLoS ONE 10: e0125441. https://doi.org/10.1371/journal.pone.0125441

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

Godt M.J.W., Johnson B.R., Hamrick J.L. (1996) Genetic diversity and population size in four rare southern Appalachian plant species. Conservation Biology 10: 796–805. https://doi.org/10.1046/j.1523-1739.1996.10030796.x

Goudet J. (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86: 485–486. https://doi.org/10.1093/oxfordjournals.jhered.a111627

Hamrick J.L., Nason J.D. (1996) Consequences of dispersal in plants. In: Rhodess Jr. O.E., Chesser R.K., Smith M.H. (eds) Population dynamics in ecological space and time: 203–236. Chicago, University of Chicago Press.

Hardy O.J., Vekemans X. (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x

Harrison S.P., Yu G., Takahara H., Prentice I.C. (2001) Palaeovegetation (communications arising): diversity of temperate plants in east Asia. Nature 413: 129–130. https://doi.org/10.1038/35093166

Haufler C.H. (1985) Enzyme variability and modes of evolution in Bommeria (Pteridaceae). Systematic Botany 10: 92–104. https://doi.org/10.2307/2418438

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. https://doi.org/10.1111/j.1095-8312.1996.tb01434.x

Hewitt G.M. (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907–913. https://doi.org/10.1038/35016000

Hope G., Kershaw A.P., van der Kaars S., Sun X., Liew P.-M., Heusser L.E., Takahara H., McGlone M., Miyoshi N., Moss P.T. (2004) History of vegetation and habitat change in the Austral-Asian region. Quaternary International 118–119: 103–126. https://doi.org/10.1016/S1040-6182(03)00133-2

Hou X.-Y. (1983) Vegetation of China with reference to its geographical distribution. Annals of the Missouri Botanical Garden 70: 509–548. https://doi.org/10.2307/2992085

Hu F.S., Hampe A., Petit R.J. (2009) Paleoecology meets genetics: deciphering past vegetational dynamics. Frontiers in Ecology and the Environment 7: 371–379. https://doi.org/10.1890/070160

Hurlbert S.H. (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52: 577–586. https://doi.org/10.2307/1934145

Jakobsson M., Rosenberg N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801–1806. https://doi.org/10.1093/bioinformatics/btm233

Janes J.K., Miller J.M., Dupuis J.R., Malenfant R.M., Gorrell J.C., Cullingham C.I., Andrew R.L. (2017) The K = 2 conundrum. Molecular Ecology 26: 3594–3602. https://doi.org/10.1111/mec.14187

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

Konnert M., Bergmann F. (1995) The geographical distribution of genetic variation of silver fir (Abies alba, Pinaceae) in relation to its migration history. Plant Systematics and Evolution 196: 19–30. https://doi.org/10.1007/BF00985333

Langella O. (1999) Populations version 1.2.30. Available from: http://bioinformatics.org/~tryphon/populations/ [accessed 14 Aug. 2016].

Lee H.J., Yang J.C., Lee Y.M., Yang H.H. (2013a) A new record of Habenaria (Orchidaceae) to Korean flora: H. dentata (Sw.) Schltr. Korean Journal of Plant Taxonomy 43: 223–226. https://doi.org/10.11110/kjpt.2013.43.3.223

Lee J.-H., Lee D.-H., Choi B.-H. (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. https://doi.org/10.1007/s10265-012-0519-1

Lesica P., Leary R.F., Allendord F.R., Bilderback O.E. (1988) Lack of genic diversity within and among populations of an endangered plant, Howellia aquatilis. Conservation Biology 2: 275–282. https://doi.org/10.1111/j.1523-1739.1988.tb00184.x

López-Pujol J., López-Vinyallonga S., Alfonso S., Ertuğrul K., Uysal T., Tugay O., Guetat A., Garcia-Jacas N. (2016) Speciation and genetic diversity in Centaurea subsect. Phalolepis in Anatolia. Scientific Reports 6: 37818. https://doi.org/10.1038/srep37818

Luikart G., Allendorf F.W., Cornuet J.-M., Sherwin W.B. (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89: 238–247. https://doi.org/10.1093/jhered/89.3.238

Maki M., Matsumua S., Yamashiro T. (2008) Allozyme diversity and history of distribution expansion in the maritime perennial plant Hedyotis strigulosa (Rubiaceae), distributed over the wide latitudes in the Japanese Archipelago. Biological Journal of the Linnean Society 93: 679–688. https://doi.org/10.1111/j.1095-8312.2007.00894.x

Maki M., Kokubugata G., Yamashiro T. (2010) Lack of allozyme diversity in populations of the endangered perennial Senecio scandens (Asteraceae) in Japan: comparison with a population in Taiwan. Journal of Phytogeography and Taxonomy 58: 39–42.

Mitton J.B., Linhart Y.B., Sturgeon K.B., Hamrick J.L. (1979) Allozyme polymorphisms detected in mature needle tissue of ponderosa pine. Journal of Heredity 70: 86–89. https://doi.org/10.1093/oxfordjournals.jhered.a109220

MOE (Ministry of Environment, Republic of Korea) (2014) Korean red list of threatened species. 2nd Ed. Incheon, National Institute of Biological Resources.

Nei M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.

