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Taxonomic Status of Lecanorchis Suginoana (Tuyama) Seriz

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Taxonomic Status of Lecanorchis Suginoana (Tuyama) Seriz Bull. Natl. Mus. Nat. Sci., Ser. B, 45(3), pp. 119–129, August 22, 2019 Taxonomic Status of Lecanorchis suginoana (Tuyama) Seriz. (Orchidaceae) Michihisa Takashima1,2,*, Yumi Yamashita3, Akihiko Kinoshita3,4, Mineo Ohta5, and Tomohisa Yukawa3 1 Tochigi Prefectural Museum, 2–2 Mutsumicho, Utsunomiya, Tochigi, 320–0865 Japan 2 Ryokusei-kenkyusho, 2–40–10 Kojimacho, Chofu, Tokyo, 182–0026 Japan 3 Tsukuba Botanical Garden, National Museum of Nature and Science, 4–1–1 Amakubo, Tsukuba, Ibaraki, 305–0005 Japan 4 Kyushu Research Center, Forestry and Forest Products Research Institute, 4–11–16 Kurokami, Kumamoto, 860–0862 Japan 5 Yuzen-sha, 1285–13 Takagosho, Kakegawa, Shizuoka, 436–0031 Japan * E-mail: [email protected] (Received 13 May 2019; accepted 26 June 2019) Abstract Lecanorchis suginoana (Tuyama) Seriz. has been interpreted as a variety of L. japon- ica Blume, a variety of L. kiusiana Tuyama, or an independent species. To re-evaluate the taxo- nomic status of this entity, macromolecular, morphological, and ecological characters were investi- gated. Divergence of nucleotide sequences supported independent status of three close relatives, viz., L. suginoana, L. kiusiana, and L. japonica. Furthermore, the results of molecular phyloge- netic analysis did not support infraspecific placement of L. suginoana in L. japonica. Moreover, flower colour, qualitative characters of labellum and column, quantitative characters of perianth lobes and column, flowering time, and associated vegetation types clearly distinguish L. suginoana from L. kiusiana. These differences corroborated the independent species status of L. suginoana rather than the infraspecific position of L. kiusiana. Key words: Japan, Lecanorchis, molecular analysis, morphological analysis, Orchidaceae, taxon- omy. tion, Tuyama (1982) pointed out close morpho- Introduction logical affinities of this entity to L. japonica var. The genus Lecanorchis Blume is a terrestrial, japonica and emphasized similarity of the shape achlorophyllous orchid genus in which about 25 of apical part of the column between them. species are distributed throughout temperate to In his revisionary work of the genus, Hashimoto tropical regions in East to Southeast Asia and (1990) proposed a new combination, L. kiusiana extending to New Guinea (WCSP, 2019). This Tuyama var. suginoana (Tuyama) T.Hashim. He group represents holomycoheterotrophy in their demonstrated common characters between this nutritional mode (Motomura et al., 2010) and entity and L. kiusiana var. kiusiana, i.e., rather depends upon carbon nutrition from particular small plant, lip with marginal papilla and con- groups of ectomycorrhizal fungi belonging to spicuous branchlets of disc-hairs, ovary with an Basidiomycota (Okayama et al., 2012). apparent ring-like excrescence below the calycu- Lecanorchis japonica Blume var. suginoana lus, and rather short fruit. Subsequently, Ser- Tuyama is one of the northernmost distributed izawa (2005) proposed to recognize it as an inde- members of the genus (Yukawa, 2015a, 2015b; pendent species L. suginoana (Tuyama) Seriz. Suetsugu et al., 2018). In the original descrip- He emphasized that this entity can be distin- 120 Michihisa Takashima et al. guished from L. kiusiana var. kiusiana by several and Ehime Prefecture, Shikoku, Japan (see Taxo- characters such as light yellow hairs on the disc nomic Treatment). They are the first records of of the labellum, earlier flowering time, and distribution in these areas. Total DNA of plants nearly truncate apical part of the column. How- was extracted from fresh or silica-gel-dried sam- ever, these conflicting taxonomic views have not ples with the DNeasy Plant Mini Kit (Qiagen, been tested so far. In this study we re-evaluate Valencia, California, USA) following the manu- the taxonomic status of this entity by use of mor- facturer’s instructions. Nucleotide sequences phological, macromolecular, and ecological char- were determined by amplifying the internal tran- acters. scribed spacer (ITS) regions of the 18S–26S nuclear ribosomal DNA via the polymerase chain reaction (PCR) from a total DNA extract. Experi- Materials and Methods mental methods follow those described in Topik From the outset, we tentatively treated the et al. (2005) and Yukawa et al. (2005) in which three taxa as independent species, viz., Lecanor- the primer information of the sequenced region is chis suginoana, L. kiusiana, and L. japonica also shown. Voucher specimens were deposited (Fig. 1). Materials used in the DNA analysis are at the Department of Botany, National Museum listed in Table 1. Besides, in the course of this of Nature and Science (TNS). study, populations of L. suginoana were found in The ITS sequences were aligned using MUS- Tochigi Prefecture, eastern part of Honshu, Japan CLE implemented in MEGA 7.0.14 (Kumar et Fig. 1. Flowering individuals of Lecanorchis suginoana (A), L. kiusiana (B) and L. japonica (C). Table 1. Materials used for DNA sequencing. All voucher specimens are deposited at TNS Species Locality