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Preliminary Phylogeny of Diplostephium (Asteraceae): Speciation Rate and Character Evolution

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Preliminary Phylogeny of Diplostephium (Asteraceae): Speciation Rate and Character Evolution NUMBER 15 VARGAS AND MADRIN˜ A´ N: SPECIATION AND CHARACTER EVOLUTION OF DIPLOSTEPHIUM 1 PRELIMINARY PHYLOGENY OF DIPLOSTEPHIUM (ASTERACEAE): SPECIATION RATE AND CHARACTER EVOLUTION Oscar M. Vargas1,2 and Santiago Madrin˜a´n2 1Section of Integrative Biology and the Plant Resources Center, The University of Texas, 205 W 24th St., Stop CO930, Austin, Texas 78712 U.S.A., email: [email protected] 2Laboratorio de Bota´nica y Sistema´tica Universidad de los Andes, Apartado Ae´reo 4976, Bogota´, D. C., Colombia Abstract: Diplostephium comprises 111 neotropical species that live in high elevation habitats from Costa Rica to Chile. Primarily Andean, the genus seems to have undergone an adaptive radiation indicated by its high number of species, broad morphological variation, and diversification primarily in an ecosystem (pa´ramo) that formed within the last 2–5 my. Internal transcriber spacer (ITS) sequences and several chloroplast markers, rpoB, rpoC1, and psbA-trnH were sequenced in order to infer a preliminary phylogeny of the genus. The chloroplast regions showed no significant variation within the genus. New ITS data were therefore analyzed together with published sequences for generating a topology. Results suggest that Diplostephium and other South American genera comprise a polytomy within which a previously described North American clade is nested. Monophyly of Diplostephium was neither supported nor rejected, but the formation of a main crown clade using different methods of analysis suggests that at least a good portion of the genus is monophyletic. A Shimodaira-Hasegawa test comparing the topology obtained and a constrained one forcing Diplostephium to be monophyletic showed no significant difference between them. Monophyly of some of the previously proposed series of the genus was not supported by the phylogenetic tree. Morphological character mapping results suggest that the high Andean forest tree species are derived from shrubby pa´ramo-puna ancestors, contradicting previous hypotheses about morphological evolution of the genus and documenting an atypical trend of downslope diversification in pa´ramo plants. Keywords: Adaptive radiation, Andes Cordillera, Astereae, Diplostephium, high Andean forest, ITS, morphological evolution, pa´ramo, psbA-trnH, puna, rpoB, rpoC1. Diplostephium Kunth is a genus of 111 DIPLOSTEPHIUM,ROSMARINIFOLIA,andRUPES- known species (Vargas, 2011), distributed TRIA) based on leaf and sinflorescence varia- from Costa Rica to northern Chile in high tion. In 1928 he added 15 more species and elevation cloud forests (2500–3000 m), pa´ra- eliminated the series DENTICULATA and FLOR- mos (3000–4500 m), and puna habitats IBUNDA.Later,Jose´ Cuatrecasas studied the (3800–4200 m). The genus is characterized genus, describing several species and publish- by alternate leaves, white to purplish or bluish ing two revisions (Cuatrecasas, 1943, 1969). ligules, and a pappus formed by two rows of In the second revision, in which 53 species bristles, the outermost one reduced. Mor- known from Colombia were treated, he phologically diverse, growth forms in the subdivided the genus even further, reinstating genus vary from decumbent subshrubs to series DENTICULATA and FLORIBUNDA,and small trees up to 6 m tall, with leaves that incorporating seven new series: ANACTINOTA, range from 3 mm to 12 cm long. Arrange- CORIACEA,CRASSIFOLIA,HUERTASINA,PHYLI- ments of capitula vary from single heads to COIDEA,SAXATILIA,andSCHULTZIANA.Cua- paniculiform or umbelliform sinflorescences. trecasas (1969: 92) proposed a ‘‘phylogenetic’’ Sydney F. Blake compiled the first revision order to these 12 series (Table 1), intuitively of the genus in 1922, recognizing 40 species. polarizing arborescent forms, large leaves, He divided the genus into five series (DEN- multi-capitulate sinflorescences, and small TICULATA,FLORIBUNDA,LAVANDULIFOLIA5 heads as ‘‘atavistic’’ (i.e., ancestral). These LUNDELLIA 15:1–15. 