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Phylogenetics of Tribe Collabieae (Orchidaceae, Epidendroideae) Based on Four Chloroplast Genes with Morphological Appraisal

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Phylogenetics of Tribe Collabieae (Orchidaceae, Epidendroideae) Based on Four Chloroplast Genes with Morphological Appraisal Phylogenetics of Tribe Collabieae (Orchidaceae, Epidendroideae) Based on Four Chloroplast Genes with Morphological Appraisal Xiao-Guo Xiang1., Wei-Tao Jin1., De-Zhu Li2, Andre´ Schuiteman3, Wei-Chang Huang4, Jian-Wu Li5, Xiao-Hua Jin1*, Zhen-Yu Li1* 1 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China, 2 Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan, China, 3 Herbarium, Library, Art and Archives Directorate, Royal Botanical Gardens, Kew, Richmond, Surrey, United Kingdom, 4 Shanghai Chenshan Botanical Garden, Songjiang, Shanghai, China, 5 Herbarium, Xishuanbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun Township, Mengla County, Yunnan, China Abstract Collabieae (Orchidaceae) is a long neglected tribe with confusing tribal and generic delimitation and little-understood phylogenetic relationships. Using plastid matK, psaB, rbcL, and trnH-psbA DNA sequences and morphological evidence, the phylogenetic relationships within the tribe Collabieae were assessed as a basis for revising their tribal and generic delimitation. Collabieae (including the previously misplaced mycoheterotrophic Risleya) is supported as monophyletic and nested within a superclade that also includes Epidendreae, Podochileae, Cymbidieae and Vandeae. Risleya is nested in Collabiinae and sister to Chrysoglossum, a relationship which, despite their great vegetative differences, is supported by floral characters. Ania is a distinct genus supported by both morphological and molecular evidence, while redefined Tainia includes Nephelaphyllum and Mischobulbum. Calanthe is paraphyletic and consists four clades; the genera Gastrorchis, Phaius and Cephalantheropsis should be subsumed within Calanthe. Calanthe sect. Ghiesbreghtia is nested within sect. Calanthe,to which the disputed Calanthe delavayi belongs as well. Our results indicate that, in Collabieae, habit evolved from being epiphytic to terrestrial. Citation: Xiang X-G, Jin W-T, Li D-Z, Schuiteman A, Huang W-C, et al. (2014) Phylogenetics of Tribe Collabieae (Orchidaceae, Epidendroideae) Based on Four Chloroplast Genes with Morphological Appraisal. PLoS ONE 9(1): e87625. doi:10.1371/journal.pone.0087625 Editor: Keith A. Crandall, George Washington University, United States of America Received June 26, 2013; Accepted December 26, 2013; Published January 31, 2014 Copyright: ß 2014 Xiang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funds were provided by a grant from the National Natural Science Foundation of China (Grant No. 31107176) and the Knowledge Innovation Program of the Chinese Academy of Sciences (Grant No. 13214G1014). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (XHJ); [email protected] (ZYL) . These authors contributed equally to this work. Background 13 genera, i.e., Acanthephippium, Ancistrochilus, Anthogonium, Aulostylis, Bletia, Calanthe, Chysis, Ipsea, Phaius, Pachystoma, Spathoglottis, The family of Orchidaceae is one of largest among seed plants, Ascotainia, and Plocoglottis, and it was considered to be a synonym and several classification systems have been proposed to reflect of Bletiinae by most subsequent authors. Dressler & Dodson [23] their phylogeny and evolution (such as [1–4]). Recent molecular placed Collabiinae and Phajinae in tribe Epidendreae, whereas phylogenetic studies have shed new light on the relationships of Holttum [24] placed these two subtribes in two informal suggested Orchidaceae from genera to subfamilies (such as [5–16]). In groups, the ‘‘Phaius tribe’’ and the ‘‘Nephelaphyllum tribe’’. Dressler Collabieae, as in many orchids, relationships have been tradition- [3] placed Phajinae and Collabiinae in Arethuseae and Cymbi- ally defined based on subjective assessments of morphological dieae, respectively, then he [4] listed Collabiinae as one of his characters, and phylogenetic relationships remain to be assessed ‘‘misfits and leftover’’ groups of uncertain systematic position. using molecular data. Recent results of cladistic analyses of combined DNA sequences Tribe Collabieae, described by Pfitzer [17] based on Collabium, have provided some new insights in the systematics of tribe is a medium-sized group with about 450–500 species distributed Collabieae. Based on matK and rbcL, Goldman et al. [25] proposed mainly in the Old World tropics with a few species extending into that Mischobulbum, Nephelaphyllum, and