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

Introduction

It is generally agreed that a complex network of factors shape genetic diversity in plant populations and species, and these can be classified into two large categories (Gray, 1996): (0 'intrinsic' biological properties of the species (mainly the life- history traits such as mode of pollination, breeding system, seed dispersal mechanism, habit, or life-form) and (ii) 'extrinsic' dynamic processes that affect species' distributions, existence or persistence (mainly historical factors that include occurrence of bottlenecks, divergence events, or Quaternary expansions/retreats). Other traits that may influence genetic diversity patterns are the biogeographical affinities (boreal, temperate, etc.), and the historical and/or contemporary geographic range. Geographic range is known to be one of the major factors determining the levels of genetic variation of plant species on the basis of a series of meta-analyses. Perhaps the best known example is the compilation of Hamrick and Godt (1989), who gathered allozyme data from 653 studies (449 species representing 165 genera) at the global level and found that species with widespread ranges had significantly higher levels of genetic diversity than range-restricted ones. A further compilation of species studied by means of another codominant marker (microsatellites) yielded similar results (95 species; Nybom, 2004); in addition, a recent compilation carried out in the western Mediterranean Basin also reported significantly higher levels of allozyme diversity in widespread species compared to endemic ones (33 species; Lopez-Pujol et al., 2009).

These heterospecific (mixed species) compilations, despite having the advantage of including a large number of species, have been criticized for the absence of a congruent statistical approach. Given that life-history traits often show strong phylogenetic inertia (i.e., a tendency of close-related species to share them; Morales, 2000; Losos, 2008), analyzing the species independently (as is done in the abovementioned compilations) may lead to statistical pseudo-replication (Silvertown & Dodd, 1996; Aguinagalde et al., 2005). Although not as effective as using phylogenetically independent contrasts (Felsenstein, 1985), limiting comparisons to congeneric pairs would be a reliable alternative, as we can be quite confident that these share a more recent common ancestor than species in other genera (Silvertown & Dodd, 1996). Congeneric comparisons have been employed by Karron (1987), who compared 11 pairs of rare and widespread congeneric plants (48 species) in relation to their genetic diversity; in 10 pairs, rare species had lower genetic diversity than their widespread congeners. Later, Gitzendanner and Soltis (2000) performed a similar study with 36 congeneric pairs (107 taxa), generally obtaining lower diversity for rare species. More recently, Cole (2003) extended this approach to a total of 247 plant species representing 57 genera, with results similar to those reported by Gitzendanner and Soltis (2000).

Although they are not strictly comparisons between widespread and range- restricted species, those comparisons between threatened and non-threatened taxa can be regarded as a relatively accurate surrogate, given the well-known correlation between extent of species' range and extinction risk (e.g., Purvis et al., 2000; Payne & Finnegan, 2007; Cardillo et al., 2008). Indeed, geographic range plays a key role in listing species on the IUCN Red List, and for most of the cases it is the only criterion used to classify a given species as threatened (Gaston & Fuller, 2009). Spielman et al. (2004) compared the heterozygosity in 170 threatened/non-threatened pairs of taxa (taxonomically related but not necessarily congeneric), from which 36 were plant species. The authors found that in 27 pairs the threatened taxa had lower heterozygosity than the non-threatened ones.

Orchidaceae are one of the largest families of flowering plants (ca. 26,000 species; Chase et al., 2015). Considerable variation in life forms is known in the family, with approximately 30% of the species being terrestrial and the majority of the remainder growing as epiphytes or lithophytes (Gravendeel et ah, 2004). Orchids are also among the most endangered plant taxa (Pillon & Chase, 2007; Swarts & Dixon, 2009; Vogt-Schilb et ah, 2015; Zhang et ah, 2015); clearly, more attention is needed to preserve the biodiversity of wild orchids for several reasons. Many orchid species rely on a complex set of interactions with other organisms (e.g., the need of host trees for ephiphytes and mycorrhizal fungi for terrestrial orchids, or the existence of intricate pollination syndromes) for their survival (Bronstein et ah, 2014). These requirements make them extremely sensitive to environmental changes (Swarts & Dixon, 2009). Environmental human-mediated changes (e.g., deforestation, overharvesting, urbanization, changes in agricultural practices, trampling, pollution, soil disturbance, etc.) have been reported as the most important drivers for orchid decline (Swarts & Dixon, 2009, Liu et ah, 2014; Fay et ah, 2015; Vogt-Schilb et ah, 2015; but see Catling & Kostiuk, 2011 who found that trail disturbance benefited some wild orchids); in fact, orchids are often the first biological indicators of ecosystem decay (Roberts & Dixon, 2008). Direct impacts on orchids, such as mass collections by orchid hunters (because of their high commercial value), are of serious concern (Swarts & Dixon, 2009). The uses of orchids as ornamental, medicinal (especially in traditional Chinese medicine), and even alimentary plants (such as the salep in Iran) have brought many species to the brink of extinction in the wild (Ghorbani et ah, 2014; Liu et ah, 2015). In addition, orchids are typically characterized by small, spatially isolated populations (e.g., Vasquez et ah, 2003; Tremblay et ah, 2005; Phillips et ah, 2011), mainly a consequence of ecological specialization and low reproductive success (Roberts & Dixon, 2008); thus, orchid populations often have small effective population size, which makes them particularly susceptible to the effects of random genetic drift (Chung et ah, 2004a; Roberts & Dixon, 2008).

On the Korean Peninsula, 97 orchid species [103 taxa (species plus subspecies and varieties) in 42 genera] are known (Lee et ah, 2007; Lee, 2011). Thirty five and 48 species are listed as threatened by the Ministry of Environment (MOE, 2012, 2014) and Korea National Arboretum (KNA, 2012), respectively, which highlights the critical status of wild orchids in the Peninsula (Lee & Choi, 2006). As a part of a larger project on conservation biology on the Korean orchids, we have conducted allozyme studies in the Orchidaceae from South Korea since the mid-1990s; at present, genetic data on 32 taxa (31 species plus one variety; ca. one third of the Korean orchid flora) in 21 genera which are broadly representative of the Korean orchid flora (covering 11 out of 14 tribes in the four subfamilies) are available. In this study, we summarize current infonnation on allozyme-based genetic diversity in South Korean orchids. We also summarize the available genetic infonnation on congeners (of the studied Korean orchids) from other parts of the world, in order to get additional insights into the patterns of genetic diversity of Korean orchids and to provide insights into associations between rarity and genetic diversity in plants. Specific aims of the present study are the following; (i) to describe the patterns of genetic variability (within and among populations) of Korean orchids; (ii) to determine whether rare Korean orchids differ in the patterns of genetic diversity from common ones; (Hi) to see whether the empirical observation of lower genetic diversity for rare species compared to their widespread congeners is also applicable to our species' dataset, and (iv) to provide recommendations for the conservation of Korean orchids.

Materials and Methods

Data Collection

We gathered all published (and several unpublished) allozyme analyses of orchids in the Korean Peninsula. A total of 32 taxa (that are indicated by "S. Korea" after taxa names in Table 1) from Korea (plus Cymbidium goeringii in Japan) have been analyzed at the same laboratory by M. Y. Chung & M. G. Chung since the mid-1990s. In addition, studies of 37 congeneric taxa of the Korean orchids sampled from outside Korea (i.e., 37 taxa outside Korea), that were conducted at different laboratories, were included in this study to make comparisons between rare and common taxa (with a total of 46 entries; Table 1). Given that Goodyera repens was included in both datasets ('in' and 'outside' Korea; Table 1), a total of 68 taxa were considered in this study. For those studies from which allozyme data were reused for subsequent papers by the same authors, and for studies examining conspecific populations occurring on close locations, we only included data from a single study that involved the largest number of populations to avoid data duplication (Karron, 1987). On the contrary, all genetic data for widespread taxa examined on more than one occasion (e.g., Epipactis helleborine, G. repens) were included when these studies involved geographically very separated populations (i.e., from different countries).

In this work we followed plant names according to "The Plant List (2013)" except for Neolindleya (= Gymnadenia) camtschatica and Amitostigma gracile for which we used the names Galearis camtschatica and Hemipilia gracile provided by Jin et al. (2014) and Tang et al. (2015) based on molecular systematics studies, respectively (Table 1).

Designations of Rare Vs. Common Orchids

Although there is no widely accepted threshold or a definition by which a taxon is termed "rare" or "common", for Korean orchids we considered that a given taxon was rare if it was included in either Rare plants in Korea (KNA, 2012) or Korean Red List of Threatened Species (MOE, 2014) except for two species. The two newly recorded terrestrial orchids Habenaria dentata in Hapcheon County, Gyeongsangnam Province (Lee et al., 2013b) and Liparis pterosepala on Jeju Island (Lee et al., 2010) were not listed in KNA (2012) and MOE (2014), but they are extremely rare in South Korea. For other orchids outside the Korean Peninsula, we have mostly relied on authors' descriptions about abundance, population sizes or geographic ranges when included within papers. For example, in North America, as Cypripedium parviflorum is more ecologically diverse and shows a wider geographical distribution (although in many cases, local US populations are quite scattered and limited, and many populations have undergone dramatic declines) than its congeners C. arietinum, C. candidum, C. fasciculatum, C. kentuckiense, and C. reginae, we considered the former as "common" whereas the latter species were regarded as "rare" (Case, 1994; Aagaard et al., 1999; Kennedy & Walker, 2007). Although C. acaule is not as widely distributed as C. parviflorum, it is common in parts of the eastern US and Canada, and most populations remain stable in size and distribution (http://explorer.natureserve. org/servlet/NatureServe?searchName=Cypripedium+acaule).

When the information was not provided in the gathered studies, we referred to various sources of infonnation (e.g., http://www.efloras.org, http://www.iucnredlist.org, http://plants.usda.gov, or http://www.orchidspecies.com). It should be noted that, for the case of widespread species, they can be "common" in some parts of their distribution area but "rare" in others. This occurs in two cases: Cymbidium goeringii and Goodyera repens. As mentioned above, the former is relatively common in South Korea, but it is a rare orchid in Japan. In Japan C. goeringii was listed as critically endangered species in the 1997 list (EAJ, 2000), but later it was delisted in the 2012 list (EAJ, 2015). As in Japan it is a relatively rare species compared to southern Korea (mainly due to over-collection; M. Y. Chung & M. G. Chung, pers. obs.; T. Yahara, pers. comm.), we still consider it a rare orchid in the former country. In contrast, G. repens is extremely rare in South Korea (KNA, 2012), but it is common in NE Poland, where conifer forest communities suitable for this species are abundant (Brzosko et al., 2013; Table 1).

