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Molecular Phylogenetics, Floral Convergence and Systematics Of Botanical Journal of the Linnean Society, 2011, 167, 1–18. With 5 figures Molecular phylogenetics, floral convergence and systematics of Dichromanthus and Stenorrhynchos (Orchidaceae: Spiranthinae) GERARDO A. SALAZAR*, LIDIA I. CABRERA and COYOLXAUHQUI FIGUEROA Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 70-367, 04510 Mexico City, Distrito Federal, Mexico Received 11 January 2011; revised 16 April 2011; accepted for publication 18 May 2011 Contrasting generic concepts of Dichromanthus and Stenorrhynchos held recently by taxonomists were assessed by means of parsimony and Bayesian cladistics analyses of 40 species/22 genera of Spiranthinae and over 2400 base pairs of non-coding nuclear and plastid DNA. Floral structure of relevant taxa was compared using fresh, pickled and herbarium specimens. Our results indicate that a broad concept of Dichromanthus corresponds to a strongly supported monophyletic group sharing several ecogeographical attributes and at least one putative floral synapo- morphy (nectary formed by a narrow channel at the base of the labellum). Dichromanthus s.l. occupies a derived position within the Spiranthes clade, with Deiregyne being strongly supported as its sister genus. Stenorrhynchos, as delimited by most previous taxonomists, is shown to be polyphyletic; monophyly requires a narrower delimi- tation and this narrow concept is strongly supported as belonging in the Stenorrhynchos clade, which also includes members of the genera Eltroplectris, Mesadenella, Pteroglossa and Sacoila. The scant published information on natural pollination and inferences made from flower colouration and morphology suggest convergence in floral characteristics between species of Dichromanthus, Stenorrhynchos and probably other distantly related genera as a result of independent adaptation to pollination by hummingbirds. Bee-pollinated D. michuacanus is recovered in a derived position relative to hummingbird-pollinated Dichromanthus spp., suggesting a secondary reversal in this trait. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 1–18. ADDITIONAL KEYWORDS: convergent evolution – floral morphology – internal transcribed spacer (ITS) – phylogenetics – pollination – trnL/trnF. ‘A point which has been generally overlooked in taxonomy in median carpel apex, a portion of which develops into the orchids is that the characters which result from adapta- the viscidium; Richard, 1817; Vermeulen, 1959; tions to bird-pollination are often striking. These characters Dressler, 1993; Kurzweil, 1998), have been considered are commonly employed by taxonomists in separating genera, of prime importance for generic delimitation in sub- with the result that closely related species may be placed in tribe Spiranthinae Lindl. (Lindley, 1840; Schlechter, distinct genera.’ 1920; Balogh, 1982; Garay, 1982; Greenwood, 1982; L. van der Pijl & C. H Dodson (1966) in Orchid flowers: their Burns-Balogh, 1986; Szlachetko, 1995; Szlachetko, pollination and evolution. Rutkowski & Mytnik, 2005; Rutkowski, Szlachetko & Górniak, 2008) and in other orchids (e.g. Micheneau, Johnson & Fay, 2009). However, reliance on such a INTRODUCTION limited source of character information for classifying > Floral characters, and especially attributes of the a large group such as Spiranthinae ( 400 species; rostellum (the modified, non-receptive part of the Salazar, 2003) by intuitively weighting character similarities and differences, has resulted in perplex- ing discrepancies among the classifications that have *Corresponding author. E-mail: been proposed for Spiranthinae (e.g. see discussion in [email protected] McVaugh, 1985: 295–296). © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 1–18 1 2 SALAZAR ET AL. One of the genera for which delimitation has been genus were its type species, S. speciosum (Jacq.) Rich. inconsistent among the different classifications is ex Spreng. and three additional species morphologi- Stenorrhynchos Rich. ex Sprengl. On the one hand, cally and ecologically similar to it. Recently, Christen- John Lindley (1840) distinguished Stenorrhynchos son (2005) described several additional species fitting from the other five genera he included in his ‘division in this restricted concept of Stenorrhynchos. Through- Spiranthidae’ (= Spiranthinae), namely Pelexia Poit. out this paper, we will refer to Stenorrhynchos in this ex Rich., Sauroglossum Lindl., Spiranthes Rich., narrow sense as Stenorrhynchos sensu stricto (s.s.), in Synnasa Lindl. and Cnemidia Lindl. (now a synonym contrast with the more inclusive delimitation of Szla- of Tropidia Lindl., a member of Epidendroideae chetko and co-workers (e.g. Szlachetko et al., 2005), known not to