Tainia should be transferred North Temperate Asia and Mesoamerica [18–21]. However, from Bletiinae (in the tribe Arethuseae) to the non-Arethuseae Collabieae has not been recognized by most of subsequent subtribe Collabiinae. Likewise, based on their analyses of ITS, authors, and the genera have been included in different tribes. matK, and trnL-F, van den Berg et al. [26] suggested that Schlechter [22] established two subtribes, Collabiinae and Collabiinae and Phajinae should be transferred to tribe Colla- Phajinae, in the tribe Kerosphaereae. The former included 7 bieae. Chase et al. [6] and Pridgeon et al. [19] tentatively genera, viz., Chrysoglossum, Collabium, Diglyphosa, Mischobulbum, redefined Collabieae to include 18–19 genera, pending future Nephelaphyllum, Pilophyllum, and Tainia, while the latter included studies. PLOS ONE | www.plosone.org 1 January 2014 | Volume 9 | Issue 1 | e87625 Phylogenetics of the Collabieae As currently defined, Collabieae include Acanthephippium, Ancis- Table 1. Parsimony statistics from phylogenetic analyses of trochilus, Ania, Calanthe, Cephalantheropsis, Collabium, Diglyphosa, the various datasets. Eriodes, Gastrorchis, Hancockia, Ipsea, Mischobulbum, Nephelaphyllum, Pachystoma, Phaius, Pilophyllum, Plocoglottis, Spathoglottis, and Tainia [19] and shows a variety of vegetative and floral variation, such as Aligned Information plants with corms or pseudobulbs of one to several internodes or Data Taxa length sites TL CI RI without storage organs; leaves petiolate or not and conduplicate or Large matrix convolute; inflorescences lateral or terminal; pollinia varying from rbcL 116 1362 182 857 0.476 0.693 2 through 4 to 8, and being soft or hard; viscidium present or absent. This diversity has led to difficulties in the circumscription matK 133 1646 433 2890 0.468 0.613 of the tribe, as well as its subtribes and genera, and made psaB 94 1666 207 838 0.548 0.679 problematic to infer the systematic position of the tribe among combined 133 4674 922 4590 0.474 0.604 other Orchidaceae [19,27]. Moreover, previous molecular sys- Reduced matrix tematic studies sampled Collabieae only superficially, with just 7 rbcL 51 1343 56 192 0.698 0.787 species in 6 genera in van den Berg et al. [26] and 10 species in 8 genera in Goldman et al. [25]. Due to the sparse sampling and/or matK 52 1846 208 678 0.723 0.780 weak support for Collabieae in previous molecular systematic trnH-psbA 35 1920 39 105 0.810 0.847 studies, subtribal and generic delimitation, as well as the psaB 32 1666 37 136 0.809 0.798 phylogenetic position of Collabieae within Orchidaceae, remain combined 52 6775 357 2372 0.702 0.739 unresolved. Generic delimitation in many genera within Collabieae is often TL: tree length; CI: Consistence Index; RI: Retention Index. doi:10.1371/journal.pone.0087625.t001 confused and inconsistent across their distribution range. The Tainia alliance, including Ania, Hancockia, Mischobulbum, Nephela- phyllum, and Tainia, is among the typical cases [18,19,24,27–30]. Subfamily-wide analysis of Epidendroideae Smith [27] included Mischobulbum and Ascotainia in Tainia. For the first analysis using the subfamily-wide matrix, under the Schlechter [22] maintained Mischobulbum, Hancockia, and Ascotainia Bayesian criterion, selection of a partition scheme based on BF as separate genera. Gagnepain [31] considered Ania, Mischobulbum, favored the P5 partition scheme (see Table 2). The trees generated Nephelaphyllum, and Tainia as congeneric. Holttum [24] subsumed by BI were congruent with those of MP analysis except for poorly Mischobulbum and Ania into Tainia. Seidenfaden [29] included Ania supported nodes along the backbone of the tree (Fig. 1, the MP in Tainia, and kept Nephelaphyllum, Mischobulbum, and Hancockia as strict consensus tree is not shown). Risleya atropurpurea is identified distinct genera. Turner [15] recognized Ania, Hancockia, Mischo- as a member of tribe Collabieae, not a member of tribe bulbum, Nephelaphyllum and Tainia. Pearce and Cribb [20] likewise Malaxideae as previously thought [19]. maintained Ania, Tainia, Mischobulbum, and Nephelaphyllum as distinct genera (Hancockia was not included in their treatment). Analysis of Collabieae Chen et al. [21], following Pridgeon et al. [19] treated Ania, For the second analysis with the reduced matrix, P6 was selected Mischobulbum and Tainia as congeneric, and kept Nephelaphyllum and as the best-fit partition scheme under the Bayesian criterion (see Hancockia as distinct genera. Table 2). The BI analysis yielded trees with topologies that were Here we use DNA sequences of chloroplast genes rbcL and psaB, consistent with those retrieved
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