Data Analysis

As done by Hamrick and Godt (1989, 1996) and Godt and Hamrick (2001), standard parameters that describe genetic diversity and structure were extracted from these studies; these parameters include percent polymorphic loci (%P), mean number of alleles per locus (A), and gene or genetic diversity (i.e., Hardy-Weinberg expected heterozygosity, He). We used the subscripts "P" or "S" to denote population means or species' (or pooled samples) values, respectively. Since these values were not reported in all orchid studies, we calculated some of the measures (in particular measures at the species level) from allele frequency data provided in the papers. Following Hamrick and Godt (1989, 1996), we also compiled data on population structuring ([G.sub.ST] or [F.sub.ST]).

We compared levels of genetic diversity between rare orchids in Korea and their Common congeners if available. To do this, we averaged all entries for those taxa examined by different authors (e.g., Cephalanthera rubra, Cypripedium parviflorum var. pubescens and Epipactis helleborine) to obtain a single estimate per taxon. We thus obtained average values from rare taxa in South Korea and from their congeners (where more than one was available; e.g., Cypripedium)', in total, comparisons were possible for nine congeneric pairs (39 taxa; see the numbers 2, 4, 6, 7, 8, 10, 13, 15, and 19; Table 1) for this dataset.

Following Karron (1987) and Gitzendanner and Soltis (2000), we plotted each measure of diversity in rare taxa against that of the widespread congener. We further conducted Wilcoxon signed-rank tests between rare and common congeners for each genetic parameter to determine whether differences between two groups were statistically significant. We also performed a Spearman's rank correlation analysis between rare and common congeners for each measure; the higher correlation between the rare and common species for each genetic measure, the smaller the differences in the measurements between two groups.

As heterospecific comparisons, we compared rare Korean orchids (24 taxa or entries) with common ones (32 entries) provided in Table 1. To do this, we used a single entry per taxon by averaging all entries of the same taxa with the exception of Cymbidium goeringii and Goodyera repens. For the former, South Korean and Japanese ranges were treated as a common taxon and a rare one, respectively; for the latter South Korean and NE Polish ranges were treated as a rare taxon and a common one, respectively (Table 1). Similarly, we compared rare orchids (38 entries) with common ones (32 entries) provided in Table 1. We used a Wilcoxon rank-sum test (or Mann-Whitney (U-test) to assess the significance of differences in all measured parameters of diversity between rare and common taxa.

Results

Congeneric Comparisons

A different relationship for the levels of genetic diversity was observed between rare and common congeners (Fig. 1). The majority of the nine points on the graphs are away from the lines of equality (e.g., eight points for %Pp, Fig. la), indicating different levels of diversity in rare and common congeners. A very similar pattern was observed at the species level (data not shown). These visual interpretations were supported by the correlation analyses that showed that for all measures of genetic diversity, at both population and species levels, there was neither high nor significant correlation between rare species and their common congeners (Table 2). Indeed, for both population and species level estimates, Wilcoxon signed-rank tests revealed that rare species had significantly lower levels of genetic diversity than their common congeners (Table 2). We did not conduct statistical analysis for [G.sub.ST] or [F.sub.ST] values for the two groups because only data for three pairs were available (Table 1).

Heterospecific Comparisons

We expanded our analyses to mixed species (heterospecific) comparisons between rare (N = 24 in Korea and N = 38 in Korea plus other countries) and common orchids (N = 32) compiled in Table 1. For both population and species level values, Wilcoxon rank-sum tests showed that rare Korean orchids had significantly lower levels of genetic diversity than common orchids (all cases P < 0.0001; Table 3). A very similar result was found between rare orchids (N = 38) and common orchids (N - 32) (again all cases P < 0.0001; Table 3). Finally, mean values of [G.sub.ST] (or [F.sub.ST]) for rare orchids and common congeners did not differ significantly from each other [rare orchids in Korea (N = 13) vs. common orchids (N = 25), mean [G.sub.ST] = 0.169 vs. 0.194, P = 0.176; rare orchids (N = 22) vs. common orchids (N = 25), mean [G.sub.ST] = 0.189 vs. 0.194, P = 0.412; Table 3).

Discussion

Congeneric Comparisons

For both population and species level estimates, rare Korean orchid species have significantly lower levels of genetic diversity than their common congeners (Table 2), as expected (Karron, 1987; Gitzendanner & Soltis, 2000; Cole, 2003; see also Spielman et al., 2004). The only exception is the pair Cymbidium goeringiil C. kanran, a common and a rare species studied from Korea (Table 1). It is noteworthy that there is no allozyme-based genetic variation within and among populations in up to six Korean native rare species from our congeneric pairs dataset (Cephalanthera subaphylla, Cypripedium japonicum, Epipactis papillosa, Goodyera repens, Liparis pterosepala, and Oreorchis coreana) (Table 1), which significantly contributes to the observed differences for the pairwise comparisons. In addition, Bulbophyllum drymoglossum and Platanthera hologlottis show very low estimates of [H.sub.eP] (Table 1). As Chung et al. (2009) suggested, rare species with small population sizes (probably due to historical stochastic events) are susceptible to random genetic drift (RGD), leading to allelic fixation at many neutral loci within populations. Population genetic theory predicts that populations of species that have suffered RGD should exhibit low [H.sub.eP] and high [G.sub.ST] due to the fixation of alternative alleles (e.g., Barrett & Kohn, 1991; Ellstrand & Elam, 1993). Although allozyme- based [G.sub.ST] estimates are not available in the six abovementioned species (as these are monomorphic), the other two species showing low levels of [H.sub.eP] (Bulbophyllum drymoglossum and Platanthera hologlottis) have moderate GSJ (0.253 and 0.328, respectively; Table 1). In addition, low levels of microsatellite-based within- population genetic variation (%[P.sub.P] = 35; [A.sub.P] = 1.53; [H.sub.ep] = 0.109 based on 10 polymorphic loci) but a much higher among-population divergence ([[PHI].sub.ST] = 0.81 including one Japanese population) have been detected in South Korean populations of Cypripedium japonicum (Son & Son, 2016). The low [H.sub.ep] values and the high [[PHI].sub.ST] values support the role played by RGD in shaping the patterns of genetic diversity of some rare Korean orchids.

One of the best examples where rarity reflects the lack of allozyme diversity is probably that of Goodyera repens in South Korea. This species is widely distributed in Asia, Europe, and North America (Chen et al., 2001) and may represent a relictual descendant of an alpine community that was more widespread during the late Pleistocene (Kallunki, 1976). Unlike Korean populations (that are monomorphic in three populations; Table 1), 11 populations from NE Poland maintain high levels allozyme diversity (%[P.sub.P] = 50; [A.sub.P] = 1.68; [H.sub.ep] = 0.197; Table 1; Brzosko et al., 2013); the authors attributed its common occurrence under pine and spruce forests as the main factor shaping levels of genetic diversity of Polish populations. Thus, lack of allozyme diversity of G. repens in three alpine Korean populations might be attributable to its rarity in the country [it is a species listed as "vulnerable" by MOE (2012, 2014) and "critically endangered" by KNA (2012) with only 10 populations occurring throughout Korea],

Oreorchis coreana is another example of a very rare species in Korea, as it is found in a small area on Jeju Island and has only five low-density populations (MOE, 2014). It shows no genetic variation, in contrast to its close congener O. patens, a common orchid in East Asia that in Korea has high levels of genetic diversity (Chung et al., 2012 and Table 1). Oreorchis coreana was considered in the past endemic to Jeju Island, but it also occurs in Nasushiobara City, Tochigi Prefecture. Honshu (Japan) (Takashima et al., 2016). Unlike on Jeju Island, only ca. 10 individuals in a single population are known in Honshu. Although the levels of genetic diversity for the Nasushiobara population have not been surveyed, one would expect a lack of allozyme diversity in this population because there is no sequence divergence in the ITS regions between Jeju and Nasushiobara populations. This finding also suggests that the Japanese population is probably the result of recent long-distance dispersal from Jeju Island rather than an old relict population separated via vicariance (Takashima et al., 2016).

Finally, it should be also taken into account that a formerly common species could have become recently rare (e.g., due to over-collection by orchid hunters), a situation that has often been reported for orchids (Swarts & Dixon, 2009; Vogt-Schilb et al., 2015; Zhang et al., 2015). However, when population reduction has taken place recently (e.g., several decades ago), little alteration in the levels of genetic diversity occurs because there have not been sufficient generations for the initial diversity to be substantially eroded by RGD (Chung et al, 2004a). Moreover, if population size reduction has been at random regarding individual genotypes, the loss of genetic variation should be even more limited (Chung & Chung, 1999). Thus, rare species that were formerly common but with most of their populations recently decimated [and, hence, that were treated as "rare" by KNA (2012) and/or MOE (2012, 2014)] might exhibit comparable levels of genetic diversity to common ones [e.g., Cymbidium goeringii in Japan (Chung & Chung, 2000); C. kanran on Jeju Island (M. Y. Chung et al., unpubl. data); Cypripedium macranthos in South Korea (Chung et al., 2009); Table 1].

Heterospecific Comparisons

Regarding heterospecific (mixed species of orchids) comparisons, the rare orchids--regardless of being Korean or not--have significantly lower levels of genetic diversity than the common orchids at both population and species levels, with the exception of a few cases (Tables 1 and 3). Such results agree with former compilations and meta-analyses of heterospecific data (e.g., Hamrick & Godt, 1989, 1996; Godt & Hamrick, 2001; Nybom, 2004; Lopez-Pujol et al., 2009) and also with our congeneric comparisons.

It should be noted that a total lack of allozyme diversity is found in 10 (ca. 42%) of 24 rare orchid species in South Korea [similarly, 14 (ca. 37%) out of 38 rare orchids provided in Table 1]. This observation may result from rarity associated with RGD. As seen in the two rare orchids Bulbophyllum drymoglossum and Platanthera hologlottis, Pelatantheria scolopendrifolius and Pogonia minor exhibit low [H.sub.eP] and moderate to high Gsx values, suggesting that populations of these species were historically rare; this pattern of genetic diversity would be the natural result of continued RGD (Barrett & Kohn, 1991). Another scenario, which is not mutually exclusive with the former, is more related to historical events. Quaternary climatic cycles can often leave a distinctive signature on levels of genetic diversity found within populations or species (Hewitt, 1996, 2000; Soltis et al., 2006; Qiu et al., 2011). Wann-temperate plant elements on the Korean Peninsula, currently limited to southern coastal areas, shifted southwards during the Last Glacial Maximum (LGM, ca. 21,000 yrs. before present) towards glacial refiagia putatively located in southern portions of Jeju Island, southern Japan, and/or southern China (Chung et al., 2013b; Lee et al, 2013a, 2014; Chung et al., 2017). The low [H.sub.eP] found in the five warm-temperate orchid species (Bletilla striata, Habenaria dentata, Pecteilis radiata, Peristylus densus, and Tipularia japonica, Table 1) might be due to founder effects during post-glacial re-colonization from a single source population (Chung et al., 2013c); a pattern of continued small size over time of founding populations would enhance the loss of genetic diversity by processes of RGD (Frankham et al., 2002; Templeton, 2006).

