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Testing Topological Hypotheses of Trapelioid Lichenized Fungi in a Large-Scale Phylogeny of Ostropomycetidae (Lecanoromycetes)

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Testing Topological Hypotheses of Trapelioid Lichenized Fungi in a Large-Scale Phylogeny of Ostropomycetidae (Lecanoromycetes) http://www.diva-portal.org This is the published version of a paper published in Fungal diversity. Citation for the original published paper (version of record): Resl, P., Schneider, K., Westberg, M., Printzen, C., Palice, Z. et al. (2015) Diagnostics for a troubled backbone: testing topologicalhypotheses of trapelioid lichenized fungi in a large-scalephylogeny of Ostropomycetidae (Lecanoromycetes). Fungal diversity, 73: 239-275 http://dx.doi.org/DOI 10.1007/s13225-015-0332-y Access to the published version may require subscription. N.B. When citing this work, cite the original published paper. Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:nrm:diva-1277 Fungal Diversity DOI 10.1007/s13225-015-0332-y Diagnostics for a troubled backbone: testing topological hypotheses of trapelioid lichenized fungi in a large-scale phylogeny of Ostropomycetidae (Lecanoromycetes) Philipp Resl1 & Kevin Schneider1 & Martin Westberg2 & Christian Printzen3 & ZdeněkPalice4,5 & Göran Thor6 & Alan Fryday7 & Helmut Mayrhofer1 & Toby Spribille1,8 Received: 19 November 2014 /Accepted: 13 April 2015 # The Author(s) 2015. This article is published with open access at Springerlink.com Abstract Trapelioid fungi constitute a widespread group of trapelioid clades within Ostropomycetidae. We found of mostly crust-forming lichen mycobionts that are key to strong support for a monophyletic group of nine core understanding the early evolutionary splits in the trapelioid genera but no statistical support to reject the Ostropomycetidae, the second-most species-rich subclass long-standing hypothesis that trapelioid genera are sister of lichenized Ascomycota. The uncertain phylogenetic to Baeomycetaceae or Hymeneliaceae. However, we can resolution of the approximately 170 species referred to reject a sister group relationship to Ostropales with high this group contributes to a poorly resolved backbone for confidence. Our data also shed light on several long- the entire subclass. Based on a data set including 657 standing questions, recovering Anamylopsoraceae nested newly generated sequences from four ribosomal and four within Baeomycetaceae, elucidating two major mono- protein-coding gene loci, we tested a series of a priori and phyletic groups within trapelioids (recognized here as new evolutionary hypotheses regarding the relationships Trapeliaceae and Xylographaceae), and rejecting the monophyly of the genus Rimularia. We transfer eleven species of the latter genus to Lambiella and describe the Electronic supplementary material The online version of this article (doi:10.1007/s13225-015-0332-y) contains supplementary material, genus Parainoa to accommodate a previously misunder- which is available to authorized users. stood species of Trapeliopsis. Past phylogenetic studies in Ostropomycetidae have invoked Bdivergence order^ for * Toby Spribille drawing taxonomic conclusions on higher level taxa. [email protected] Our data show that if backbone support is lacking, con- trasting solutions may be recovered with different or 1 Institute of Plant Sciences, NAWI Graz, University of Graz, added data. We accordingly urge caution in concluding Holteigasse 6, A-8010 Graz, Austria evolutionary relationships from unresolved phylogenies. 2 Department of Botany, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden Keywords Ascomycota . Fungi . Lambiella . 3 Senckenberg Forschungsinstitut und Naturmuseum, Lecanoromycetes . Ostropomycetidae . Parainoa . Senckenberganlage 25, D-60325 Frankfurt am Main, Germany Paraphyly . SOWH test . Taxon sampling 4 Institute of Botany, Academy of Sciences of the Czech Republic, Zámek 1, 252 43 Průhonice, Czech Republic 5 Department of Botany, Faculty of Sciences, Charles University in Introduction Prague, Benátská 2, 128 01 Praha 2, Czech Republic 6 Department of Ecology, Swedish University of Agricultural Early concepts of the phylogenetic relationships of lichenized Sciences, P. O. Box 7044, SE-750 07 Uppsala, Sweden fungi drew heavily on the shape and gross attributes of 7 Herbarium, Department of Plant Biology, Michigan State University, ascomata, ascospores and thallus and the photobionts with East Lansing, MI 48824, USA which they associate (Watson 1929). Starting in the 1960s, 8 Division of Biological Sciences, University of Montana, 32 Campus detailed anatomical studies of the ascus (Letrouit-Galinou Drive, Missoula, MT 59812, USA 1966; Hafellner 1984), ascomatal ontogeny (Letrouit- Fungal Diversity Galinou 1968) and secondary metabolite chemistry 2013: ITS, mtSSU, nuLSU; Otálora and Wedin 2013:mtSSU, (Culberson 1969), as well as increased