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20120620144528 1897.Pdf Annals of Botany 104: 431–445, 2009 doi:10.1093/aob/mcp089, available online at www.aob.oxfordjournals.org Molecular phylogenetics and morphological reappraisal of the Platanthera clade (Orchidaceae: Orchidinae) prompts expansion of the generic limits of Galearis and Platanthera Richard M. Bateman1,*, Karen E. James2, Yi-Bo Luo3, Robert K. Lauri4, Timothy Fulcher1, Phillip J. Cribb1 and Mark W. Chase1 1Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK, 2Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD, UK, 3Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, 100093, China and 4Rancho Santa Ana Botanic Garden, 1500 North College Avenue, Claremont, CA 91711, USA Received: 22 July 2008 Returned for revision: 4 December 2008 Accepted: 30 March 2009 Published electronically: 21 April 2009 † Background and Aims The Platanthera clade dominates the North American orchid flora and is well represented in eastern Asia. It has also generated some classic studies of speciation in Platanthera sections Platanthera and Limnorchis. However, it has proved rich in taxonomic controversy and near-monotypic genera. The clade is reviewed via a new molecular phylogenetic analysis and those results are combined with brief reconsideration of morphology in the group, aiming to rationalize the species into a smaller number of larger monophyletic genera and sections. † Methods Nuclear ribosomal internal transcribed spacer (ITS) sequences were obtained from 86 accessions of 35 named taxa, supplemented from GenBank with five accessions encompassing a further two named taxa. † Key Results Using Pseudorchis as outgroup, and scoring indels, the data matrix generated 30 most-parsimo- nious trees that differed in the placement of two major groups plus two closely related species. Several other internal nodes also attracted only indifferent statistical support. Nonetheless, by combining implicit assessment of morphological divergence with explicit assessment of molecular divergence (when available), nine former genera can be rationalized into four revised genera by sinking the monotypic Amerorchis, together with Aceratorchis and Chondradenia (neither yet sequenced), into Galearis, and by amalgamating Piperia, Diphylax and the monotypic Tsaiorchis into the former Platanthera section Platanthera. After further species sampling, this section will require sub-division into at least three sections. The present nomenclatural adjustments prompt five new combinations. † Conclusions Resolution of major groups should facilitate future species-level research on the Platanthera clade. Recent evidence suggests that ITS sequence divergence characterizes most species other than the P. bifolia group. The floral differences that distinguished Piperia, Diphylax and Tsaiorchis from Platanthera, and Aceratorchis and Chondradenia from Galearis, reflect various forms of heterochrony (notably paedomorphosis); this affected both the perianth and the gynostemium, and may have proved adaptive in montane habitats. Floral reduction was combined with lateral expansion of the root tubers in Piperia and Diphylax (including Tsaiorchis), whereas root tubers were minimized in the putative (but currently poorly supported) Neolindleya–Galearis clade. Allopolyploidy and/or autogamy strongly influenced speciation in Platanthera section Limnorchis and perhaps also Neolindleya. Reproductive biology remains an important driver of evolution in the clade, though plant–pol- linator specificity and distinctness of the species boundaries have often been exaggerated. Key words: Aceratorchis, Amerorchis, Chondradenia, Diphylax, Galearis, generic delimitation, internal transcribed spacer, Neolindleya, orchid, Piperia, phylogeny, Platanthera, Pseudorchis, speciation, Tsaiorchis. INTRODUCTION authors elected to divide Platanthera into several genera, each of which typically contained few (1–5) species. During the Platanthera Rich. (the butterfly orchids) is one of the most second half of the 20th century, the view most commonly species-rich genera of North Temperate orchids (Hapeman expressed by morphological systematists recognized the and Inoue, 1997), having centres of diversity in East Asia majority of these former genera as sections of the genus (Inoue, 1983) and North America (Luer, 1975; Sheviak, Platanthera (e.g. Lysiella, Limnorchis, Blephariglottis and 2002). Platanthera and allied genera share with many other tem- Tulotis). In contrast, other relevant taxa became more com- perate orchid groups a long and complex taxonomic history. monly recognized as distinct genera, notably Pseudorchis Victorian luminaries including Robert Brown and Joseph Seguier (syn. Leucorchis A. & D. Lo¨ve), Piperia