The Baekdudaegan (BDDG, the main mountain system of the Korean Peninsula) served as a glacial refugium for a large assemblage of boreal and temperate plants during the LGM (Chung et al., 2017). In many cases (with the exception of Goodyera repens), plants from the BDDG maintain moderate to high levels of within- population genetic diversity (Table 3; see also Table 1 in Chung et al, 2017) because these mountains might provide relatively stable habitats, ensuring relatively large population sizes. Species belonging to this scenario might include Cypripedium macranthos, Galearis cyclochila, Liparis makinoana, and Oreorchis patens in South Korea (Chung et al., 2005a, 2005b, 2009, 2012; Chung, 2009a). Neottianthe cucullata, in spite of being located in the BDDG, has low levels of within-population allozyme variation, which might be due to a relatively small scale of sampling (four populations were collected within a 1.2-km linear distance; Chung, 2009a). A total lack of allozyme diversity was also found in the autogamous Liparis kumokiri in South Korea, a common orchid that occurs on lowlands (K. Suetsugu, pers. comm.). In contrast, the self-incompatible and genetically-diverse congener L. makinoana mostly occurs in the BDDG and its vicinity (Oh et al., 2001), which illustrates the role of these mountains in preserving the genetic diversity of plant species.

There are five rare taxa in South Korea (Calanthe discolor, C. reflexa, C. sieboldii, Cremastra appendiculata var. variabilis, and Galearis cyclochila) and Cypripedium macranthos var. rebunense (endemic to Rebun Island, Japan) that, unexpectedly, exhibit moderate to high levels of genetic variation within populations (Table 1). Like Cymbidium kanran on Jeju Island, the three Calanthe species have been the target of orchid collectors during the past several decades (Chung et al., 2013d). As explained above, recent negative effects (i.e., human-mediated disturbance) could not have altered levels of genetic diversity in remnant populations. Even though their distributions are relatively narrow, locally common populations could maintain moderate levels of genetic variation. All these species, in addition to Cypripedium macranthos in South Korea and Cymbidium goeringii in Japan, appear to belong to this category.

As heterospecific comparisons, our mean estimates (N = 68) of genetic diversity for orchids are similar to those (N = 32 and 16, respectively) compiled by Case (2002) and Hamrick and Godt (1996) (Table 3), which are also comparable to the average values for all plants (N = 725: Hamrick & Godt, 1989), narrowly distributed plants (N = 101; Hamrick & Godt, 1989), short-lived herbaceous plants (N = 152; Hamrick & Godt, 1989), plants with outcrossing-animal breeding system (N = 172, Hamrick & Godt, 1989), rare plants in the southeastern US (N = 52; Godt & Hamrick, 2001), and plants from NW Mediterranean Basin (N = 36; Lopez-Pujol et al., 2009), but somewhat higher than endemic plants (N = 81, Hamrick & Godt, 1989) (Table 3).

The degree of genetic differentiation among populations of orchids was once controversial (Forrest et al., 2004), due to the low mean value reported in one of the few meta-analyses available at that time ([G.sub.ST] = 0.087, N= 16; Hamrick & Godt, 1996). Our mean ([G.sub.ST] = 0.190, N = 68) is comparable, nevertheless, to those averaged by most of the previous studies ([G.sub.ST] = 0.146, 0.161, and 0.163; Phillips et al., 2012; Forrest et al., 2004; Case, 2002, respectively) (Table 3). The slightly higher [G.sub.ST] value estimated in this study is partly due to the inclusion of Pelatantheria scolopendrifolius ([G.sub.ST] = 0.899; Chung et al., 2007a) and Hemipilia gracile ([G.sub.ST] = 0.781; Chung, 2009a), two orchids with disproportionate levels of genetic differentiation. The lack of significant differences in the mean [G.sub.ST] values between rare and common orchids from our datasets are in agreement with the study of Hamrick and Godt (1989) for plants in general. However, Phillips et al. (2012) found that rare terrestrial orchid species had significantly higher population genetic differentiation than common ones (mean rare [F.sub.ST] = 0.279, N - 13; mean common [F.sub.ST] = 0.092, N = 22; Mann-Whitney U-test, P = < 0.001). These differences among studies might be due to different criteria for choosing papers for the meta-analyses and perhaps also different criteria for classifying species into rare and common (Phillips et al., 2012). We further test whether our results would change when six rare species of our dataset (that were formerly common but with most of their populations recently decreased) were considered, instead, as common ones (e.g., three Calanthe species, Cremastra appendiculata var. variabilis, Cymbidium goeringii in Japan, and Cypripedium macranthos); again, we did not detect significant differences between the groups regarding [G.sub.ST] (data not shown).

Conservation Implications for Rare Orchids in Korea

There are two main "hotspots" of orchids on the Korean Peninsula regarding species richness; the BDDG (that stretches ca. 1625 km), in which 40 taxa (38.8% of total orchids) occur, and Jeju Island (1848 [km.sup.2], also a tourist hotspot), where 60 taxa (58.3%) can be found (Lee, 2011). Jeju Island is, however, much more significant as a hotspot for threatened species; for example, of the 48 orchid species designated by Korea National Arboretum (KNA) in 2012 as rare/threatened plants (KNA, 2012), 37 occur on Jeju, whereas only seven are found on the main ridge (or in the immediate vicinity) of the BDDG. A similar trend is found in the Korean Red List of Threatened Species (MOE, 2014); out of 35 threatened orchid species, only five occur on the main ridge of the BDDG or its vicinity, whereas 29 grow on Jeju.

The BDDG has a high floristic richness of over 1500 taxa just in South Korea (Lim, 2003). It is mainly covered by temperate deciduous forests (with Quercus mongolica and Pinus densiflora as dominant species) in its southern and central sections, whereas mixed forests (Abies, Betula, Pinus, Tilia, Ulmus) are common in its northern section (Yi, 2011). Under relatively stable habitats along the BDDG, many plant species might have persisted with large population sizes and consequently maintained moderate to high levels of genetic diversity (Chung & Chung, 2014; Chung et al., 2017). This may partly account for why in the BDDG there are relatively few threatened orchid species. The floristic richness of the BDDG as well as its role as a Pleistocene glacial refugium has stressed the need to ensure effective and integral conservation of this mountain range. Although these mountains remain relatively well preserved, some conservation measures have been already undertaken, whereas others have been suggested in detail in Chung et al. (2016, 2017), including enlarging the current network of protected areas, stopping of deforestation activities (especially worrisome in North Korea), and increasing cooperation between the two Koreas.

Jeju Island was on the "crossroads" of several post-glacial colonization routes, consequently harboring different floristic elements including subtropical, temperate, boreal, and arctic-alpine species (Kong & Watts, 1993; Dolezal et al., 2012; Chung et al., 2013b). Currently, Jeju harbors 1990 taxa of vascular plants (Kim, 2009), with about 13% of native Korean orchid species exclusively occurring here (Lee, 2011). Some of the reasons why Jeju has many rare orchids might be due to the island's relatively small area (less than 2000 [km.sup.2]) and/or recent plant immigration (colonization) by a single or few dispersal events from adjacent regions (perhaps, from southern Japan; Eum et al., 2011). Fortunately, Hallasan National Park (1950 m at peak) has been designated as an UNESCO Biosphere Reserve (covering 830.94 [km.sup.2]; Chung & Hwang, 2015) in 2002, and a World Heritage Site in 2007, for its pristine environments, unique altitudinal zonation of vegetation and high endemism (Kong & Watts, 1993; Dolezal et al., 2012). In addition, five wetlands have been included on the list of Ramsar Wetlands (http://www.ramsar.org/wetland/republic-of-korea), and the whole island was recognized as an UNESCO Global Geopark in 2010 (Chung & Hwang, 2015). Although the biosphere reserve--that represents ca. 45% of the total land area of Jeju--is well preserved, large destruction is taking place in the low peripheral areas of Gotjawal, a forest often called the "lung" of Jeju (Kang et al., 2013), while several development projects (including the construction of a new airport, resorts and residential complexes; Bridger, 2016) have been planned. To protect and conserve plants and animals, further expansion of the biosphere reserve to the whole island has been suggested (Chung & Hwang, 2015).

To our best knowledge, this study is the first to summarize levels of genetic diversity focusing on the Korean orchids, although it also includes data from several orchid species outside the Korean Peninsula. As Godt and Hamrick (2001) stressed, empirical genetic studies of rare plants can provide insights that may guide conservation and management plans. We found that 24 rare Korean orchids maintain significantly lower within- population genetic variation than their common congeners and common orchid species at the global level. Of particular concern, we found that ten species exhibit a total lack of allozyme genetic diversity (Cephalanthera subaphylla, Cypripedium japonicum, Epipactis papillosa, Goodyera repens, Habenaria dentata, Liparis pterosepala, Oreorchis coreana, Pecteilis radiata, Peristylus densus, and Tipularia japonica; Table 1). In addition, other six species (Bletilla striata, Galearis cyclochila, Neottianthe cucullata, Pelatantheria scolopendrifolius, Platanthera hologlottis, and Pogonia minor, Table 1) also harbor extremely low levels of within-population genetic variation.

Based on the genetic data presented here, conservation priority should be given to rare orchid species on the Korean Peninsula. Particularly, special attention should be paid to Jeju, as a large part of the orchids that exhibit low levels of genetic diversity occur on this island (Cephalanthera subaphylla, Goodyera repens, Liparis pterosepala, Oreorchis coreana, Pelatantheria scolopendrifolius, Peristylus densus, Platanthera hologlottis, Pogonia minor, and Tipularia japonica). One of these species is endemic to Jeju (Liparis pterosepala), another is quasi-endemic (Oreorchis coreana), and a third species' Korean occurrences are restricted to Jeju (Peristylus densus). In addition, the rare terrestrial orchid Nervilia nipponica (formerly known as an endemic orchid to southern Japan) was newly recorded on Jeju (Kim et al., 2009), exhibiting extremely low levels of nrDNA genetic diversity (Eum et al., 2011). We recommend periodic monitoring of the rare orchid species on Jeju to detect any declining trend in their populations.

