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Molecular Phylogeny of the Arthrostylidioid Bamboos (Poaceae: Bambusoideae: Bambuseae: Arthrostylidiinae) and New Genus Didymogonyx ⇑ Christopher D

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Molecular Phylogeny of the Arthrostylidioid Bamboos (Poaceae: Bambusoideae: Bambuseae: Arthrostylidiinae) and New Genus Didymogonyx ⇑ Christopher D Molecular Phylogenetics and Evolution 65 (2012) 136–148 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny of the arthrostylidioid bamboos (Poaceae: Bambusoideae: Bambuseae: Arthrostylidiinae) and new genus Didymogonyx ⇑ Christopher D. Tyrrell a, , Ana Paula Santos-Gonçalves b, Ximena Londoño c, Lynn G. Clark a a Dept. of Ecology, Evolution and Organismal Biology, Iowa State University, 251 Bessey Hall, Ames, IA 50011, USA b Universidade Federal de Viçosa, Departamento de Biologia Vegetal, CCB2, Viçosa, 36570-000 Minas Gerais, Brazil c Instituto Vallecaucano de Investigaciones Cientificas (INCIVA), AA 11574, Cali, Colombia article info abstract Article history: We present the first multi-locus chloroplast phylogeny of Arthrostylidiinae, a subtribe of neotropical Received 17 January 2012 woody bamboos. The morphological diversity of Arthrostylidiinae makes its taxonomy difficult and prior Revised 18 May 2012 molecular analyses of bamboos have lacked breadth of sampling within the subtribe, leaving internal Accepted 29 May 2012 relationships uncertain. We sampled 51 taxa, chosen to span the range of taxonomic diversity and mor- Available online 6 June 2012 phology, and analyzed a combined chloroplast DNA dataset with six chloroplast regions: ndhF, trnD-trnT, trnC-rpoB, rps16-trnQ, trnT-trnL, and rpl16. A consensus of maximum parsimony and Bayesian inference Keywords: analyses reveals monophyly of the Arthrostylidiinae and four moderately supported lineages within it. Arthrostylidiinae Six previously recognized genera were monophyletic, three polyphyletic, and two monotypic; Rhipido- Woody bamboo Chloroplast markers cladum sect. Didymogonyx is here raised to generic status. When mapped onto our topology, many of Didymogonyx the morphological characters show homoplasy. Guaduinae Ó 2012 Elsevier Inc. All rights reserved. Phylogeny 1. Introduction (BPG, in preparation; Clark et al., 2007; Sungkaew et al., 2009; Zhang and Clark, 2000). In recent studies, this clade is moderately The bamboos, with about 1450 species, are the only grass sub- supported as sister to Chusqueinae, thus forming a neotropical family (Poaceae: Bambusoideae) to diversify primarily in forests woody bamboo clade, which is sister to the paleotropical woody (BPG, 2006a, 2012; Bouchenak-Khelladi et al., 2010; GPWG, bamboo clade (BPG, in preparation; Sungkaew et al., 2009). 2001). Our understanding of Bambusoideae taxonomy is in a state The results of the BPG (in preparation), Sungkaew et al. (2009) of flux, but the emerging picture based on molecular sequence data and Zhang and Clark (2000) support the monophyly of each sub- (Sungkaew et al., 2009) is that the bamboos evolved into three tribe; however, each is represented by only one to three exemplar main lineages: woody, mainly north temperate species (Arundinar- taxa. Other molecular analyses included more species but discov- ieae), woody tropical species (Bambuseae), and herbaceous bam- ered reciprocally misplaced taxa. Guala et al. (2000) generated a boos (Olyreae). The Bambuseae, including nearly 800 described phylogeny that included seven Arthrostylidiinae and two Guadui- species, is usually classified into seven subtribes, of which four nae species, and found that two presumed Guaduinae taxa were al- are paleotropical and three are neotropical (BPG, 2012; Judziewicz lied with Arthrostylidiinae. Conversely, Ruiz-Sanchez et al. (2008, et al., 1999; Soderstrom and Ellis, 1987). The present work is fo- 2011) found two species of Arthrostylidiinae that resolved within cused on one morphologically diverse but understudied subtribe the Guaduinae based on plastid sequence data. Guala et al. of neotropical woody bamboos. (2000) recovered a topology with moderate support for the two The three neotropical subtribes of Bambuseae are Arthrostyli- subtribes as sister clades, whereas Ruiz-Sanchez et al. (2011) diinae (172 described species), Chusqueinae (160 described spe- recovered a robustly supported Guaduinae sister to the Arthrostyli- cies) and Guaduinae (45 described species) (BPG, 2012; Fisher diinae, but without support. Clark et al. (2007) and Ruiz-Sanchez et al., 2009; Judziewicz et al., 1999). The Arthrostylidiinae plus et al. (2008), however, recovered a robustly monophyletic Guadu- Guaduinae are recovered as a moderately- to well-supported clade inae derived from within a paraphyletic Arthrostylidiinae. The Arthrostylidiinae can be distinguished from other woody bamboo subtribes using branch leaf micromorphology and anat- ⇑ Corresponding