Rydb. Hooker lumped Platanthera species into Habenaria, misled (1901a) and Diphylax Hook.f. (1869), together with the more by superficial floral similarities of these genera evident in, for obscure, monotypic Tsaiorchis Tang & Wang (1936). The example, rostellum morphology (cf. Dressler, 1993). Other most notorious ‘taxonomic football’ was Piperia, which was * For correspondence. E-mail [email protected] variously assigned to four other genera (Table 1b). # The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 432 Bateman et al. — Phylogeny of the Platanthera clade Also relevant to this discussion are a small number of narrowly defined groups of Platanthera, most notably the Eurasian species that were attributed by many authors to P. dilatata group (section Limnorchis) in North America the dominantly European genus Orchis L., despite obvious (Wallace, 2003, 2004, 2006) and the P. bifolia group (section floral and especially vegetative differences. Toward the Platanthera) in Eurasia in general and England in particular end of the 20th century these species became more com- (Bateman, 2005; Bateman et al., 2009). The P. bifolia group monly assigned to the small, dominantly Eurasian genus is of particular significance because it generated one of the Galearis Rafinesque (1833) and to two monotypic genera: classic textbook examples of selection-mediated co-evolution the exclusively North American Amerorchis Hulte´n (1968) between orchids and their pollinating insects (e.g. Nilsson, and the Chinese Aceratorchis Schlechter (1922). A similarly 1983, 1985; Maad and Nilsson, 2004; reviewed by Hapeman monotypic east Asian genus, Neolindleya Kraenzlin (1897– and Inoue, 1997; Bateman and Sexton, 2008), and has contrib- 1904), was more commonly misassigned to Gymnadenia, uted to contrasting theories of instantaneous saltational specia- again despite obvious floral and especially vegetative differ- tion (summarized by Bateman and Rudall, 2006). ences. Few if any authors suggested close relationships The present ITS analysis includes several additional species among (a) Neolindleya,(b) Amerorchis plus Galearis,(c) from Platanthera sections Platanthera, Limnorchis and Lacera Aceratorchis or (d) Pseudorchis plus Platanthera; moreover, sensu Hapeman and Inoue (1997), together with representa- the supposed close relationship between Pseudorchis and tives of putative sections not recognized by Hapeman and Platanthera was frequently challenged, Pseudorchis often Inoue (Lysiella and Lysias). It also includes two of the three being attributed to Gymnadenia by authors who ignored commonly recognized species of the putative genus several obvious floral differences (cf. Bateman et al., Diphylax, considered to be an upland endemic of the eastern 2006; Delforge, 2006). Himalayas (Tang and Wang, 1940; Cribb, 2001). The Over the last decade, these intuitively inferred boundaries purpose of the study is primarily to complete our revision of of, and relationships among, genera have been systematically generic limits in the Platanthera clade, applying the principle revised (and, in many cases, overturned) by sequence-based of monophyly to the ITS data (where available) and reconsi- phylogenetic analyses using the rapidly evolving nuclear ribo- dering selected morphological characters across the clade. somal internal transcribed spacers (ITS) of nuclear ribosomal We also provide a better informed phylogenetic context for DNA (nrDNA). Pridgeon et al. (1997) and Bateman et al. more focused ongoing evolutionary studies of the P. dilatata (1997) identified a weakly supported Platanthera clade, con- and P. bifolia aggregates. Lastly, we speculate briefly on spe- sisting of Pseudorchis (one species analysed) as sister to ciation mechanisms, notably heterochrony, that appear to be Galearis (two species) plus Platanthera (six species, acting operating within the Platanthera clade. as placeholders for putative sections within this larger genus, estimated at .85 species by Hapeman and Inoue, 1997). These generic relationships were also obtained (again with MATERIALS AND METHODS limited statistical support) by Bateman et al. (2003), in a Fieldwork and analytical materials study benefiting from substantially increased taxon sampling. Pseudorchis (two species) was again shown as basally diver- Data for the full ITS1–5.8S–ITS2 assembly were generated gent, followed by the monotypic Amerorchis, which was by the present authors from 86 accessions. Of these sequences, placed as sister to Galearis (three species). The next branch four were first published by Hapeman and Inoue (1997), nine showed the monotypic Neolindleya as sister to Platanthera by Pridgeon et al. (1997; also Bateman et al., 1997)
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