openness to the possi- RPB1, MCM7; Prieto and Wedin 2013: nuSSU, nuLSU, 5.8S, bility of convergent evolution, led to a shake-up in the classi- mtSSU, RPB1, MCM7 and Prieto et al. 2013,sameloci).The fication of lichenized fungi. One of the numerous enduring pattern of persistent low backbone support is perhaps best legacies of this era is the recognition that emerged in the visualized in the large-scale phylogeny of the group presented 1970s and 1980s of the close relatedness of a group of genera by Miadłikowska et al. (2014,Fig.2). These results convinced with a characteristic non-amyloid, unitunicate ascus and well- us that any resolution of deep relationships of trapelioid fungi defined apical cushion that came to be called the Agyrium-or would require a taxon sampling that encompassed representa- Trapelia-type ascus (Hertel 1970). Using mainly ascus and tives of all key clades and more loci than anything sampled to ontogenetic characters, Lumbsch (1997) proposed uniting 16 date. of these genera into Lecanorales suborder Agyriinae, which Aside from trapelioid fungi, the Ostropomycetidae are wassubsequentlyraisedtothelevelofitsownorder, dominated by two species-rich main groups, usually treated Agyriales (Lumbsch et al. 2001a). However, with the applica- as orders, namely the Ostropales, which have almost always tion of molecular phylogenetics to more members of this been recovered as monophyletic (Kauff and Lutzoni 2002; group it became apparent that ascus characters and ontogeny Miadłikowska et al. 2006, 2014; Lumbsch et al. 2007b; also exhibit convergent evolution, and that several of these Prieto and Wedin 2013;Prietoetal.2013), and the genera are only distantly related, including Anzina and Pertusariales, which usually have not (e.g., Wedin et al. Elixia (Wedin et al. 2005), Miltidea (Widhelm and Lumbsch 2005; Lumbsch et al. 2007a, 2007b;Prietoetal.2013; 2011) and not least the name-giving genus Agyrium (Lumbsch Prieto and Wedin 2013;butseeMiadłikowska et al. et al. 2007a). This latter finding resulted in the taxonomic 2014). Five smaller Bfloating clades^ also feature in most orphaning of the genera remaining and led to several new studies: Arctomiaceae, Baeomycetaceae, Hymeneliaceae, taxonomic proposals, partly reflecting renewed attention to Sarrameanaceae and Schaereriaceae. Phylogenetic hypo- relationships with Baeomycetaceae (e.g., Lumbsch et al. theses including trapelioid fungi repeatedly recover three 2007a; Lumbsch and Huhndorf 2010; Hodkinson and recurring motifs that, though mostly lacking statistical Lendemer 2011). The rump group can now be considered to support and in some cases forming polytomies, form the consist of 11 genera (Trapeliaceae sensu Lumbsch and working basis for evolutionary hypotheses in this group: Huhndorf 2010): Amylora, Coppinsia, Lambiella (Spribille et al. 2014), Lithographa, Placopsis (encompassing 1) trapelioids are sister to the Baeomycetaceae, with or with- Aspiciliopsis and Orceolina), Placynthiella, Ptychographa, out the Hymeneliaceae (Wedin et al. 2005, as Agyriales; Rimularia, Trapelia, Trapeliopsis and Xylographa (Sarea Lumbsch et al. 2007a, as Agyriaceae core group, and was recently excluded by Miadłikowska et al. 2014). Several Lumbsch et al. 2007b, as Agyriales; Lumbsch et al. of these genera were included in Lecanoromycetes subclass 2007c; Bendiksby and Timdal 2013); Ostropomycetidae at the time it was first recognized 2) trapelioids are sister to the Ostropales or sandwiched be- (Miadłikowska and Lutzoni 2004) and have since been rou- tween the Ostropales and Baeomyces+ Arctomia tinely included in phylogenetic hypotheses of that subclass. (Miadłikowska et al. 2006; Prieto et al. 2013;Prietoand For the purposes of the present discussion we will refer to this Wedin 2013); group as the trapelioid fungi (Fig. 1). 3) trapelioids are sister to the Ostropales+Arctomiaceae Several characteristics suggest that trapelioid fungi are a (Miadłikowska et al. 2014, as Trapeliales); this is the only promising study system for evolutionary biology of the lichen study to present statistical support for multiple symbiosis, namely their role as pioneer colonizers (e.g., Jahns relationships. 1982; Ullmann et al. 2007;Raggioetal.2012), their photobiont diversity (Voytsekhovich et al. 2011), and their The lack of support until now for sister group level substrate specificity (Spribille et al. 2008, 2014). Developing relationships in the vicinity of trapelioid fungi makes it them as a model system however requires resolving evolution- impossible to confidently infer order of divergence, and ary relationships that until now have been deeply entangled by extension character evolution, in this speciose group. with other clades of Ostropomycetidae. Since its recognition A deeper locus sampling is in our view the only way a as a subclass by Reeb et al. (2004), nearly all phylogenies of confident assessment of
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