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Phylogeny and Diversification of Valerianaceae

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Phylogeny and Diversification of Valerianaceae Molecular Phylogenetics and Evolution 63 (2012) 724–737 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny and diversification of Valerianaceae (Dipsacales) in the southern Andes ⇑ Charles D. Bell a, ,1, Adriana Kutschker b,1, Mary T.K. Arroyo c,d a Department of Biological Sciences, University of New Orleans, 2000 Lakeshore Drive, New Orleans, LA 70148, USA b Facultad de Ciencias, Universidad Nacional de la Patagonia San Juan Bosco, Ruta 259-Km 4, 9200 Esquel, Chubut, Argentina c Instituto de Ecologia y Biodiversidad (IEB), Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile d Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile article info abstract Article history: The southern Andean clade of Valeriana provides an excellent model for the study of biogeography. Here Received 20 December 2010 we provide new data to help clarify phylogenetic relationships among the South American valerians, with Revised 11 January 2012 special focus on taxa found in the southern Andes. We found that the southern Andean taxa formed a Accepted 15 February 2012 clade in maximum likelihood and maximum parsimony analyses, and used a Bayesian relaxed clock Available online 7 March 2012 method to estimate divergence times within Valerianaceae. Our temporal results were similar to other studies, but we found greater variance in our estimates, suggesting that the species of Valeriana have Keywords: been on the South American continent for some time, and have been successful at exploiting new niche Andes opportunities that reflects the contemporary radiation. Regardless of the time frame for the radiation of Patagonia Argentina the clade, the uptick in the rate of diversification in Valerianaceae appears correlated with a dispersal Chile event from Central to South America. The appearance of Valeriana in the southern Andes (13.7 Ma) cor- Valerianaceae responds with the transition from closed forest on the western side of the Andes in central Chile to a more open Mediterranean woodland environment. This would suggest that the high species richness of Valerianaceae in South America is the result of multiple, smaller radiations such as the one in the south- ern Andes, that may or may not be geographically isolated. These smaller radiations may also be driven by species moving into new biomes (migration from a temperate to a more Mediterranean-type climate and into alpine). The degree to which different ecological and geological factors interact to drive diversi- fication is difficult to ascertain. Likewise, without a better-resolved phylogeny it is impossible to deter- mine the directionality of dispersal in this group; did they colonize the southern Andes first, then move northward as the central Andean alpine habitat became more widely available or vice versa? Published by Elsevier Inc. 1. Introduction continuous corridor of andean (alpine) vegetation comprised of páramo (11°N–8°S), puna (8–27°S), and southern Andean steppe The Andes are the dominant physiographic feature of western (27–55°S), (Arroyo et al., 2010). On both the western and eastern South America, extending almost the entire length of the continent flanks the páramo is subtended by humid montane cloud forest, for some 9000 km, largely unbroken for more than 66° of latitude. Andean rainforest and tropical rainforest, and occasionally by On strict geological grounds, the Andes have been divided into drier deciduous forest lower down on its eastern side. The main the northern (11°N–5°S), central (5–47°S) and southern Andes organizing component of the mid- and low-elevation vegetation (47–55°S) (Gansser, 1973). Biologists, however, tend to use the types at the latitudes occupied by the puna vegetation and south- terms central and southern Andes differently, referring to the first ern Andean steppe is the so-called ‘‘Arid Diagonal’’ of South as the part of the Andean chain occurring in most of Peru, Bolivia, America (Garleff et al., 1991; Villagrán and Hinojosa, 1997). This northern Chile and north-western Argentina, and the southern arid zone is a product of two severe rain shadows (Arroyo Andes as occurring south of central Chile and corresponding lati- et al., 1988; Placzek et al., 2009) that produce contrasting cli- tudes in Argentina. mates and a wide range of ecological conditions and vegetation On a global scale the Andean region is characterized by signif- types on either side of the Andes at any given latitude. icant vegetation diversity and high species-richness and ende- The biogeographical consequences of the Andean uplift during mism (Barthlott et al., 2005). At elevations above tree line (or the mid-Miocene–Pliocene (Gregory-Wodzicki, 2000; Ramos and its phytogeographic equivalent), is found the world´ s largest Ghiglione, 2008; Rech et al., 2006; Graham, 2009) have been inves- tigated in a number of genera (e.g., Simpson and Todzia, 1990; Ezcurra, 2002; Rauscher, 2002; Sánchez-Baracaldo, 2004; Bell ⇑ Corresponding author. and Donoghue, 2005a; Hughes and Eastwood, 2006; Jaramillo E-mail address: [email protected] (C.D. Bell). 