Another take-home message from this study is that the results of genetic analyses of several orchid species (e.g., three Calanthe species, Cymbidium kanran, Cypripedium macranthos, Galearis cyclochila, Liparis kumokiri, etc.) could not have been predicted based on generalizations from the allozyme literature or on analyses of congeneric species with similar life history traits, again stressing the importance of empirical genetic studies (Godt & Hamrick, 2001). Such genetic studies would also be important to elucidate the evolutionary trajectories of rare and endangered orchids on the Korean Peninsula (including Jeju), especially if conspecific populations from adjacent countries are included. In addition, these studies are essential to design tailored conservation measures. For example, in the specific case of warm-temperate orchids, individuals from their colonization sources (e.g., the former LGM refugial areas in southeastern Japan) could be used as source populations for their in situ (reinforcement and reintroduction) or ex situ conservation, if genetic analyses demonstrate that they are genetically similar to the Korean populations (as combining two genetically- divergent populations may result in outbreeding depression; Fenster & Dudash, 1994).

Future Perspectives

In future studies, some issues on how natural and/or artificial habitat (population) fragmentation and gene flow (or lack of) impact the genetic diversity and demography of rare orchid species and also how global warming may impact some of these species must be studied in depth (Liu et al, 2010; Chung et al., 2014). In fact, recent studies have shown that many orchids are extremely susceptible to habitat destruction or disturbance compared to other plants because they have "above" and "below" ground limitations (i.e., pollinator specialization, limited recruitment, and mycorrhizal specificity; Cozzolino & Widmer, 2005; Waterman et al.. 2011; McCormick & Jacquemyn, 2014). Thus, in parallel to genetic and phylogeographic surveys, long-term ecological studies (e.g., minimum viable population size and demographic dynamics, extent of seed dispersal, pollination biology and ecology, seed gennination ecology, association of mycorrhizal fungi, processes of colonization and population growth) are also necessary before effective conservation strategies can be designed and implemented. Unfortunately, this suggestion is critical because only a few such works focused on Korean orchids are available to date.

https://doi.org/10.1007/s12229-017-9190-5

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, Dermis Whigham, Dorset Trapnell, Ken Cameron, Hans Jacquemyn, Chris Wilcock, and Mary Ruth Nciland, 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 1m, Masayuki Maki, Naoto Sugiura, Tadashi Yamashiro, Takayuki Kawahara, Kenji Suctsugu, Kaoru Tsuji, Huai Zhcn 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, NRF2013R1A1A3010892, 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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Mi Yoon Chung (1) * Jordi Lopez-Pujol (2) * Sungwon Son (3) * Gang Uk Suh (3) * Tomohisa Yukawa (4) * Myong Gi Chung (1,5)

(1) Division of Life Science and the Research Institute of Natural Science, Gyeongsang National University, Jinju 52828, Republic of Korea

(2) BioC-GReB, Botanic Institute of Barcelona (IBB-CSIC-ICUB), Passeig del Migdia s/n, 08038 Barcelona, Spain

(3) Plant Conservation Division, Korea National Arboretum, Pocheon 11186, Republic of Korea

(4) Tsukuba Botanical Garden, National Museum of Nature and Science, Tsukuba 305-0005. Japan

(5) Author for Correspondence; e-mail: mgchung@gnu.ac.kr Published online: 31 October 2017

Caption: Fig. 1 Plots of genetic variation in rare Korean orchid species vs. their common congeners (nine pairs) at the population level. The line in each graph represents the portion of the graph where rare and common congeners have the same levels of genetic parameters.(%[P.sub.P]; [A.sub.p], [H.sub.eP]
Table 1 Comparisons of Allozyme-Based Genetic Diversity and Genetic
Differentiation for Orchids in South Korea (Bold Faced) and their
Available Congeners. The number in the Column Represents an
Alphabetic Order of 21 Genera

Species (country sampled) (R/C) (a)          Ecol. Affinity (b)/
                                             Range (c) (R/C) (d)

1. Bletilla striata (S. Korea) (R)           WT/CSC, MY, SJ, SK (R)
2. Bulbophyllum diymoglossum                 WT/SC, SJ, SK, TW (R)
   (S. Korea) (R)
   B. adiamantinum (Brazil) (C)              TR/ BR (C)
   B. bidentatum (Brazil) (C)                TR/ BR (C)
   B. epiphytum (Brazil) (C)                 TR/ BR (C)
   B. exaltatum (Brazil) (C)                 TR/ BR, GU, VE (C)
   B. insectiferum (Brazil) (C)              TR/ BR (C)
   B. involution (Brazil) (C)                TR/ BR (C)
   B. plumosum (Brazil) (C)                  TR/ BR (C)
   B. regnellii (Brazil) (C)                 TR/ BR (C)
   B. rapicola (Brazil) (C)                  TR/ BR (C)
   B. sanderianum (Brazil) (C)               TR/ BR (C)
   B. weddellii (Brazil) (C)                 TR/ BR (C)
3. Calanthe discolor (S. Korea) (R)          WT/CSC, SJ, SK (C)
   C. reflexa (Jeju Is. in S. Korea) (R)     WT/CSC, JJ, MY, SJ,
                                             TW (C)
   C. sieboidii (S. Korea) (R)               WT/HU, RY, SK, TW (C)
4. Cephaianthera longibracteata              T/K, J, NEC (C)
      (S. Korea) (C)
   C. subaphyila (S. Korea) (R)              B, T/BH, EH, K, J,
                                             NEC, RFE (R)
   C. damasonium (C. Italy) (C)              T, WT/BH, EU, IN, MY,
                                             NWY, SWA (C)
   C. longifolia (C. Italy) (C)              B, T/BH, CC, EU, IN,
                                             KAS, MY, NAF, NE,
                                             PA, SWA, SWC (C)
   C. rubra (C. Italy) (C)                   T/EU to CEA (C)
   C. rubra (NE Poland) (C)
5. Cremastra appendiculata var.              T, WT/CSC, J, SK, NV,
     variahilis (S. Korea) (R)               TH (C)
6. Cymbidium goeringii (S. Korea) (C)        WT/BH, CSC, J, SK, TW,
   C. goeringii (Japan) (R)                  NWI (C)
   C. kanran (Jeju Is. in S. Korea) (R)      WT/SC, SJ, TW (R)
7. Cypripedium japonicum (S. Korea) (R)      T/CSC, J, K (R)
   C. macranthos (S. Korea) (R)              B/J, K, NEC, R. TW (C)
   C. macranthos var. rebunense              B/RI (R)
     (Rebun Is. in Japan) (R)
   C. acaule (Michigan, USA) (C)             B, T/CEC, EUS (C)
   C. arietinum (Michigan, USA) (R)          B, T/CEC, GL, NEUS (R)
   C. calceolus (Poland) (C)                 B, T/EU, J, NEC, NK,
                                             R (C)
   C. candidum (Michigan, USA) (R)           B, T/MWUS (R)
   C. fasciculatum (Washington, USA) (R)     T/WUS (R)
   C. kenluckiense (Arkansa, Oklahoma,       T/SUS (R)
      Texas, Virginiain USA) (R)
   C. parvijlorum var. makasin (Indiana,     B. T/NECA, NUS,
      Michigan in USA) (C)                   SUNA (C)
   C. parvijlorum (Georgia, Missouri,        T/SEUS (C)
      Oklahoma, Virginia in USA) (C)
   C. parviflorum var. pubescens             B, T/CAN, EUS,
      (northern form) (Illinois, Indiana,    SUNA (C)
      Michigan, Ohio in USA) (C)
   C. parviflorum var. pubescens             T/SEUS (C)
      (southern form) (SE USA, Ohio in
      USA) (C)
   C. regime (Michigan, USA) (R)             B, T/CEC, EUS (R)
   C. regime (SE USA, Ohio in USA) (R)
      Epipactis thunbergii (S. Korea) (C)    T, WT/EZ, J, SK (C)
8. E. papillosa (S. Korea) (R)               T/ J, K, SLF (R)
   E. atrorubens(NE Poland) (R)              B, T/EU, ES, CEA (C)
   E. helleborine (NE Poland) (C)            T/EUA, CEA to J (C)
   E. helleborine (Scotland, England) (C)
   E. helleborine (Belgium, Denmark,
      England, France, Germany, Scotland,
      Switzerland) (C)
   E. helleborine (Canada,
      naturalized) (C)
   E. helleborine (C. Italy) (C)
   E. helleborine (Denmark) (C)
   E. leptochila (Scotland, England) (C)     T/WEU (C)
   E. microphylla (C. Italy) (R)             T/EUA (R)
   E. palustris (C. Italy) (R)               B/CIB (R)
   E. phyllanthes (Denmark) (R)              T/WEU (R)
   E. phyllanthes (Scotland, England) (R)
   E. purpurata (Denmark) (R)                T/WEU (R)
9. Galearis (Orchis) cyclochila (S.          B/J, K, NEC, NEQ,
   Korea) (R)                                R (C)
   G. (Gymnadenia) camtschatica (Ulleung     B/J, K, NEC, RFE (C)
       Is. in S. Korea) (R)
10. Goodyera rosulacea (S. Korea) (C)        T/SK (C)
    G. repens (S. Korea) (R)                 B/BH, C, EU, IN, J, K,
                                             KAS, MY, NA, NE, R,
                                             TW (C)
    G. repens (NE Poland) (C)
    G. procera (Hong Kong) (C)               TR, WT/BA, BH, CA, HA,
                                             IN, IND, LA, MY,
                                             NE, PH, RY, SC, SR,
                                             TH, TW, VI, YT (C)
11. Habenaria Jentata (S. Korea) (R)         T, WT. TR/CA, IN, LA,
                                             MY, NE, SC, SJ,
                                             SK, TH, TW, VI (C)
12. Hemipilia (Amitostigma) gracile          T/CSC, J, K, TW (R)
    (S. Korea) (C)
13. Liparis kumokiri (S. Korea) (C)          B, T/J, K, RFE (C)
    L. makinoana (S. Korea) (C)              B, T/J, K, RFE (C)
    L. pterosepala (Jcju Is., S.             WT/JJ (R)
    Korea) (R)
14. Neottianthe (Gymnadenia) cucullata       B. T, WT/BH, C, EEU,
    (S. Korea) (R)                           J, K, MO, NE. R (C)
15. Oreorchis patens (S. Korea) (C)          B/C, J, K, RFE, TW (C)
    O. coreana (Jeju Is. in S. Korea) (R)    WT/JJ, SJT (R),
16. Pecteilis (Habenaria) radiata            T, WT/SK, J, WH (R)
    (S. Korea) (R)
17. Pelatantheria (Sarcanthus)               WT/CC, SJ, SK (R)
    scolopendrifolius (S. Korea) (R)
18. Peristylus densus (Jeju Is.) (R)         WT/JJ, SJ (R)
    (= Habenaria flagellifera)
19. Platanthera hologlattis                  B/C, J, K, RFE (C)
    (S. Korea) (R)
    P. leucophaea (NE USA) (R)               T/NEUS (R)
    P. chlorantha (NE Poland) (R)            B, T/C, J, K, R, WA,
                                             EU (C)
    P. bifolia (NE Poland) (C)               B, T/ EUA (C)
20. Pogonia minor (S. Korea) (R)             T, TR, WT/J, SK,
                                             ST (C)
21. Tipularia japonica (S. Korea) (R)        WT/SK, SJ(R)

