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Phylogenetics of Tribe Orchideae (Orchidaceae: Orchidoideae)

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Phylogenetics of Tribe Orchideae (Orchidaceae: Orchidoideae) Annals of Botany 110: 71–90, 2012 doi:10.1093/aob/mcs083, available online at www.aob.oxfordjournals.org Phylogenetics of tribe Orchideae (Orchidaceae: Orchidoideae) based on combined DNA matrices: inferences regarding timing of diversification and evolution of pollination syndromes Luis A. Inda1,*, Manuel Pimentel2 and Mark W. Chase3 1Escuela Polite´cnica Superior de Huesca, Universidad de Zaragoza, carretera de Cuarte sn. 22071 Huesca, Spain, 2Facultade de Ciencias, Universidade da Corun˜a, Campus da Zapateira sn. 15071 A Corun˜a, Spain and 3Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK * For correspondence. E-mail [email protected] Received: 3 November 2011 Returned for revision: 9 December 2011 Accepted: 1 March 2012 Published electronically: 25 April 2012 † Background and aims Tribe Orchideae (Orchidaceae: Orchidoideae) comprises around 62 mostly terrestrial genera, which are well represented in the Northern Temperate Zone and less frequently in tropical areas of both the Old and New Worlds. Phylogenetic relationships within this tribe have been studied previously using only nuclear ribosomal DNA (nuclear ribosomal internal transcribed spacer, nrITS). However, different parts of the phylogenetic tree in these analyses were weakly supported, and integrating information from different plant genomes is clearly necessary in orchids, where reticulate evolution events are putatively common. The aims of this study were to: (1) obtain a well-supported and dated phylogenetic hypothesis for tribe Orchideae, (ii) assess appropriateness of recent nomenclatural changes in this tribe in the last decade, (3) detect possible examples of reticulate evolution and (4) analyse in a temporal context evolutionary trends for subtribe Orchidinae with special emphasis on pollination systems. † Methods The analyses included 118 samples, belonging to 103 species and 25 genera, for three DNA regions (nrITS, mitochondrial cox1 intron and plastid rpl16 intron). Bayesian and maximum-parsimony methods were used to construct a well-supported and dated tree. Evolutionary trends in the subtribe were analysed using Bayesian and maximum-likelihood methods of character evolution. † Key Results The dated phylogenetic tree strongly supported the recently recircumscribed generic concepts of Bateman and collaborators. Moreover, it was found that Orchidinae have diversified in the Mediterranean basin during the last 15 million years, and one potential example of reticulate evolution in the subtribe was iden- tified. In Orchidinae, pollination systems have shifted on numerous occasions during the last 23 million years. † Conclusions The results indicate that ancestral Orchidinae were hymenopteran-pollinated, food-deceptive plants and that these traits have been dominant throughout the evolutionary history of the subtribe in the Mediterranean. Evidence was also obtained that the onset of sexual deception might be linked to an increase in labellum size, and the possibility is discussed that diversification in Orchidinae developed in parallel with diversification of bees and wasps from the Miocene onwards. Key words: Character evolution, Diseae, evolution, food deception, Habenariinae, Orchideae, Orchidinae, pollination shifts, rpl16 intron, sexual deception. INTRODUCTION have indicated that some of the characters used by both authors are homoplastic. The abundance of alternative Circumscription of subfamily Orchidoideae (Orchidaceae) has systems has led to considerable disagreement regarding not varied extensively in recent decades from a broadly delimited only subtribal and tribal concepts, but also subfamilial definition comprising all monandrous orchids to a more delimitation. restricted one in which the terrestrial habit, lack of leaf fibres Chase et al. (2003) proposed a series of nomenclatural and presence of root tubers became defining traits changes in Orchidoideae based on the results of phylogenetic (Freudenstein and Rasmussen, 1999; reviewed by Pridgeon studies conducted using plastid and nuclear data (Kores et al., 2001). The wide variation in the definition of et al., 1997; Cameron et al., 1999; Douzerey et al., 1999). Orchidoideae has impinged on the tribal number and arrange- Four tribes, Cranichideae, Diurideae, Codonorchideae and ments proposed. For example, Garay (1972), based mostly on Orchideae, were recognized in the subfamily. Chase et al. floral characters, divided the subfamily into three tribes, (2003) also recognized three subtribes in tribe Orchideae: Orchideae (including Diurideae), Diseae and Disperideae, Brownleeinae, Disinae and Orchidinae. This study focuses on