1 These authors contributed equally to the completion of this manuscript et al., 2006; Herskovitz et al., 2006; Hoot et al., 2008; Scherson 1055-7903/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.ympev.2012.02.015 C.D. Bell et al. / Molecular Phylogenetics and Evolution 63 (2012) 724–737 725 et al., 2008; Simpson et al., 2009). However, most studied to date We amplified and sequenced 9 chloroplast regions, 6 of which are restricted to a few vegetation types or are predominantly trop- have not previously been examined in Valerianaceae, including: ical or temperate groups, thus impeding a broader understanding trnS-trnG intergenic space with primers of Hamilton (1999), and of the evolutionary connection between different habitats and a the psbM-trnD intergenic spacer was amplified using the primers more complete view of Andean biogeography. of Lee and Wen (2004). We used primers published by Ford et al. Among the South American taxa, species of Valerianaceae are (2009) for amplification and sequencing the rpoC1, accD, ndhJ, well represented in the high, mid, and low elevation habitats and accD regions. Information about primers for the matK, trnK in- throughout the entire length of the Andean region. With approxi- tron, and trnL-F region can be found in Bell (2007). mately 350 species, Valerianaceae represents the largest radiation In addition to the chloroplast genome markers, we amplified within Dipsacales (Borsini, 1966; Backlund, 1996; Bell, 2004, 2007; and sequenced the nuclear ribosomal ITS region using the primers Bell and Donoghue, 2005a). The family contains annual and peren- ITS2, ITS3 (in some cases, ITS3B), ITS4, and ITS5. For the ITS region, nial herbs and shrubs characterized by: (1) thyrsic inflorescences we cloned many of the PCR products using an Invitrogen Topo-TA with perfect or unisexual, symmpetalous, asymmetric flowers; cloning kit (Invitrogen, Inc., Carlsbad, California). We then screened (2) corolla epigynous, sometimes with a gibba or spur at the base 8–16 clones per sample to evaluate sequences heterogeneity. of corolla tube; (3) basically three-carpelate ovaries with one fer- We sequenced all regions via dye terminator cycle sequencing tile carpel with axillary placentation and one anatropus ovule; using the protocol specified by the manufacturer and then visual- and (4) fruits with the persistent pappus-like calyx (sometimes ized on an ABI 3100 capillary sequencer. Next, we visualized and leafy or absent) and lack of endosperm in the ripe seed (except edited sequence fragments using the computer package Sequen- Triplostegia)(Borsini, 1966; Eriksen, 1989a, 1989b; Kutschker, cher (Gene Codes Corporation, Ann Arbor MI) to build contig se- 2009). Although Valerianaceae, like many dipsacalean taxa, occur quences. Finally, we aligned all sequences visually with the help widely in the northern hemisphere, the bulk of the species are of MacClade version 4.0 (Maddison and Maddison, 2000). All found in the Andean region of South America where several intro- aligned matrices are available in TreeBase (Accession #S1117; ductions from the northern hemisphere have occurred (Bell, 2004, www.treebase.org) or on request from the authors and all se- 2007; Bell and Donoghue, 2005a). The distribution of Valeriana- quences were deposited in GenBank (see Appendix 1). ceae in many Andean vegetation types and throughout the length of the South American Andes makes it ideal for detailed phyloge- 2.1. Phylogenetic analyses and divergence time estimation netic analyses of the association between habitat types. Of the approximately 250 species of Valerianaceae in South Maximum parsimony searches were conducted using heuristic America, 40 taxa are restricted to the Andes of Argentina and Chile. search methods with tree bisection reconnection (TBR) branch Species in the southern Andes are found mostly in mid- and low- swapping, collapse of zero-length branches, and all characters elevation habitats, with some alpine species and a least two re- weighted equally. The analyses were repeated 100 times with stricted to the upper alpine. These grow mainly in open to shaded the RANDOM ADDITION option. Sets of equally most parsimonious habitats and exceptionally in wet boggy areas. Species in northern trees were summarized with a strict consensus tree. Bootstrap Chile and northwestern
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