author. Present address: Biology Dept., University of New omy (Soderstrom and Ellis, 1987). The leaf blades of Arthrostylidii- Brunswick, P.O. Box 4400, Fredericton NB, Canada E3B 5A3. Fax: +1 506 452 6271. nae possess a unique combination of intercostal sclerenchyma E-mail addresses: [email protected] (C.D. Tyrrell), santosgonc@gmail. com (A.P. Santos-Gonçalves), [email protected] (X. Londoño), lgclark@iastate. fibers in the blades and simple vasculature in the midrib, and the edu (L.G. Clark). leaf blades are basically hypostomatic with papillae usually 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.05.033 C.D. Tyrrell et al. / Molecular Phylogenetics and Evolution 65 (2012) 136–148 137 developed only on the abaxial epidermis. A green marginal stripe Myriocladus the prophylls are cordate in shape. The remaining taxa on the abaxial leaf epidermis (due to reduced or no wax deposi- have triangular shaped prophylls. tion) is also characteristic of Arthrostylidiinae, although this is seen Arthrostylidioid bamboos typically have branch complements occasionally in other neotropical Bambuseae, Olyreae, and even with one dominant branch that arises from the main culm often some Arundinarieae (BPG, 2012; Judziewicz et al., 1999; Soder- with several smaller branches arising laterally, a pattern com- strom and Ellis, 1987; pers. obs. by all authors). In several taxa of monly seen in other woody bamboos (e.g., Bambusa Schreb.). Yet Arthrostylidiinae, stomates have been observed on the adaxial sur- the branch complements of several genera deviate from this face over the abaxial green stripe, but they appear to be restricted arrangement. Atractantha and Athroostachys Benth. exhibit three to this region and it is unknown how general this pattern is (San- to five subequal branches, which may or may not rebranch, arising tos-Gonçalves, 2005). Arthrostylidiinae also have sympodial rhi- from each node; Aulonemia ulei has five to seven subequal zomes, usually a single primary branch bud at each node, branches per node. Actinocladum McClure ex Soderstr., Merostachys rudimentary florets terminating the spikelets or pseudospikelets, Spreng., and Rhipidocladum share an unusual branching morphol- and reflexed pseudopetioles (except in Glaziophyton Franch., Fil- ogy superficially resembling a hand fan. This is termed apsidate gueirasia Guala and some species of Aulonemia Goudot; BPG, 2012). branching (McClure, 1973), referring to the numerous subequal With 172 described species currently classified into 13 genera secondary branches that radiate in an apsidal or vault-like fashion exhibiting a broad range of life forms, Arthrostylidiinae is arguably from a flattened triangular surface (postulated to be a modification the most morphologically diverse subtribe of neotropical woody of the dominant branch); we here use the less technical term bamboo. In comparison, the Chusqueinae include nearly the same ‘‘fan-branching’’ to describe this morphology. In Arthrostylidium, number of described species but only one genus, Chusquea Kunth, Alvimia, Atractantha, Aulonemia, Colanthelia and Elytrostachys McC- is recognized based on a uniform spikelet structure and papillate lure, the branches arise from a raised, ellipsoidal base, called a subsidiary cells (Fisher et al., 2009). The characters most com- promontory, which either continues as a dominant branch (often monly used to distinguish among genera of Arthrostylidiinae, how- producing small lateral branches from its basal nodes) or separates ever, often intergrade in a ‘‘mosaic pattern of variation’’ (Clark and into multiple subequal branches. If the latter, the branches are not Londoño, 1991) making taxonomy and phylogenetic inference dif- orderly as in fan-branching. Arthrostylidium merostachyoides mani- ficult (Judziewicz et al., 1999). McClure (1973) notes that ‘‘such fests a combination of promontory and fan-branching morpholo- divergent attributes are connected by intermediate expressions gies when mature. to form clines, both from one species to another and (in some The most common synflorescence forms in Arthrostylidiinae are cases) within the same specimen.’’ Notable morphological enigmas paniculate or racemose with a straight axis, but this character within the subtribe include internode length pattern, culm leaf exemplifies the mosaic variation seen in the subtribe. Arthrostylidi- blade orientation, vegetative bud prophyll shape, branching archi- um venezuelae, Ar. sarmentosum Pilg., Ar. multispicatum, Ar. ecuado- tecture, synflorescence form, the occurrence of pseudospikelets, rense Judz. & L.G. Clark, Ar. virolinensis Londoño & L.G. Clark, and R. and fruit anatomy. The observations summarized in the following harmonicum all have racemose synflorescences with a geniculate paragraphs are based on decades of field work in the Neotropics or zig-zag axis. This kinked morphology is
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