whereas Dressler (1990, 1993), based on vegetative and em- the last group. bryological traits, recognized Diurideae, Diseae (including In Orchidinae, two broad-scale molecular analyses con- Disperidae) and Orchideae. Molecular and morphological ducted by Pridgeon et al. (1997) and Bateman et al. (1997, studies (Pridgeon and Chase, 1995; Kores et al., 1997, 2001) 2003) using ribosomal internal transcribed spacer (ITS) # The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 72 Inda et al. — Phylogeny and evolution of the European orchids regions enabled a new understanding of relationships among phylogenetic studies of these taxa (Cozzolino and Widmer, genera and species. There were three main taxonomic conclu- 2005). The recent development of Bayesian methods of char- sions from these studies. (1) Orchis as previously defined, acter reconstruction (Pagel et al., 2004; Ronquist, 2004; largely based on floral traits, was triphyletic. As a conse- Pagel and Meade, 2006) opens up new insight into the evo- quence, the authors reassigned species from Orchis sensu lution of pollination systems. Finally, new discoveries in the lato (s.l.) to expanded concepts of Neotinea and, especially, orchid fossil record, including fossil pollinia attributed to a Anacamptis. Also, the monospecific genus Aceras was Goodyerinae species and fossil leaves belonging to genera included in Orchis sensu stricto (s.s.). (2) Gymnadenia as pre- Dendrobium and Earina (Conran et al., 2009; reviewed by viously defined was paraphyletic unless genus Nigritella was Gustafsson et al., 2010), have allowed dating of the main di- included, and it was therefore expanded. (3) Finally, versification events in the orchid phylogenetic tree Coeloglossum was nested within the Dactylorhiza clade and (Gustafsson et al., 2010). This temporal framework should transferred to the latter. also be considered in studies of the evolution of pollination Despite several morphological and molecular studies pub- systems. lished on subtribe Orchidinae, a comprehensive phylogenetic The purpose of this study is two-fold. First, we aim to study using molecular data from all three plant genomes is unravel the phylogenetic relationships (including the temporal still lacking. Such a robust phylogenetic analysis could framework) within Orchideae (with special emphasis in sub- offer important insight into the evolution of this complex tribe Orchidinae) using the plastid rpl16 intron (sequences group of plants, especially regarding their pollination generated in this study), nuclear ribosomal (nr)ITS (Bateman syndromes. et al., 2003) and mitochondrial cox1 (Inda et al., 2010). The Orchids offer some of the most striking examples of different regions were used jointly and separately in the phylo- plant–pollinator relationships, and this association has intri- genetic analyses in order to detect possible reticulation events gued scientists for at least the last 200 years (e.g. Darwin, in the evolution of Orchidinae. Second, the dated phylogenetic 1888; reviewed by Van der Cingel, 1995, 2001; Micheneau tree produced here was used to study the evolution of a series et al., 2010). Although plant–pollinator relationships are con- of characters of relevance to pollination biology of these taxa. sidered to be mostly mutualistic, with deception evolving in- The plastid rpl16 gene is involved in the synthesis of a dependently in a limited number of species and families, chloroplast ribosomal protein, and it consists of two exons deception is widespread in orchids. Thus, around one-third separated by a relatively large group II intron (reviewed by of orchid species use this strategy (e.g. Cozzolino and Jordan et al., 1996). This intron was chosen for this phylogen- Widmer, 2005; Smithson, 2009). Orchids are also the only etic study due to the high level of variability that it generally plants in which sexual deception of pollinators has evolved, displays (Wolfe et al., 1987). In orchids, this region has been and this strategy is present in orchid genera from little used; Wallace (2006) used it to analyse the biology of Australasia, Europe and Central and South America some Platanthera populations, and Pillon et al. (2006) (reviewed in Gaskett, 2011). Deception of pollinators (using employed it to assess the relationship between taxonomic sexual or food decoys as attractants) is clearly the norm and phylogenetic diversity in the widespread Eurasian genus among the Mediterranean and European orchids that consti- Dactylorhiza. The combined analysis of independent loci tute the core of subtribe Orchidinae. The evolutionary from different genomes (nuclear, mitochondrial and plastid) origin and significance of deception, both in this subtribe has been considered a good approach to analyse reticulate evo- and in orchids more
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