Species (country sampled) (R/C) (a)          GF (e)   NP (f)

1. Bletilla striata (S. Korea) (R)           T        16
2. Bulbophyllum diymoglossum                 E, L     2
   (S. Korea) (R)
   B. adiamantinum (Brazil) (C)              E, R     2
   B. bidentatum (Brazil) (C)                R        1
   B. epiphytum (Brazil) (C)                 E        2
   B. exaltatum (Brazil) (C)                 E, R     20
   B. insectiferum (Brazil) (C)              R        1
   B. involution (Brazil) (C)                R        7
   B. plumosum (Brazil) (C)                  E        4
   B. regnellii (Brazil) (C)                 E        1
   B. rapicola (Brazil) (C)                  R        1
   B. sanderianum (Brazil) (C)               R        2
   B. weddellii (Brazil) (C)                 R        4
3. Calanthe discolor (S. Korea) (R)          T        9
   C. reflexa (Jeju Is. in S. Korea) (R)     T        2

   C. sieboidii (S. Korea) (R)               T        3
4. Cephaianthera longibracteata              T        3
      (S. Korea) (C)
   C. subaphyila (S. Korea) (R)              T        2

   C. damasonium (C. Italy) (C)              T        13

   C. longifolia (C. Italy) (C)              T        3

   C. rubra (C. Italy) (C)                   T        7
   C. rubra (NE Poland) (C)                  T        9
5. Cremastra appendiculata var.              T        12
     variahilis (S. Korea) (R)
6. Cymbidium goeringii (S. Korea) (C)        T        16
   C. goeringii (Japan) (R)                  T        7
   C. kanran (Jeju Is. in S. Korea) (R)      T        1
7. Cypripedium japonicum (S. Korea) (R)      T        6
   C. macranthos (S. Korea) (R)              T        4
   C. macranthos var. rebunense              T        5
     (Rebun Is. in Japan) (R)
   C. acaule (Michigan, USA) (C)             T        4
   C. arietinum (Michigan, USA) (R)          T        4
   C. calceolus (Poland) (C)                 T        32

   C. candidum (Michigan, USA) (R)           T        5
   C. fasciculatum (Washington, USA) (R)     T        3
   C. kenluckiense (Arkansa, Oklahoma,       T        8
      Texas, Virginiain USA) (R)
   C. parvijlorum var. makasin (Indiana,     T        8
      Michigan in USA) (C)
   C. parvijlorum (Georgia, Missouri,        T        8
      Oklahoma, Virginia in USA) (C)
   C. parviflorum var. pubescens             T        12
      (northern form) (Illinois, Indiana,
      Michigan, Ohio in USA) (C)
   C. parviflorum var. pubescens             T        12
      (southern form) (SE USA, Ohio in
      USA) (C)
   C. regime (Michigan, USA) (R)             T        3
   C. regime (SE USA, Ohio in USA) (R)       T        9
      Epipactis thunbergii (S. Korea) (C)    T        8
8. E. papillosa (S. Korea) (R)               T        8
   E. atrorubens (NE Poland) (R)             T        4
   E. helleborine (NE Poland) (C)            T        5
   E. helleborine (Scotland, England) (C)    T        13
   E. helleborine (Belgium, Denmark,         T        35
      England, France, Germany, Scotland,
      Switzerland) (C)
   E. helleborine (Canada,                   T        12
      naturalized) (C)
   E. helleborine (C. Italy) (C)             T        4
   E. helleborine (Denmark) (C)              T        13
   E. leptochila (Scotland, England) (C)     T        2
   E. microphylla (C. Italy) (R)             T        2
   E. palustris (C. Italy) (R)               T        1
   E. phyllanthes (Denmark) (R)              T        6
   E. phyllanthes (Scotland, England) (R)    T        2
   E. purpurata (Denmark) (R)                T        5
9. Galearis (Orchis) cyclochila (S.          T        2
   Korea) (R)
   G. (Gymnadenia) camtschatica (Ulleung     T        4
       Is. in S. Korea) (R)
10. Goodyera rosulacea (S. Korea) (C)        T        7
    G. repens (S. Korea) (R)                 T        3

    G. repens (NE Poland) (C)                T        11
    G. procera (Hong Kong) (C)               T        15

11. Habenaria Jentata (S. Korea) (R)         T        1

12. Hemipilia (Amitostigma) gracile          L        17
    (S. Korea) (C)
13. Liparis kumokiri (S. Korea) (C)          T        17
    L. makinoana (S. Korea) (C)              T        4
    L. pterosepala (Jcju Is., S.             T        2
    Korea) (R)
14. Neottianthe (Gymnadenia) cucullata       T        4
    (S. Korea) (R)
15. Oreorchis patens (S. Korea) (C)          T        12
    O. coreana (Jeju Is. in S. Korea) (R)    T        4
16. Pecteilis (Habenaria) radiata            T        1
    (S. Korea) (R)
17. Pelatantheria (Sarcanthus)               E, L     3
    scolopendrifolius (S. Korea) (R)
18. Peristylus densus (Jeju Is.) (R)         T        1
    (= Habenaria flagellifera)
19. Platanthera hologlattis                  T        3
    (S. Korea) (R)
    P. leucophaea (NE USA) (R)               T        7
    P. chlorantha (NE Poland) (R)            T        6

    P. bifolia (NE Poland) (C)               T        14
20. Pogonia minor (S. Korea) (R)             T        11

21. Tipularia japonica (S. Korea) (R)                 8

Species (country sampled) (R/C) (a)          Genetic parameter (g)

                                             %[P.sub.S]   %[P.sub.P]

1. Bletilla striata (S. Korea) (R)           15.0         12.8
2. Bulbophyllum diymoglossum                 4.8          2.4
   (S. Korea) (R)
   B. adiamantinum (Brazil) (C)              100.0        92.9
   B. bidentatum (Brazil) (C)                100.0        100.0
   B. epiphytum (Brazil) (C)                 100.0        92.7
   B. exaltatum (Brazil) (C)                 100.0        66.1
   B. insectiferum (Brazil) (C)              92.9         92.9
   B. involution (Brazil) (C)                100.0        69.9
   B. plumosum (Brazil) (C)                  100.0        92.9
   B. regnellii (Brazil) (C)                 92.9         92.9
   B. rapicola (Brazil) (C)                  100.0        100.0
   B. sanderianum (Brazil) (C)               66.7         38.9
   B. weddellii (Brazil) (C)                 77.8         47.2
3. Calanthe discolor (S. Korea) (R)          88.2         68.6
   C. reflexa (Jeju Is. in S. Korea) (R)     47.1         47.1

   C. sieboidii (S. Korea) (R)               76.5         66.7
4. Cephaianthera longibracteata              30.0         18.0
      (S. Korea) (C)
   C. subaphyila (S. Korea) (R)              0.0          0.0

   C. damasonium (C. Italy) (C)              0.0          0.0

   C. longifolia (C. Italy) (C)              55.6         48.1

   C. rubra (C. Italy) (C)                   66.7         33.3
   C. rubra (NE Poland) (C)                  53.9         13.9
5. Cremastra appendiculata var.              50.0         48.1
     variahilis (S. Korea) (R)
6. Cymbidium goeringii (S. Korea) (C)        71.0         63.0
   C. goeringii (Japan) (R)                  71.4         62.2
   C. kanran (Jeju Is. in S. Korea) (R)      66.7         66.7
7. Cypripedium japonicum (S. Korea) (R)      0.0          0.0
   C. macranthos (S. Korea) (R)              50.0         46.7
   C. macranthos var. rebunense              62.0         60.4
     (Rebun Is. in Japan) (R)
   C. acaule (Michigan, USA) (C)             46.2         34.7
   C. arietinum (Michigan, USA) (R)          0.0          0.0
   C. calceolus (Poland) (C)                 54.6         36.4

   C. candidum (Michigan, USA) (R)           66.7         38.3
   C. fasciculatum (Washington, USA) (R)     25.0         19.5
   C. kenluckiense (Arkansa, Oklahoma,       25.0         12.5
      Texas, Virginiain USA) (R)
   C. parvijlorum var. makasin (Indiana,     81.8         69.3
      Michigan in USA) (C)
   C. parvijlorum (Georgia, Missouri,        54.5         35.2
      Oklahoma, Virginia in USA) (C)
   C. parviflorum var. pubescens             81.8         65.2
      (northern form) (Illinois, Indiana,
      Michigan, Ohio in USA) (C)
   C. parviflorum var. pubescens             81.8         50.8
      (southern form) (SE USA, Ohio in
      USA) (C)
   C. regime (Michigan, USA) (R)             18.2         15.2
   C. regime (SE USA, Ohio in USA) (R)       10.0         7.8
      Epipactis thunbergii (S. Korea) (C)    4.3          3.8
8. E. papillosa (S. Korea) (R)               0.0          0.0
   E. atrorubens (NE Poland) (R)             9.1          9.1
   E. helleborine (NE Poland) (C)            40.9         32.7
   E. helleborine (Scotland, England) (C)    na           33.2
   E. helleborine (Belgium, Denmark,         na           55.0
      England, France, Germany, Scotland,
      Switzerland) (C)
   E. helleborine (Canada,                   na           58.0
      naturalized) (C)
   E. helleborine (C. Italy) (C)             62.5         59.0
   E. helleborine (Denmark) (C)              88.9         73.6
   E. leptochila (Scotland, England) (C)     57.1         26.5
   E. microphylla (C. Italy) (R)             0.0          0.0
   E. palustris (C. Italy) (R)               29.0         29.0
   E. phyllanthes (Denmark) (R)              0.0          0.0
   E. phyllanthes (Scotland, England) (R)    7.1          7.1
   E. purpurata (Denmark) (R)                0.0          0.0
9. Galearis (Orchis) cyclochila (S.          50.0         46.4
   Korea) (R)
   G. (Gymnadenia) camtschatica (Ulleung     18.2         18.2
       Is. in S. Korea) (R)
10. Goodyera rosulacea (S. Korea) (C)        31.6         27.8
    G. repens (S. Korea) (R)                 0.0          0.0

    G. repens (NE Poland) (C)                50.0         50.0
    G. procera (Hong Kong) (C)               33.3         21.8