Nei M., Maruyama T., Chakraborty R. (1975) The bottleneck effect and genetic variability in populations. Evolution 29: 1–10. https://doi.org/10.2307/2407137

Nei M., Tajima F., Tateno Y. (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. Journal of Molecular Evolution 19: 153–170. https://doi.org/10.1007/BF02300753

Ohwi J. (1965) Flora of Japan. Washington, D.C., Smithsonian Institution.

Page R.D.M. (1996) TreeView: an application to display phylogenetic trees on personal computers. Bioinformatics 12: 357–358. https://doi.org/10.1093/bioinformatics/12.4.357

Phillips R.D., Dixon K.W., Peakall R. (2012) Low population genetic differentiation in the Orchidaceae: implications for the diversification of the family. Molecular Ecology 21: 5208–5220. https://doi.org/10.1111/mec.12036

Prentice I.C., Harrison S.P., Bartlein P.J. (2011) Global vegetation and terrestrial carbon cycle changes after the last ice age. New Phytologist 189: 988–998. https://doi.org/10.1111/j.1469-8137.2010.03620.x

Pritchard J.K., Stephens M., Donnelly P. (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

Pritchard J.K., Wen X., Falush D. (2010) Documentation for structure software: Version 2.3. Chicago, Department of Human Genetics, University of Chicago. Available from: http://web.stanford.edu/group/pritchardlab/structure_software/release_versions/v2.3.3/structure_doc.pdf [accessed 14 Jan. 2017].

Qiu Y.-X., Fu C.-X. Comes H.P. (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 Phylogenetics and Evolution 59: 225–244. https://doi.org/10.1016/j.ympev.2011.01.012

Rosenberg N.A. (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4: 137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x

Rousset F. (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219–1228.

Rull V. (2009) Microrefugia. Journal of Biogeography 36: 481–484. https://doi.org/10.1111/j.1365-2699.2008.02023.x

Soltis D.E., Haufler C.H., Darrow D.C., Gastony G.J. (1983) Starch gel electrophoresis of ferns: a compilation of grinding buffers, gel and electrode buffers, and staining schedules. American Fern Journal 73: 9–27. https://doi.org/10.2307/1546611

Sun M., Wong K.C. (2001) Genetic structure of three orchid species with contrasting breeding systems using RAPD and allozyme markers. American Journal of Botany 88: 2180–2188.

Takashima M., Hasegawa J., Yukawa T. (2016) Oreorchis coreana (Orchidaceae), a new addition to the flora of Japan. Acta Phytotaxonomica et Geobotanica 67: 61–66. https://doi.org/10.18942/apg.KJ00010238488

Torroba-Balmori P., Budde K.B., Heer K., González-Martínez S.C., Olsson S., Scotti-Saintagne C., Casalis M., Sonké B., Dick C.W., Heuertz M. (2017) Altitudinal gradients, biogeographic history and microhabitat adaptation affect fine-scale spatial genetic structure in African and Neotropical populations of an ancient tropical tree species. PLoS ONE 12: e0182515. https://doi.org/10.1371/journal.pone.0182515

Trapnell D.W., Hamrick J.L. (2004) Partitioning nuclear and chloroplast variation at multiple spatial scales in the neotropical epiphytic orchid, Laelia rubescens. Molecular Ecology 13: 2655–2666. https://doi.org/10.1111/j.1365-294X.2004.02281.x

Trapnell D.W., Hamrick J.L., Ishibashi C.D., Kartzinel T.R. (2013) Genetic inference of epiphytic orchid colonization; it may only take one. Molecular Ecology 22: 3680–3692. https://doi.org/10.1111/mec.12338

van der Bank H., van der Bank M., van Wyk B.-E. (2001) A review of the use of allozyme electrophoresis in plant systematics. Biochemical Systematics and Ecology 29: 469–483. https://doi.org/10.1016/S0305-1978(00)00086-7

Weir B.S., Cockerham C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370. https://doi.org/10.2307/2408641

Widmer A., Lexer C. (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends in Ecology & Evolution 16: 267–269. https://doi.org/10.1016/S0169-5347(01)02163-2

Willis K.J., Niklas K.J. (2004) The role of Quaternary environmental change in plant macroevolution: the exception of the rule? Philosophical Transactions of the Royal Society B: Biological Sciences 359: 159–172. https://doi.org/10.1098/rstb.2003.1387

Wilson G.A., Rannala B. (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163: 1177–1191.

Wright S. (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19: 395–420. https://doi.org/10.2307/2406450

Wu Z.Y., Raven P.H., Hong D.Y. (eds) (2009) Flora of China, Vol. 25 (Orchidaceae). Beijing, Science Press; St. Louis, Missouri Botanical Garden Press.

Yeh F.C., Yang R.-C., Boyle T.B.J. (1999) POPGENE version 1.31. Microsoft Windows-based freeware for population genetic analysis. Quick users’ guide. Edmonton, University of Alberta. Available from https://sites.ualberta.ca/~fyeh/popgene.pdf [accessed 3 Jan. 2018].

Yi S., Kim S.-J. (2010) Vegetation changes in western central region of Korean Peninsula during the last glacial (ca. 21.1–26.1 cal kyr BP). Geosciences Journal 14: 1–10. https://doi.org/10.1007/s12303-010-0001-9

Yukawa T., Kawaguchi D., Mukai A., Komaki Y. (2012) Discovery of Geodorum densiflorum (Ochidaceae) on the Ogasawara (Bonin) Islands: a case of ongoing colonization subsequent to long-distance dispersal. Bulletin of the National Museum of Nature and Science. Series B, Botany 38: 131–137.

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