2012 2 LUNDELLIA DECEMBER, 2012 TABLE 1. Cuatrecasas’ circumscription of Diplostephium species for Colombia (1963). Series are ordered by morphological polarization of series that contain atavistic (i.e., ancestral) characteristics (top), to series that present derived characteristics (bottom). Series Species DENTICULATA D. ochraceum, D. bicolor, D. ellipticum, D. dentatum, D. oblongifolium, D. antioquense, D. tenuifolium, D. tamanum, D. mutiscuanum, D. fosbergii, D. grantii, D. ocanense, D. tachirense, D. leiocladum. CRASSIFOLIA D. crassifolium. CORIACEA D. coriaceum. HUERTASINA D. huertasii, D. juliani. FLORIBUNDA D. floribundum, D. tolimense, D.farallonense, D. pittierii, D. cinerascens, D. cayambense. SCHULTZIANA D. juabioyi, D. alveolatum, D schultzii, D. rhododendroides, D. romboidale. ROSMARINIFOLIA D. lacunosum, D. revolutum, D. violaceum, D. heterophyllum, D. cyparissias, D. rosmarinifolium. PHYLICOIDEA D. phylicoides. RUPESTRIA D. rupestre, D. eriophorum, D. weddellii. SAXATILIA D. saxatile, D. romeroi, D. tergocanum. DIPLOSTEPHIUM D. micradenium, D. glutinosum, D. apiculatum, D. nevadense, D. glandulosum, D. spinulosum, D. colombianum, D. parvifolium, D. hartwegii. ANACTINOTA D. anactinotum, D. inesianum. character-states are found in series DENTICU- recognized species (Vargas and Madrin˜a´n, LATA,CORIACEA,andCRASSIFOLIA,which 2006). grow mostly in montane forests. In contrast, Within the Asteraceae, Diplostephium character-states such as a shrubby habit, small has been placed in the tribe Astereae and the thick revolute leaves, single capitula, and large subtribe Hinterhuberinae based on mor- heads were considered derived and occur in phology (Nesom, 1994; Nesom and Robin- the pa´ramo and puna species placed in series son, 2007), along with other South Ameri- RUPESTRIA,ANACTINOTA,andDIPLOSTEPH- can genera such as Floscaldasia Cuatrec., IUM. This hypothesis suggests that extant Flosmutisia Cuatrec., Hinterhubera Sch. Bip. pa´ramo-puna species were derived from high ex Wedd., Llerasia Triana, Laestadia Kunth Andean forest-dwelling ancestors, comparable ex Less., and Oritrophium (Kunth) Cuatrec. to other pa´ramo plant radiations such as the Bonifacino and Sancho (2004) also hypoth- Espeletiinae intensely studied by Cuatrecasas esized that Diplostephium is closely related to (1986). Cuatrecasas’ revision of the Colom- the genus Guynesomia Bonifacino & Sancho. bian species (1969) is considered the last At the molecular level, there are three comprehensive study of the genus because of published sequences of the genus represent- the number of species included and the ing two species (two for the internal rearrangement and description of new series. transcriber spacer nrDNA marker ITS, and Additionally, Cuatrecasas (1986) hypothesized one for the external transcriber spacer ETS). that the main center of speciation and the These have been used in studies focusing on origin of the genus were in Colombia probably the generic relationships within tribe Aster- based this on the fact that more than half of eae (Noyes and Rieseberg, 1999; Brouillet the species of the genus from all the series et al., 2008; Karaman-Castro and Urbatsch, described including the presumed ‘‘ancestral 2009). Noyes and Rieseberg’s study (1999) morphotypes’’ are found in that country. included one ITS sequence of Diplostephium Colombia now has 63 reported species rupestre. Using ITS, Noyes and Rieseberg accounting for ca. 57% of the currently (1999) revealed a North American crown NUMBER 15 VARGAS AND MADRIN˜ A´ N: SPECIATION AND CHARACTER EVOLUTION OF DIPLOSTEPHIUM 3 clade nested in a Southern Hemisphere grade, Here, however, the Diplostephium samples, suggesting a single origin for the North the same used by Brouillet et al. (2008), American Astereae. Diplostephium appeared formed a monophyletic clade in the ITS tree in a South American grade close to the North with moderate support. For the ETS American clade with low support. Noyes and phylogenetic analysis, Karaman-Castro and Rieseberg suggested that the putative ances- Urbatsch (2009) sequenced one species of tors of the North American Astereae were Diplostephium yielding no evidence about South American taxa, and that the Southern the monophyly of the genus. Additionally, Hemisphere basal grade contains the more the authors concluded that the ETS topol- ancient lineages for the tribe. ogy was poorly resolved in comparison to Brouillet et al.’s (2008) study comprised the ITS. a comprehensive ITS phylogenetic analysis Diplostephium appears to be a rapidly of the Astereae tribe using a considerable evolving genus. It is morphologically diverse sample size of genera. The authors of this and has more than 90 species living in the paper concluded that the origin of the tribe Andean pa´ramos and punas, habitats that was probably African, due to the biogeo- were not available until 2–4 mya (van der graphic pattern of the basal lineages in the Hammer and Cleef, 1986). Thus, in order to topology. Based on these results, they attempt to reconstruct a molecular phylo- hypothesized that South American species gentic tree of the genus and test if the genus of the tribe are split between the ‘‘Paleo is monophyletic it is necessary to use South American clade’’ and the ‘‘South markers with high levels of sequence varia- American lineages.’’ The Paleo South Amer- tion. The ITS, the region between the 18S- ican clade is nested between the basal 26S nuclear ribosomal DNA (Baldwin et al., lineages and a New Zealand clade, while 1995), has been proven to be a valuable the South American lineages appear in a marker
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