11. Habenaria Jentata (S. Korea) (R)         0.0          0.0

12. Hemipilia (Amitostigma) gracile          5.3          2.5
    (S. Korea) (C)
13. Liparis kumokiri (S. Korea) (C)          0.0          0.0
    L. makinoana (S. Korea) (C)              73.3         70.0
    L. pterosepala (Jcju Is., S.             0.0          0.0
    Korea) (R)
14. Neottianthe (Gymnadenia) cucullata       27.3         12.5
    (S. Korea) (R)
15. Oreorchis patens (S. Korea) (C)          76.5         62.8
    O. coreana (Jeju Is. in S. Korea) (R)    0.0          0.0
16. Pecteilis (Habenaria) radiata            0.0          0.0
    (S. Korea) (R)
17. Pelatantheria (Sarcanthus)               4.8          1.6
    scolopendrifolius (S. Korea) (R)
18. Peristylus densus (Jeju Is.) (R)         0.0          0.0
    (= Habenaria flagellifera)
19. Platanthera hologlattis                  10.0         6.7
    (S. Korea) (R)
    P. leucophaea (NE USA) (R)               25.0         11.9
    P. chlorantha (NE Poland) (R)            33.3         25.6

    P. bifolia (NE Poland) (C)               33.3         22.3
20. Pogonia minor (S. Korea) (R)             14.3         2.7

21. Tipularia japonica (S. Korea) (R)        0.0          0.0

Species (country sampled) (R/C) (a)          Genetic parameter (g)

                                             [A.sub.S]   [A.sub.P]

1. Bletilla striata (S. Korea) (R)           1.15        1.13
2. Bulbophyllum diymoglossum                 1.05        1.03
   (S. Korea) (R)
   B. adiamantinum (Brazil) (C)              na          2.95
   B. bidentatum (Brazil) (C)                3.80        3.80
   B. epiphytum (Brazil) (C)                 na          3.20
   B. exaltatum (Brazil) (C)                 4.11        2.07
   B. insectiferum (Brazil) (C)              2.60        2.60
   B. involution (Brazil) (C)                3.33        2.00
   B. plumosum (Brazil) (C)                  na          2.95
   B. regnellii (Brazil) (C)                 3.40        3.40
   B. rapicola (Brazil) (C)                  3.40        3.40
   B. sanderianum (Brazil) (C)               1.89        1.60
   B. weddellii (Brazil) (C)                 2.56        1.68
3. Calanthe discolor (S. Korea) (R)          2.59        2.01
   C. reflexa (Jeju Is. in S. Korea) (R)     1.53        1.50

   C. sieboidii (S. Korea) (R)               2.35        1.96
4. Cephaianthera longibracteata              1.45        1.27
      (S. Korea) (C)
   C. subaphyila (S. Korea) (R)              1.00        1.00

   C. damasonium (C. Italy) (C)              1.00        1.00

   C. longifolia (C. Italy) (C)              1.67        1.59

   C. rubra (C. Italy) (C)                   1.67        1.33
   C. rubra (NE Poland) (C)                  1.54        1.14
5. Cremastra appendiculata var.              1.77        1.70
     variahilis (S. Korea) (R)
6. Cymbidium goeringii (S. Korea) (C)        2.71        2.08
   C. goeringii (Japan) (R)                  2.21        1.95
   C. kanran (Jeju Is. in S. Korea) (R)      2.83        2.83
7. Cypripedium japonicum (S. Korea) (R)      1.00        1.00
   C. macranthos (S. Korea) (R)              1.50        1.47
   C. macranthos var. rebunense              1.85        1.69
     (Rebun Is. in Japan) (R)
   C. acaule (Michigan, USA) (C)             1.77        1.44
   C. arietinum (Michigan, USA) (R)          1.00        1.00
   C. calceolus (Poland) (C)                 2.36        1.58

   C. candidum (Michigan, USA) (R)           2.00        1.43
   C. fasciculatum (Washington, USA) (R)     na          1.20
   C. kenluckiense (Arkansa, Oklahoma,       1.33        1.15
      Texas, Virginiain USA) (R)
   C. parvijlorum var. makasin (Indiana,     2.40        1.80
      Michigan in USA) (C)
   C. parvijlorum (Georgia, Missouri,        1.90        1.40
      Oklahoma, Virginia in USA) (C)
   C. parviflorum var. pubescens             2.50        1.70
      (northern form) (Illinois, Indiana,
      Michigan, Ohio in USA) (C)
   C. parviflorum var. pubescens             2.50        1.60
      (southern form) (SE USA, Ohio in
      USA) (C)
   C. regime (Michigan, USA) (R)             1.27        1.15
   C. regime (SE USA, Ohio in USA) (R)       1.20        1.11
      Epipactis thunbergii (S. Korea) (C)    1.04        1.04
8. E. papillosa (S. Korea) (R)               1.00        1.00
   E. atrorubens (NE Poland) (R)             1.14        1.12
   E. helleborine (NE Poland) (C)            1.68        1.51
   E. helleborine (Scotland, England) (C)    na          1.46
   E. helleborine (Belgium, Denmark,         na          1.77
      England, France, Germany, Scotland,
      Switzerland) (C)
   E. helleborine (Canada,                   na          1.90
      naturalized) (C)
   E. helleborine (C. Italy) (C)             2.00        1.82
   E. helleborine (Denmark) (C)              2.78        2.63
   E. leptochila (Scotland, England) (C)     1.71        1.36
   E. microphylla (C. Italy) (R)             1.00        1.00
   E. palustris (C. Italy) (R)               1.29        1.29
   E. phyllanthes (Denmark) (R)              1.00        1.00
   E. phyllanthes (Scotland, England) (R)    1.07        1.07
   E. purpurata (Denmark) (R)                1.00        1.00
9. Galearis (Orchis) cyclochila (S.          1.71        1.68
   Korea) (R)
   G. (Gymnadenia) camtschatica (Ulleung     1.18        1.18
       Is. in S. Korea) (R)
10. Goodyera rosulacea (S. Korea) (C)        1.37        1.31
    G. repens (S. Korea) (R)                 1.00        1.00

    G. repens (NE Poland) (C)                1.90        1.68
    G. procera (Hong Kong) (C)               1.33        1.22

11. Habenaria Jentata (S. Korea) (R)         1.00        1.00

12. Hemipilia (Amitostigma) gracile          1.11        1.03
    (S. Korea) (C)
13. Liparis kumokiri (S. Korea) (C)          1.00        1.00
    L. makinoana (S. Korea) (C)              2.27        2.07
    L. pterosepala (Jcju Is., S.             1.00        1.00
    Korea) (R)
14. Neottianthe (Gymnadenia) cucullata       1.27        1.13
    (S. Korea) (R)
15. Oreorchis patens (S. Korea) (C)          2.53        1.96
    O. coreana (Jeju Is. in S. Korea) (R)    1.00        1.00
16. Pecteilis (Habenaria) radiata            1.00        1.00
    (S. Korea) (R)
17. Pelatantheria (Sarcanthus)               1.10        1.02
    scolopendrifolius (S. Korea) (R)
18. Peristylus densus (Jeju Is.) (R)         1.00        1.00
    (= Habenaria flagellifera)
19. Platanthera hologlattis                  1.10        1.07
    (S. Korea) (R)
    P. leucophaea (NE USA) (R)               1.67        1.18
    P. chlorantha (NE Poland) (R)            1.60        1.36

    P. bifolia (NE Poland) (C)               na          1.48
20. Pogonia minor (S. Korea) (R)             1.14        1.04

21. Tipularia japonica (S. Korea) (R)        1.00        1.00

Species (country sampled) (R/C) (a)          Genetic parameter (g)

                                             [H.sub.eS]   [H.sub.eP]

1. Bletilla striata (S. Korea) (R)           0.060        0.049
2. Bulbophyllum diymoglossum                 0.016        0.011
   (S. Korea) (R)
   B. adiamantinum (Brazil) (C)              na           0.439
   B. bidentatum (Brazil) (C)                0.612        0.612
   B. epiphytum (Brazil) (C)                 na           0.466
   B. exaltatum (Brazil) (C)                 0.338        0.266
   B. insectiferum (Brazil) (C)              0.439        0.439
   B. involution (Brazil) (C)                0.333        0.267
   B. plumosum (Brazil) (C)                  na           0.439
   B. regnellii (Brazil) (C)                 0.481        0.481
   B. rapicola (Brazil) (C)                  0.490        0.490
   B. sanderianum (Brazil) (C)               0.179        0.160
   B. weddellii (Brazil) (C)                 0.238        0.183
3. Calanthe discolor (S. Korea) (R)          0.244        0.227
   C. reflexa (Jeju Is. in S. Korea) (R)     0.186        0.185

   C. sieboidii (S. Korea) (R)               0.293        0.280
4. Cephaianthera longibracteata              0.097        0.036
      (S. Korea) (C)
   C. subaphyila (S. Korea) (R)              0.000        0.000

   C. damasonium (C. Italy) (C)              0.000        0.000

   C. longifolia (C. Italy) (C)              0.188        0.168

   C. rubra (C. Italy) (C)                   0.180        0.127
   C. rubra (NE Poland) (C)                  0.125        0.059
5. Cremastra appendiculata var.              0.231        0.215
     variahilis (S. Korea) (R)
6. Cymbidium goeringii (S. Korea) (C)        0.251        0.240
   C. goeringii (Japan) (R)                  0.240        0.230
   C. kanran (Jeju Is. in S. Korea) (R)      0.173        0.173
7. Cypripedium japonicum (S. Korea) (R)      0.000        0.000
   C. macranthos (S. Korea) (R)              0.200        0.185
   C. macranthos var. rebunense              0.187        0.183
     (Rebun Is. in Japan) (R)
   C. acaule (Michigan, USA) (C)             0.095        0.080
   C. arietinum (Michigan, USA) (R)          0.000        0.000
   C. calceolus (Poland) (C)                 0.228        0.151

   C. candidum (Michigan, USA) (R)           0.054        0.050
   C. fasciculatum (Washington, USA) (R)     0.040        0.030
   C. kenluckiense (Arkansa, Oklahoma,       0.050        0.042
      Texas, Virginiain USA) (R)
   C. parvijlorum var. makasin (Indiana,     0.290        0.230
      Michigan in USA) (C)
   C. parvijlorum (Georgia, Missouri,        0.130        0.130
      Oklahoma, Virginia in USA) (C)
   C. parviflorum var. pubescens             0.220        0.200
      (northern form) (Illinois, Indiana,
      Michigan, Ohio in USA) (C)
   C. parviflorum var. pubescens             0.190        0.160
      (southern form) (SE USA, Ohio in
      USA) (C)
   C. regime (Michigan, USA) (R)             0.037        0.024
   C. regime (SE USA, Ohio in USA) (R)       0.051        0.038
      Epipactis thunbergii (S. Korea) (C)    0.020        0.013
8. E. papillosa (S. Korea) (R)               0.000        0.000
   E. atrorubens (NE Poland) (R)             0.042        0.034
   E. helleborine (NE Poland) (C)            0.141        0.115
   E. helleborine (Scotland, England) (C)    na           0.145
   E. helleborine (Belgium, Denmark,         na           0.230
      England, France, Germany, Scotland,
      Switzerland) (C)
   E. helleborine (Canada,                   na           0.232
      naturalized) (C)
   E. helleborine (C. Italy) (C)             0.238        0.233
   E. helleborine (Denmark) (C)              0.302        0.274
   E. leptochila (Scotland, England) (C)     0.152        0.117
   E. microphylla (C. Italy) (R)             0.000        0.000
   E. palustris (C. Italy) (R)               0.085        0.085
   E. phyllanthes (Denmark) (R)              0.000        0.000
   E. phyllanthes (Scotland, England) (R)    0.028        0.028
   E. purpurata (Denmark) (R)                0.000        0.000
9. Galearis (Orchis) cyclochila (S.          0.216        0.210
   Korea) (R)
   G. (Gymnadenia) camtschatica (Ulleung     0.066        0.067
       Is. in S. Korea) (R)
10. Goodyera rosulacea (S. Korea) (C)        0.100        0.126
    G. repens (S. Korea) (R)                 0.000        0.000

