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Molecular Phylogenetics and Evolution 63 (2012) 374–387

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Molecular Phylogenetics and Evolution 63 (2012) 374–387 Molecular Phylogenetics and Evolution 63 (2012) 374–387 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Implementing a cumulative supermatrix approach for a comprehensive phylogenetic study of the Teloschistales (Pezizomycotina, Ascomycota) Ester Gaya a, Filip Högnabba b, Ángela Holguin c, Katalin Molnar d, Samantha Fernández-Brime e, Soili Stenroos b, Ulf Arup f, Ulrik Søchting g, Pieter Van den Boom h, Robert Lücking i, Harrie J.M. Sipman j, ⇑ François Lutzoni a, a Department of Biology, Duke University, Durham, NC 27708-0338, USA b Botanical Museum, Finnish Museum of Natural History, FI-00014 University of Helsinki, Finland c Department of Biology, Universidad de Los Andes, Carrera 1, 18A-12 Bogotá, Colombia d Institute of Ecology and Botany, Hungarian Academy of Sciences, 2163 Vácrátót, Alkotmány u. 2-4, Hungary e Department of Plant Biology (Botany Unit), Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 645, 08028 Barcelona, Spain f Botanical Museum, Lund University, Östra Vallgatan 18, SE-223 61 Lund, Sweden g Section on Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark h Arafura 16, NL-5691 JA Son, The Netherlands i Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605-2496, USA j Botanischer Garten und Botanisches Museum Berlin-Dahlem, Königin-Luise-Strasse 6-8, D-14195 Berlin, Germany article info abstract Article history: The resolution of the phylogenetic relationships within the order Teloschistales (Ascomycota, lichen- Received 5 September 2011 forming-fungi), with nearly 2000 known species and outstanding phenotypic diversity, has been hin- Revised 5 January 2012 dered by the limitation in the resolving power that single-locus or two-locus phylogenetic studies have Accepted 13 January 2012 provided to date. In this context, an extensive taxon sampling within the Teloschistales with more loci Available online 28 January 2012 (especially nuclear protein-coding genes) was needed to confront the current taxonomic delimitations and to understand evolutionary trends within this order. Comprehensive maximum likelihood and Keywords: Bayesian analyses were performed based on seven loci using a cumulative supermatrix approach, includ- Bayesian inference ing protein-coding genes RPB1 and RPB2 in addition to nuclear and mitochondrial ribosomal RNA-coding Caliciales Lichens genes. We included 167 taxa representing 12 of the 15 genera recognized within the currently accepted Maximum likelihood Teloschistineae, 22 of the 43 genera within the Physciineae, 49 genera of the closely related orders Lecan- Missing data orales, Lecideales, and Peltigerales, and the dubiously placed family Brigantiaeaceae and genus Sipman- Supermatrix iella. Although the progressive addition of taxa (cumulative supermatrix approach) with increasing Teloschistales amounts of missing data did not dramatically affect the loss of support and resolution, the monophyly of the Teloschistales in the current sense was inconsistent, depending on the loci-taxa combination ana- lyzed. Therefore, we propose a new, but provisional, classification for the re-circumscribed orders Calici- ales and Teloschistales (previously referred to as Physciineae and Teloschistineae, respectively). We report here that the family Brigantiaeaceae, previously regarded as incertae sedis within the subclass Lecanoromycetidae, and Sipmaniella, are members of the Teloschistales in a strict sense. Within this order, one lineage led to the diversification of the mostly epiphytic crustose Brigantiaeaceae and Letrou- itiaceae, with a circumpacific center of diversity and found mostly in the tropics. The other main lineage led to another epiphytic crustose family, mostly tropical, and with an Australasian center of diversity – the Megalosporaceae – which is sister to the mainly rock-inhabiting, cosmopolitan, and species rich Teloschistaceae, with a diversity of growth habits ranging from crustose to fruticose. Our results confirm the use of a cumulative supermatrix approach as a viable method to generate comprehensive phylogenies summarizing relationships of taxa with multi-locus to single locus data. Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction bacteria. Most recent estimates of the number of lichen-forming fungal species have been between 17,500 and 20,000 (i.e., about Lichens are obligate mutualistic ectosymbioses between fungi 20% of all known fungal species; Kirk et al., 2008). This diversity (mycobiont) and either or both photobiont green algae and cyano- is highly concentrated in the most species rich phylum, the Asco- mycota (more specifically within the Leotiomyceta sensu Schoch ⇑ Corresponding author. Fax: +1 919 660 7293. et al., 2009), with >98% of the lichen-forming fungal species classi- E-mail address: fl[email protected] (F. Lutzoni). fied in this phylum and accounting for 40% of the phylum species 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2012.01.012 E. Gaya et al. / Molecular Phylogenetics and Evolution 63 (2012) 374–387 375 richness (Kirk et al., 2008). Within the Leotiomyceta, the great The Megalosporaceae was recognized within the Teloschistales majority of lichen-forming species are found in the third largest (Eriksson, 2005), based on Helms et al. (2003) and Lutzoni et al. class of all Fungi, the Lecanoromycetes. The order Teloschistales (2004). The three genera (Megalospora, Megaloblastenia, and as currently delimited, with nearly 2000 known species and Austroblastenia) classified in this family (with a total of 39 species accounting for >10% of all known lichen-forming fungi (Kirk according to Kirk et al., 2008) are also mostly found in the tropics et al., 2008), is one of the three main orders recognized within and subtropics, with a few exceptions in temperate regions, and the largest subclass of the Lecanoromycetes – the Lecanoromycet- are corticolous. The family Megalosporaceae was initially proposed idae (Hibbett et al., 2007; Kirk et al., 2008; Lumbsch and Huhndorf, by Veˇzda (1974) to unite Megalospora and Bombyliospora De Not. 2010; Miadlikowska et al., 2006). with a few other lichen genera. Hafellner and Bellemère (1981a) The current circumscription of the Teloschistales was estab- considered the ascus structure a good character for such a family, lished by Miadlikowska et al. (2006) in which two suborders were but the Megalosporaceae as defined by Veˇzda was deemed hetero- recognized, the Teloschistineae, which corresponds to the tradi- geneous, and Hafellner and Bellemère (1981c) transferred the tionally circumscribed order (composed of the three families Bombyliospora species with thick spore septa and anthraquinones Letrouitiaceae, Megalosporaceae, and Teloschistaceae), and the (i.e., the B. domingensis group) to the genus Letrouitia. The remain- Physciineae, which contains the Caliciaceae (with about 731 spe- ing Bombyliospora species were synonymized within Megalospora cies) and the Physciaceae (with 510 species) (Kirk et al., 2008). (Hafellner and Bellemère, 1981a). The recognition of this group of lichens at the ordinal level, and The family Brigantiaeaceae (Hafellner and Bellemère, 1981b), is the inclusion of these five families within this order, has been currently considered as a family incertae sedis within the Lecanor- broadly accepted (Hibbett et al., 2007; Kirk et al., 2008; Lumbsch omycetidae, with potentially two genera, Argopsis? and Brigantiaea and Huhndorf, 2007). (Lumbsch and Huhndorf, 2010) and 25 species (Kirk et al., 2008). Growth habits have traditionally played a major role in the clas- Members of this family are found on bark in the tropics and on soil sification within these two suborders. Taxa currently included or decaying vegetation in cool climates. The Brigantiaeaceae was within the Physciineae were initially placed into two separate fam- initially included within the Lecanorales (Hafellner, 1997), and is ilies, Buelliaceae Zahlbruckner (1907) and Physciaceae Zahlbruck- still recognized as such by Kirk et al. (2008). Brigantiaea species ner (1898), based on their respective growth forms, crustose and had been placed within the genus Lopadium Körb. as circumscribed foliose (Zahlbruckner, 1926b). Subsequently, Poelt (1973) unified by Zahlbruckner (1926a,b), which Santesson (1952) found to be both families into the Physciaceae, and Henssen and Jahns (1974) heterogeneous. The latter author recognized six species groups described the suborder Physciineae to encompass the Physciaceae. within Lopadium. One of them, the ‘Brigantiaea group,’ included Ascus and ascospore types have been used traditionally to circum- species of both the Lopadium leucoxanthum group (now Brigantiaea scribe the Physciineae (Bellemère and Letrouit-Galinou, 1981, s.str.) and the Bombyliospora domingensis group (now Letrouitia). 1987; Hafellner, 1984; Matzer and Mayrhofer, 1996; Mayrhofer, Due to the presence of muriform ascospores, the latter two groups 1982, 1984). To date, the delimitation of the Caliciaceae and Phy- were considered to be closely related. However, further characters sciaceae remains controversial. Shared phenotypic similarities by did not support this unification, and Brigantiaea was restricted to members of these two families and several molecular studies sup- the Lopadium leucoxanthum group (Hafellner, 1997). Brigantiaea ported a close relationship within the Lecanorales (e.g., Wedin
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