be closely related to Spiranthinae) by referred to here as Stenorhynchos sensu lato (s.l.). the large showy flowers, large coloured bracts, The genus Dichromanthus Garay was proposed absence of ‘calli’ (swollen nectar glands) at the base of originally to include a single species, D. cinnabarinus the labellum and possession of a hard, sharply (Lex.) Garay (Garay, 1982). This species had been pointed rostellum remnant (i.e. what remains of the placed by both Lindley (1840) and Schlechter (1920) rostellum after the removal of the pollinarium). On in Stenorrhynchos, in spite of its ‘soft, pliable, linear the other hand, in the first modern generic revision of oblong, blunt rostellum’ [remnant] (Garay, 1982). Spiranthinae, Schlechter (1920) raised the number of Balogh (1982), Balogh & Greenwood (1982) and genera to 24, seven of which showed the rostellum Greenwood (1982) also noticed the distinctive rostel- characteristics of Stenorrhynchos sensu Lindley lum structure of ‘Stenorrhynchos’ cinnabarinus, (1840). These seven genera were grouped into one of describing its rostellum remnant as ‘tubular-tipped’ the four greges or generic alliances (Gattungsreichen) and the viscidium as having a ‘plug-like’ extension proposed by Schlechter (1920, 1926), namely grex that fits in the tube prior to its removal by the Raphiorrhyncha. Over half a century later, Garay pollinator. Balogh & Greenwood (1982) proposed the (1982) revised the generic classification of Spiranthi- new genus, Cutsis Burns-Bal., E.W.Greenw. & nae and recognized 44 genera, which he did not group R.González, to accommodate this atypical species, but into alliances. For the species with ‘stenorrhynchoid’ Dichromanthus has nomenclatural priority. Lately, floral attributes, Garay retained most of the generic two contrasting views concerning the circumscription concepts of Schlechter but transferred some species of of Dichromanthus have been held by taxonomists. On Stenorrhynchos sensu Schlechter (1920) to additional the one hand, Salazar and co-workers (Salazar, Chase genera, including Cotylolabium Garay, Dichroman- & Soto, 2002; Salazar, 2003, 2009; Salazar et al., thus Garay, Sacoila Raf. and Skeptrostachys Garay. 2003, 2006; Hágsater et al., 2005; Soto et al., 2007; Almost simultaneously, Balogh (1982) published a Figueroa et al., 2008; Salazar & García-Mendoza, competing classification in which she accepted only 16 2009; Salazar & Ballesteros-Barrera, 2010) embraced genera of Spiranthinae, recognized four alliances a broader concept of Dichromanthus to include three similar to the greges of Schlechter (1920, 1926) and additional species, namely D. aurantiacus (Lex.) embraced generic concepts substantially broader than Salazar & Soto Arenas, D. michuacanus (Lex.) those of both Schlechter and Garay. For instance, she Salazar & Soto Arenas and the recently discovered treated nearly all the previously recognized genera D. yucundaa Salazar & García-Mend. (Salazar & with a stiff, sharply pointed rostellum remnant as García-Mendoza, 2009), based on their vegetative, sections of a broadly defined Stenorrhynchos. reproductive and genetic similarities to D. cinnabari- More recently, Szlachetko (1995) split Spiranthinae nus. This broader generic circumscription will be into three less inclusive subtribes, namely Spiranthi- hereafter referred to as Dichromanthus s.l. On the nae, Cyclopogoninae Szlach. and Stenorrhynchidinae other hand, Szlachetko et al. (2005) considered Szlach. The circumscription of the stenorrhynchoid Dichromanthus as a monotypic genus and included genera in his system largely followed Garay (1982), D. aurantiacus and D. michuacanus (plus a few seg- although subsequently he and his co-workers created regates from these species here considered as their additional genera (see Szlachetko et al., 2005; Rut- synonyms) in the genus Stenorrhynchos,asdid kowski et al., 2008). In contrast, in a synopsis of the Lindley (1840), Schlechter (1920) and Garay (1982). genera of Spiranthinae, Salazar (2003) adopted the Burns-Balogh (1986) also treated Dichromanthus as generic concepts of Garay (1982) to minimize arbi- monotypic but placed D. aurantiacus in Stenorrhyn- trary changes not supported by explicit phylogenetic chos and D. michuacanus in Schiedeella. hypotheses, making minor adjustments to match the Salazar et al. (2003) assessed the phylogenetic rela- results of a molecular phylogenetic study (Salazar tionships of tribe Cranichideae Endl., with a special et al., 2003). The concept of Stenorrhynchos upheld by focus on Spiranthinae, analysing sequence and Salazar, however, was narrower than that of any insertion/deletion (indel) data from five regions of previous treatment. The only species retained in this plastid and nuclear DNA.
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