Voucher Lecanorchis flavicans Japan, Kagoshima Pref., Amami-oshima Is. T. Yukawa 09-21 Lecanorchis japonica Japan, Kagoshima Pref., Amami-oshima Is H. Yamashita s. n. Japan, Shikoku, Ehime Pref., Uwajima-shi S. Hyodo 17864 Japan, Honshu, Gifu Pref., Mizunami-shi H. Nakagawa s. n. Japan, Honshu, Tochigi Pref., Mashiko-machi M. Takashima s. n. Japan, Honshu, Miyagi Pref., Shiroishi-shi M. Takashima s. n. Japan, Honshu, Fukui Pref., Echizen-cho T. Wakasugi & H. Enomoto 51886 Lecanorchis kiusiana Japan, Shikoku, Ehime Pref., Uwajima-shi S. Hyodo 17862 Japan, Honshu, Shizuoka Pref., Kakegawa-shi M. Takashima s. n. Japan, Honshu, Tochigi Pref., Mashiko-machi M. Takashima s. n. Korea, Jeju Is. S. Matsumoto 03-171 Lecanorchis suginoana Japan, Honshu, Shizuoka Pref., Kakegawa-shi T. Yukawa 14-10 Japan, Honshu, Ibaraki Pref., Mito-shi H. Uchiyama s. n. Japan, Honshu, Tochigi Pref., Yaita-shi M. Takashima s. n. Taxonomic status of Lecanorchis suginoana 121 al., 2016). All insertions/deletions were coded as ate differences of these characters between the missing data in the phylogenetic analysis of ITS. two taxa. Moreover, we conducted canonical dis- Lecanorchis flavicans Fukuy. was chosen as an criminant analysis and cluster analysis (Ward’s outgroup taxon on the basis of the results of phy- method) of the two taxa by using the same data logenetic analysis of the whole genus (unpub- set of morphological characters. All statistical lished). The evolutionary history was inferred by analyses were performed using Bell Curve for using a model based Bayesian approach and the Excel ver. 3.00 (Social Survey Research Infor- Maximum Likelihood (ML) method. A Bayesian mation Co., Ltd., Tokyo, Japan). search was performed using MrBayes 3.2 (Ron- We further carried out detailed phenological quist et al., 2012) and using the program Kaku- surveys of Lecanorchis suginoana and L. kiusi- san 4 (Tanabe, 2011) to select the ‘best-fit’ model ana in the four populations used for morphologi- of evolution under the Akaike information crite- cal analyses (Yaita and Kakegawa populations rion. Two separate runs were carried out using for L. suginoana; Mashiko and Kakegawa popu- the GTR＋I＋Γ model in each analysis. The lations for L. kiusiana). Five characters, viz., Markov chains were run for 1 million genera- number of individuals, number of buds, number tions and the first 10 thousand runs were burned of flowers in full bloom, and number of wilted in. ML analysis was conducted using MEGA and flowers, were recorded for the plants in each the Kimura 2-parameter model (Kimura, 1980) quadrat. In Yaita (L. suginoana habitat) and was chosen as the best fitting model for our data- Mashiko (L. kiusiana habitat), ca. 47 km apart set. Bootstrap analysis (Felsenstein, 1985) with each other, 11 consecutive surveys were con- 1000 replicates was used to assess the relative ducted in May and June 2012. In Kakegawa, the robustness of support for all branches. two taxa formed populations less than 20 m apart. Since the results of molecular phylogenetic Surveys were conducted in 17 and 30 May 2015. analysis demonstrated that Lecanorchis sugino- Furthermore, we recorded vegetation in associa- ana occupied a sister position of L. kiusiana and tion with L. suginoana and L. kiusiana at the was distantly related to L. japonica (see Results above-mentioned four habitats. Methods for and Discussion), morphological analyses were recording vegetation composition followed confined to the former two taxa. Observation of Braun-Blanquet (1964). morphological characters was based on living plants, dried herbarium specimens, and spirit- Results and Discussion preserved specimens listed in the section “Speci- mens examined”. Detailed measurements of Macromolecular characters quantitative morphological characters were car- In ca. 760 base pairs of ITS, three samples of ried out from the flowers collected in Yaita and Lecanorchis suginoana from different localities Kakegawa populations for L. suginoana, and had identical sequences. Four samples of L. kiu- Mashiko and Kakegawa populations for L. kiusi- siana had identical ITS sequences and two nucle- ana. Yaita and Mashiko are situated in the east- otide substitutions discriminated these two taxa. ern part of Honshu, Japan and Kakegawa is situ- In Kakegawa, populations of L. suginoana and L. ated in the central part of Honshu, Japan. A kiusiana are less than 20 m apart. It is likely that single flower was taken from each individual and reproductive isolation between these two taxa 63 samples were collected in total. Ten charac- occurs because no trace of hybridization was ters, viz., length of dorsal sepal, length of lateral detected in the nuclear nucleotide sequences sepal, length of petal, width of petal, length of investigated for these nearly sympatric popula- labellum, width of labellum, length of column, tions. Two ITS phylotypes demarcated by a sin- and width of column, were measured for each gle substitution were recognized in seven sam- sample. Student’s t-test was performed to evalu- ples of L. japonica. Both L. suginoana and L. 122 Michihisa Takashima et al. Fig. 2. Phylogenetic relationships of Lecanorchis suginoana, L. kiusiana and L.
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