    G. repens (NE Poland) (C)                0.210        0.197
    G. procera (Hong Kong) (C)               na           0.073

11. Habenaria Jentata (S. Korea) (R)         0.000        0.000

12. Hemipilia (Amitostigma) gracile          0.026        0.009
    (S. Korea) (C)
13. Liparis kumokiri (S. Korea) (C)          0.000        0.000
    L. makinoana (S. Korea) (C)              0.346        0.317
    L. pterosepala (Jcju Is., S.             0.000        0.000
    Korea) (R)
14. Neottianthe (Gymnadenia) cucullata       0.039        0.036
    (S. Korea) (R)
15. Oreorchis patens (S. Korea) (C)          0.258        0.237
    O. coreana (Jeju Is. in S. Korea) (R)    0.000        0.000
16. Pecteilis (Habenaria) radiata            0.000        0.000
    (S. Korea) (R)
17. Pelatantheria (Sarcanthus)               0.015        0.002
    scolopendrifolius (S. Korea) (R)
18. Peristylus densus (Jeju Is.) (R)         0.000        0.000
    (= Habenaria flagellifera)
19. Platanthera hologlattis                  0.047        0.031
    (S. Korea) (R)
    P. leucophaea (NE USA) (R)               0.103        0.033
    P. chlorantha (NE Poland) (R)            0.102        0.078

    P. bifolia (NE Poland) (C)               na           0.093
20. Pogonia minor (S. Korea) (R)             0.010        0.008

21. Tipularia japonica (S. Korea) (R)        0.000        0.000

Species (country sampled) (R/C) (a)          Genetic      Ref (h)
                                          parameter (g)

                                             [G.sub.ST]

1. Bletilla striata (S. Korea) (R)           0.130        1
2. Bulbophyllum diymoglossum                 0.253        2
   (S. Korea) (R)
   B. adiamantinum (Brazil) (C)              0.018        3
   B. bidentatum (Brazil) (C)                na           3
   B. epiphytum (Brazil) (C)                 0.166        3
   B. exaltatum (Brazil) (C)                 0.230        4
   B. insectiferum (Brazil) (C)              na           3
   B. involution (Brazil) (C)                0.232        4
   B. plumosum (Brazil) (C)                  0.008        3
   B. regnellii (Brazil) (C)                 na           3
   B. rapicola (Brazil) (C)                  na           3
   B. sanderianum (Brazil) (C)               0.145        4
   B. weddellii (Brazil) (C)                 0.269        4
3. Calanthe discolor (S. Korea) (R)          0.068        5
   C. reflexa (Jeju Is. in S. Korea) (R)     0.006        5

   C. sieboidii (S. Korea) (R)               0.072        5
4. Cephaianthera longibracteata              0.247        6
      (S. Korea) (C)
   C. subaphyila (S. Korea) (R)              na           7

   C. damasonium (C. Italy) (C)              na           8

   C. longifolia (C. Italy) (C)              0.104        8

   C. rubra (C. Italy) (C)                   0.247        8
   C. rubra (NE Poland) (C)                  0.267        9
5. Cremastra appendiculata var.              0.066        10
     variahilis (S. Korea) (R)
6. Cymbidium goeringii (S. Korea) (C)        0.098        11
   C. goeringii (Japan) (R)                  0.027        12
   C. kanran (Jeju Is. in S. Korea) (R)      na           7
7. Cypripedium japonicum (S. Korea) (R)      na           13
   C. macranthos (S. Korea) (R)              0.059        13
   C. macranthos var. rebunense              0.085        14
     (Rebun Is. in Japan) (R)
   C. acaule (Michigan, USA) (C)             0.164        15
   C. arietinum (Michigan, USA) (R)          na           15
   C. calceolus (Poland) (C)                 0.137        16

   C. candidum (Michigan, USA) (R)           0.069        15
   C. fasciculatum (Washington, USA) (R)     0.040        17
   C. kenluckiense (Arkansa, Oklahoma,       0.182        18
      Texas, Virginiain USA) (R)
   C. parvijlorum var. makasin (Indiana,     0.199        19
      Michigan in USA) (C)
   C. parvijlorum (Georgia, Missouri,        0.149        19
      Oklahoma, Virginia in USA) (C)
   C. parviflorum var. pubescens             0.137        19
      (northern form) (Illinois, Indiana,
      Michigan, Ohio in USA) (C)
   C. parviflorum var. pubescens             0.209        19
      (southern form) (SE USA, Ohio in
      USA) (C)
   C. regime (Michigan, USA) (R)             0.349        15
   C. regime (SE USA, Ohio in USA) (R)       0.212        20
      Epipactis thunbergii (S. Korea) (C)    0.388        21
8. E. papillosa (S. Korea) (R)               na           22
   E. atrorubens (NE Poland) (R)             0.265        23
   E. helleborine (NE Poland) (C)            0.220        24
   E. helleborine (Scotland, England) (C)    0.240        25
   E. helleborine (Belgium, Denmark,         0.200        26
      England, France, Germany, Scotland,
      Switzerland) (C)
   E. helleborine (Canada,                   0.090        26
      naturalized) (C)
   E. helleborine (C. Italy) (C)             0.033        27
   E. helleborine (Denmark) (C)              0.087        28
   E. leptochila (Scotland, England) (C)     na           29
   E. microphylla (C. Italy) (R)             na           27
   E. palustris (C. Italy) (R)               na           27
   E. phyllanthes (Denmark) (R)              na           28
   E. phyllanthes (Scotland, England) (R)    na           29
   E. purpurata (Denmark) (R)                na           28
9. Galearis (Orchis) cyclochila (S.          0.030        30
   Korea) (R)
   G. (Gymnadenia) camtschatica (Ulleung     0.000        31
       Is. in S. Korea) (R)
10. Goodyera rosulacea (S. Korea) (C)        0.150        32
    G. repens (S. Korea) (R)                 na           7

    G. repens (NE Poland) (C)                0.060        33
    G. procera (Hong Kong) (C)               0.523        34

11. Habenaria Jentata (S. Korea) (R)         na           7

12. Hemipilia (Amitostigma) gracile          0.781        31
    (S. Korea) (C)
13. Liparis kumokiri (S. Korea) (C)          na           35, 36
    L. makinoana (S. Korea) (C)              0.107        35, 36
    L. pterosepala (Jcju Is., S.             na           7
    Korea) (R)
14. Neottianthe (Gymnadenia) cucullata       0.081        31
    (S. Korea) (R)
15. Oreorchis patens (S. Korea) (C)          0.075        37
    O. coreana (Jeju Is. in S. Korea) (R)    na           37
16. Pecteilis (Habenaria) radiata            na           7
    (S. Korea) (R)
17. Pelatantheria (Sarcanthus)               0.899        2
    scolopendrifolius (S. Korea) (R)
18. Peristylus densus (Jeju Is.) (R)         na           7
    (= Habenaria flagellifera)
19. Platanthera hologlattis                  0.328        7
    (S. Korea) (R)
    P. leucophaea (NE USA) (R)               0.754        38
    P. chlorantha (NE Poland) (R)            0.251        9

    P. bifolia (NE Poland) (C)               0.048        39
20. Pogonia minor (S. Korea) (R)             0.211        31

21. Tipularia japonica (S. Korea) (R)        na           22

(a) R/C, rare or common in area, regions, country or countries that
sampled for allozyme studies

(b) Ecological affinity: B, boreal; T, temperate; TR, tropical; WT,
warm temperate (or subtropical)

(c) Range: BA, Bangladesh; BH, Bhutan; BR, Brazil; C, China; CA,
Cambodia; CAN, Canada; CC, central China; CEA, central Asia; CEC,
central and eastern Canada; CIB, circumboreal regions; CSC, central
and southern China; CUS, central United States of America; EC,
eastern Canada; EH, eastern Himalayas; EEU, eastern Europe; ES,
eastern Siberia; EU, Europe; EUA, Eurasia; EUS, eastern US; EZ,
eastern Zhejiang, eastern China; GL, States around the Great Lakes
in US; GU, Guyana; HA, Hainan Island, South China; HU, Hunan,
southern China; IN, India; IND, Indonesia; J, Japan; JJ, Jeju
Island, South Korea; K, Korea; KAS, Kashmir; LA, Laos; MO,
Mongolia; M WUS, Midwest US; MY, Myanmar; NA, North America; NAF,
northern Africa; NCUS, North Central US; NE, Nepal; NEC,
northeastern China; NECA, northeastern California, US; NEQ,
northeastern Qinghai, western China; NEUS, North Eastern US; NI,
northern India; NK, northern Korea; NUS, northern US; NV, North
Vietnam; NWI, Northwest India; NWY, northwestern Yunnan, South
China; PA, Pakistan; PH, Philippines; R, Russia; RFE, Russian Far
East; RI, Rebun Island, Japan; RY. Ryukyu Islands, southern Japan;
SA, Sakhalin; SC, South China; SCUS, South Central US; SEUS,
southeastern US; SJ, southern Japan; SJT, Tochigi Prefecture in
southern Japan; SK, southern Korea; SLF, Fcngcheng in southern
Liaoning, northeastern China; SR, Sri Lanka; ST, southern Taiwan;
SUNA, subarctic North America; SUS, South US; SWA, South Western
Asia; SWC, South Western China; TH, Thailand; TW, Taiwan; TX,
Texas, USA; VE, Venezuela; VI, Vietnam; WA, Western Asia; WEU,
Western Europe; WH, Western Henan, South China; WUS, West US; WCUS,
West Central US; YT, Yakushima and Tanekashima Islands, southern
Japan

(d) R/C, rare or common at regional or global levels (at the
species level). See more explanations in Materials and Methods
section

(e) Growth form: E, epiphytic; L, lithophytic, R, rupicolous
(inhabiting rock areas or rock crevices); T, terrestrial

