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Phylogeny and Biogeography of the Tribe Liabeae (Compositae Subfamily Cichorioideae)

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Phylogeny and Biogeography of the Tribe Liabeae (Compositae Subfamily Cichorioideae) TAXON 61 (2) • April 2012: 437–455 Funk & al. • Phylogeny and biogeography of Liabeae Phylogeny and biogeography of the tribe Liabeae (Compositae subfamily Cichorioideae) Vicki A. Funk, Carol Kelloff & Raymund Chan U.S. National Herbarium, Department of Botany, Smithsonian Institution MRC 166, P.O. Box 37012, Washington D.C. 20013, U.S.A. Author for correspondence: Vicki A. Funk, [email protected] Abstract The tribe Liabeae (Compositae) contains ca. 175 species distributed in 18 genera and its members occupy a variety of habitats in the Andes of South America as well as in Mexico, Central America, and the West Indies. The tribe is recognizable by a combination of morphological characters. DNA sequence data from the nuclear ribosomal ITS region and three chloroplast regions (trnL-F, 3′ end of ndhF, matK; a total of more than 5 kb of sequence data) were used to infer a phylogeny. The data were analyzed using maximum parsimony, maximum likelihood, and Bayesian inference. The results support the monophyly of the tribe and show a consistent placement for all genera except Cacosmia. Four well-supported clades are recovered in the remainder of the tribe, all recognized as subtribes. Liabineae (Ferreyranthus, Dillandia, Oligactis, Sampera, Liabum) are the sister group of the rest of the tribe. Sinclairineae (Sinclairiopsis and Sinclairia with segregates Liabellum and Megaliabum) are the sister group of Munnoziinae (Chrysactinium nested inside Munnozia s.l.) plus Paranepheliinae (Stephenbeckia, Micro liabum, Pseudonoseris, Paranephelius, Chionopappus, Philoglossa, Erato). Cacosmia is placed as the sister group of either all the rest of the tribe or of subtribe Liabineae; morphologically its characters are either autapomorphic or plesiomorphic. Bishopanthus could not be confidently placed in any of the subtribes; it is only known from scraps of the type and a molecular study is not possible. The phylogeny slightly alters previous assumptions about the biogeography and it seems that Liabeae originated in the central and northern Andes and spread north and south with several independent introductions into Mexico and Central America and one into the Caribbean. With the exception of the Liabeae (Andes) and Moquineae (Brazil), all of the tribes in the subfamily Cichorioideae are either restricted to or have their basal grade in Africa. Keywords Asteraceae; Caribbean; molecular systematics; North America; South America Supplementary Material Figure S1 is available in the Electronic Supplement to the online version of this article (http://www .ingentaconnect.com/content/iapt/tax). INTRODUCTION Liabeae were subject of a recent review (Dillon & al., 2009) that included an overview of its taxonomic history which need Liabeae are concentrated in the northern and central Andes not be repeated here. However, it is useful to note that all re- although they extend north to central Mexico and the Carib- cent phylogenetic studies have supported the monophyly of bean, and as far south as the mountains of northern Argentina. the tribe and its placement in subfamily Cichorioideae near The tribe contains ca. 175 species arranged in 18 genera and Vernonieae and Arctotidieae and more distantly Cichorieae as such it represents one of the smaller tribes in the family. Its (Funk & Chan, 2009). The paper by Dillon & al. (2009) also component taxa have been variously placed in several tribes, provided a detailed discussion on the structure of the pollen most frequently Vernonieae or Senecioneae. Despite work by and chromosome numbers in relation to the preliminary tree Rydberg (1927), who established the tribe, and subsequent work that they had at the time. Although the present study alters the by Blake (1935), Cabrera (1954), and Sandwith (1956), the tribe tree, it does not affect the conclusions by Dillon & al. (2009) Liabeae was not adopted until Robinson and co-workers pub- that Liabeae completely lack lophate pollen and that the most lished a series of papers bringing the genera together (Robin- likely base chromosome number is x = 9. son & Brettell, 1973, 1974; see Robinson, 1983a for additional The majority of taxa in Liabeae often are confined to a references). small geographic area. Members of the tribe occupy sites in Table 1 documents the center of generic diversity in the forest communities (50–4750 m) or high-elevation areas such Liabeae; it lies in Peru where 13 of the 18 genera are found, fol- as subpáramo, páramo, jalca, and puna (> 3000 m). More rarely lowed by Ecuador (9 genera), Colombia (8), Bolivia (7), Costa they are found in seasonally dry scrub, desert habitats, or dis- Rica and Panama (5 each), Venezuela and Argentina (4), Mex- turbed areas. ico (3), Guatemala, El Salvador, Honduras, and Nicaragua (2), Since the Dillon & al. (2009) paper, a new genus has been and the Caribbean (1). Recently two collections were