(f) NP, number of populations examined

(g) %P, percentage of polymorphic loci; A, mean number of alleles
per locus; [H.sub.e], genetic diversity. Allozyme-bascd genetic
diversity parameters arc well described in Berg and Hamrick
(1997).The subscript "S" denotes species' (or pooled samples)
values, while the subscript "P" indicates population means. GST
(Fsr), measures of among-population differentiation

(h) Source references: 1, Chung et al. (2013c); 2, Chung et al.
(2007a); 3, Azevedo et al. (2007); 4, Ribeiro et al. (2008); 5,
Chung et al. (2013d); 6. Chung et al. (2004b); 7. M. Y. Chung & M.
G. Chung (unpubl. Data); 8, Scacchi et al. (1991); 9, Brzosko and
Wroblewska(2013); 10, Chung ct al. (2013a); 11, Chung and Chung
(1999); 12, Chung and Chung (2000); 13, Chung et al. (2009); 14,
Izawa ct al. (2007); 15, Case (1994); 16, Brzosko et al. (2011);
17, Aagaard et al. (1999); 18, Case et al. (1998); 19, Wallace and
Case (2000); 20, Kennedy and Walker (2007); 21, Chung and Chung
(2007); 22, Chung (2009b); 23, Brzosko et al. (2006); 24, Brzosko
ct al. (2004); 25, Hollingsworth and Dickson (1997); 26, Squirrell
et al. (2001); 27, Scacchi ct al. (1987); 28, Ehlers and Pedersen
(2000); 29, Harris and Abbott (1997); 30, Chung et al. (2005a); 31,
Chung (2009a); 32. Chung and Chung (2010); 33. Brzosko et al.
(2013); 34, Wong and Sun (1999); 35, Chung et al. (2005b); 36,
Chung et al. (2007b); 37, Chung ct al. (2012); 38, Wallace (2002);
39, Brzosko ct al. (2009)

Table 2 Summary Statistics of the Genetic Diversity for Rare Orchids
in Korea and their Common Congeners at the Global Scale (Nine
Pairs) (a)

Parameter    Mean values (SE)                Wilcoxon signed-rank
                                             test

             Rare            Common          Z        P

%[P.sub.P]   11.04(7.41)     45.00 (6.68)    -2.547   0.006
[A.sub.P]    1.24 (0.20)     1.74 (0.15)     -1.836   0.038
[H.sub.eP]   0.031 (0.019)   0.181 (0.032)   -2.666   0.005
%[P.sub.S]   12.43 (7.39)    54.88 (7.33)    -2.666   0.005
[A.sub.S]    1.28 (0.21)     2.11 (0.21)     -2.380   0.010
[H.sub.eS]   0.033 (0.021)   0.209 (0.029)   -2.520   0.007

Parameter    Rare vs. common orchid correlation

             Corr. cocf.   P
             ([r.sub.s])

%[P.sub.P]   0.347         0.359
[A.sub.P]    0.402         0.291
[H.sub.eP]   0.237         0.552
%[P.sub.S]   0.237         0.552
[A.sub.S]    0.682         0.069
[H.sub.eS]   0.546         0.171

(a) Wilcoxon signed-rank tests were conducted for comparing both
population (subscript "P") and species (subscript "S") level
values for each measure

Table 3 Summary of Allozyme-Based Genetic Parameters for Rare,
Common Orchids, Plants having Similar Life History-Traits, and
Species from two Areas Largely Recognized as Harboring Glacial
Rcfugia [i.e., the Baekdudaegan (BDDG, the main Mountain System of
the Korean Peninsula), the Southeastern US, North--western
Mediterranean Basin] (a)

Category                                     %[P.sub.S]   %[P.sub.P]

Rare orchids in Korea (N = 24)                  21.8         18.6
Rare orchids in Table 1 (N = 38)                23.3         19.2
Common orchids in Table 1 (N = 32)              62.3         50.4
Means for orchids                               41.0         33.2
([N.sub.S] = 68; [N.sub.P] = 68)
Means for orchids                               46.2         33.7
([N.sub.S] = 32; [N.sub.P] = 36)
Means for orchids ([N.sub.S] = 16)              44.8          na
Means for orchids ([N.sub.S] = 71)               na           na
Means for orchids ([N.sub.S] = 52)               na           na
All plants                                      52.2         35.1
([N.sub.S] = 725; [N.sub.P] = 725)
Endemic plants                                  40.0         26.3
([N.sub.S] = 81; [N.sub.P] = 100)
Plants narrowly-distributed                     45.1         30.6
([N.sub.S] = 101; [N.sub.P] = 115)
Short-lived herbaceous perennials               41.3         28.0
([N.sub.S] = 152; [N.sub.P] = 159)
Plants with outcrossing-animal breeding         51.1         35.9
system ([N.sub.S] = 172; [N.sub.P] = 164)
Plants occurring mainly in the BDDG             64.3         46.0
in Korea (c) ([N.sub.S] = 16;
[N.sub.P] = 16)
Rare plants in the southeastern US              46.7         33.3
([N.sub.S] = 52; [N.sub.P] = 52)
Plants from NW Mediterranean Basin               na          34.2
([N.sub.P] = 36)

Category                                     [A.sub.S]   [A.sub.P]

Rare orchids in Korea (N = 24)                 1.34        1.22
Rare orchids in Table 1 (N = 38)               1.37        1.27
Common orchids in Table 1 (N = 32)             2.17        1.90
Means for orchids                              1.71        1.55
([N.sub.S] = 68; [N.sub.P] = 68)
Means for orchids                              1.83        1.46
([N.sub.S] = 32; [N.sub.P] = 36)
Means for orchids ([N.sub.S] = 16)              na          na
Means for orchids ([N.sub.S] = 71)              na          na
Means for orchids ([N.sub.S] = 52)              na          na
All plants                                     1.99        1.53
([N.sub.S] = 725; [N.sub.P] = 725)
Endemic plants                                 1.80        1.39
([N.sub.S] = 81; [N.sub.P] = 100)
Plants narrowly-distributed                    1.83        1.45
([N.sub.S] = 101; [N.sub.P] = 115)
Short-lived herbaceous perennials              1.70        1.40
([N.sub.S] = 152; [N.sub.P] = 159)
Plants with outcrossing-animal breeding        1.99        1.54
system ([N.sub.S] = 172; [N.sub.P] = 164)
Plants occurring mainly in the BDDG            2.20        1.72
in Korea (c) ([N.sub.S] = 16;
[N.sub.P] = 16)
Rare plants in the southeastern US             1.87        1.53
([N.sub.S] = 52; [N.sub.P] = 52)
Plants from NW Mediterranean Basin              na         1.53
([N.sub.P] = 36)

Category                                     [H.sub.eS]   [H.sub.eP]

Rare orchids in Korea (N = 24)                 0.075        0.070
Rare orchids in Table 1 (N = 38)               0.073        0.066
Common orchids in Table 1 (N = 32)             0.225        0.217
Means for orchids                              0.135        0.134
([N.sub.S] = 68; [N.sub.P] = 68)
Means for orchids                              0.119        0.107
([N.sub.S] = 32; [N.sub.P] = 36)
Means for orchids ([N.sub.S] = 16)             0.137          na
Means for orchids ([N.sub.S] = 71)               na           na
Means for orchids ([N.sub.S] = 52)               na           na
All plants                                     0.153        0.116
([N.sub.S] = 725; [N.sub.P] = 725)
Endemic plants                                 0.096        0.063
([N.sub.S] = 81; [N.sub.P] = 100)
Plants narrowly-distributed                    0.137        0.105
([N.sub.S] = 101; [N.sub.P] = 115)
Short-lived herbaceous perennials              0.116        0.096
([N.sub.S] = 152; [N.sub.P] = 159)
Plants with outcrossing-animal breeding        0.167        0.124
system ([N.sub.S] = 172; [N.sub.P] = 164)
Plants occurring mainly in the BDDG            0.193        0.159
in Korea (c) ([N.sub.S] = 16;
[N.sub.P] = 16)
Rare plants in the southeastern US             0.123        0.100
([N.sub.S] = 52; [N.sub.P] = 52)
Plants from NW Mediterranean Basin               na         0.113
([N.sub.P] = 36)

Category                                       [G.sub.ST]      Ref (b)

Rare orchids in Korea (N = 24)               0.169 (N = 12)       1
Rare orchids in Table 1 (N = 38)             0.189 (N = 21)       1
Common orchids in Table 1 (N = 32)           0.194 (N = 25)       1
Means for orchids                            0.190 (N = 68)       1
([N.sub.S] = 68; [N.sub.P] = 68)
Means for orchids                            0.163 (N = 32)       2
([N.sub.S] = 32; [N.sub.P] = 36)
Means for orchids ([N.sub.S] = 16)           0.087 (N = 16)       3
Means for orchids ([N.sub.S] = 71)           0.161 (N = 71)       4
Means for orchids ([N.sub.S] = 52)           0.146 (N = 52)       5
All plants                                   0.225 (N = 830)      6
([N.sub.S] = 725; [N.sub.P] = 725)
Endemic plants                               0.248 (N = 52)       6
([N.sub.S] = 81; [N.sub.P] = 100)
Plants narrowly-distributed                  0.242 (N = 82)       6
([N.sub.S] = 101; [N.sub.P] = 115)
Short-lived herbaceous perennials            0.233 (N = 119)      6
([N.sub.S] = 152; [N.sub.P] = 159)
Plants with outcrossing-animal breeding      0.197 (N = 124)      6
system ([N.sub.S] = 172; [N.sub.P] = 164)
Plants occurring mainly in the BDDG          0.175 (N = 16)       7
in Korea (c) ([N.sub.S] = 16;
[N.sub.P] = 16)
Rare plants in the southeastern US           0.187 (N = 52)       8
([N.sub.S] = 52; [N.sub.P] = 52)
Plants from NW Mediterranean Basin           0.248 (N = 36)       9
([N.sub.P] = 36)

(a) Na, not available

(b) Source references: 1, present study; 2, Case (2002); 3. Hamrick
and Godt (1996); 4, Forrest et al. (2004); 5, Phillips et al.
(2012); 6, Hamrick and Godt (1989); 7, Chung et al. (2017); 8, Godt
and Hamrick (2001); 9, Lopez-Pujol et al. (2009)

(c) Only species with most of their populations in Korea (more than
half) occurring on main ridge or on immediate vicinity of the BDDG
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Author:Chung, Mi Yoon; Lopez-Pujol, Jordi; Son, Sungwon; Suh, Gang Uk; Yukawa, Tomohisa; Chung, Myong Gi
Publication:The Botanical Review
Article Type:Report
Geographic Code:9SOUT
Date:Mar 1, 2018
Words:16213
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