identified added, Stephanbeckia (Robinson & Funk, 2011), based on a from Acre (Brazil) that extend the range of the tribe into that recent collection from Bolivia by Stephan Beck for whom the country: Liabum acuminatum Rusby (Prance & al. 7310, US) genus is named. It seems that every treatment of the tribe is and L. amplexicaule Poepp. & Endl. (Daly & al. 9631, US). fated to be followed by a new genus (Robinson, 1983a was 437 Funk & al. • Phylogeny and biogeography of Liabeae TAXON 61 (2) • April 2012: 437–455 followed by Bishopanthus, Robinson, 1983b; Funk & al., 1996 MATERIALS AND METHODS by Dillandia, Funk & Robinson, 2001; Funk & al., 2007b by Sampera, Funk & Robinson, 2009; and Dillon & al., 2009 by DNA amplification and sequencing. — DNA extractions Stephanbeckia, Robinson & Funk, 2011). This may happen were performed using DNeasy Plant Mini Kits (Qiagen, Ger- again as the new monotypic genus Inkaliabum D.G. Gut. has mantown, Maryland, U.S.A.) following the manufacturer’s recently been published (Gutiérrez, 2010) but any decision on its instructions, but with an extended incubation period (up to acceptance has been deferred until specimens can be examined. 40 minutes) for herbarium material. For some samples, besides The purpose of this study is to produce a molecular phy- the usual preference for young leaflets, removing debris such as logeny of the Liabeae and to investigate how such a phylogeny epidermal hairs from the plant tissue under a dissecting scope affects our ideas about the origin and evolution of this tribe. proved essential to avoid amplifying contaminating fungal A preliminary version of this tree was used in Dillon & al. DNA. The extracted DNA was further purified using the Ultra (2009) by permission of the authors of this study. However, Clean 15 DNA purification kit (MO BIO Laboratories, Carlsbad, since that paper was published 17 additional taxa have been California, U.S.A.) when the initial PCR amplification was un- added to the ingroup as well as 2.8 kb of matK sequence data successful. The Ultra Clean protocol for large DNA fragments for each taxon. was followed to avoid shearing the extracted genomic DNA. Table 1. Genera of Liabeae (with abbreviations in parentheses) and their distributions. Latitude Genus Abbr. Species Distribution range Bishopanthus H. Rob. 1 Peru, type collection only 3°S–7°S Cacosmia Kunth Cac 3 Ecuador, Peru 0.0°–10.5°S Chionopappus Benth. Chi 1 Peru 7°S–13°S Chrysactinium Wedd. Cry 8 Ecuador, Peru 0.5°N–11°S Dillandia V.A. Funk & H. Rob. Dil 3 Colombia, Peru 1.37°N–5.7°S Erato DC. Era 5 Costa Rica, Panama, Venezuela, Colombia, Ecuador, Peru, Bolivia 11°N–18.5°S Ferreyranthus H. Rob. & Brettell Fer 8 Ecuador, Peru 1°S–15°S Liabum Adans. Lia 37 Mexico, Caribbean, Guatemala, El Salvador, Honduras, Nicaragua, 21.5°N–23°S Costa Rica, Panama, Venezuela, Colombia, Ecuador, Peru, Bolivia, Brazil, Argentina Microliabum Cabrera Mic 5 Bolivia, Argentina 19°S–33°S Munnozia Ruiz & Pav. Mun 46 Costa Rica, Panama, Venezuela, Colombia, Ecuador, Peru, Bolivia, 11°N–23.5°S Argentina Oligactis Cass. Oli 7 Ecuador, Colombia, Venezuela, Costa Rica, Panama 10°N–4°S Paranephelius Poepp. Par 7 Peru, Bolivia, Argentina 3°S–22.5°S Philoglossa DC. Phi 5 Colombia, Ecuador, Peru, Bolivia 0.5°N–17°S Pseudonoseris H. Rob. & Brettell Psu 3 Peru 3°S–17°N Sampera V.A. Funk & H. Rob. Sam 8 Colombia, Ecuador, Peru 4°N–6°S Sinclairiopsis Rydb. Sio 2 Mexico 17°–18°N Sinclairia Hook. & Arn., Liabellum Sin, Lib, 25 Mexico, Guatemala, El Salvador, Honduras, Nicaragua, Costa Rica, 23°N–4°N Rydb., Megaliabum Rydb. Meg Panama, Colombia Stephanbeckia H. Rob. & V.A. Ste 1 Bolivia, type collection only 21°S–22°S Funk 438 TAXON 61 (2) • April 2012: 437–455 Funk & al. • Phylogeny and biogeography of Liabeae All primer sequences and their sources are shown in DNA) for each subsequent reaction cycle. After a total of 40 Table 2. Primers ITS5A and ITS4 were used to amplify and reaction cycles, an additional 7-min extension at 72°C was al- sequence the complete ITS region. For a few samples, it was lowed for completion of unfinished DNA strands. The anneal- necessary to substitute primer ITS5A with ITS5HP and use a ing temperature was raised when necessary to obtain a single higher annealing temperature (up to 58°C) to avoid amplifying fragment product. All PCR products were quantified by agarose fungal ITS sequences. gel electrophoresis with comparison of an aliquot of products Primers trnL-C and trnL-F were used to amplify and se- with a known quantity of a 100-bp DNA ladder (GeneChoice, quence the plastid trnL-F intron and intergenic spacer region. Frederick, Maryland, U.S.A.) visualized with ethidium bromide. The 3′ end of the plastid ndhF gene was amplified and se- The remainder was stored at 4°C until utilized. quenced using primers ndhF1603 and ndhF+607. The entire PCR products used for sequencing were enzymatically pu- matK gene and part of the upstream and downstream flanking rified for sequencing using ExoSAP-IT (USB now Affymetrix, trnK introns were amplified and sequenced in two fragments Cleveland, Ohio, U.S.A.).
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