Hostname: page-component-76d6cb85b7-hqrjx Total loading time: 0 Render date: 2026-07-15T14:35:49.237Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogenetic relations of European shrubby taxa of the genus Usnea

Published online by Cambridge University Press:  29 July 2011

Lauri SAAG ,
Tiiu TÕRRA ,
Andres SAAG ,
Ruth DEL-PRADO  and
Tiina RANDLANE
Lauri SAAG
Affiliation:
Estonian Biocentre, Riia 23b, 51010 Tartu, Estonia. Email: lauri.saag@ut.ee
Tiiu TÕRRA
Affiliation:
University of Tartu, Institute of Ecology and Earth Sciences, Department of Botany, Lai 38, 51005 Tartu, Estonia.
Andres SAAG
Affiliation:
University of Tartu, Institute of Ecology and Earth Sciences, Department of Botany, Lai 38, 51005 Tartu, Estonia.
Ruth DEL-PRADO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense, E-28040 Madrid, Spain.
Tiina RANDLANE
Affiliation:
University of Tartu, Institute of Ecology and Earth Sciences, Department of Botany, Lai 38, 51005 Tartu, Estonia.
Get access Rights & Permissions [Opens in a new window]

Abstract

This study focuses on European Usnea species with sorediate shrubby thalli, with the aim to evaluate the morphological and chemical separation of species in the light of molecular data. Twenty-two Usnea species, including widely distributed taxa such as U. diplotypus, U. fulvoreagens, U. glabrescens, U. lapponica, U. subfloridana, U. substerilis and U. wasmuthii, were included in the study using Bayesian and maximum parsimony analyses of nuclear ITS and beta-tubulin sequences. The analyses showed that: 1) most taxa that are morphologically well delimited are also distinct by means of molecular characters, 2) shrubby taxa in the section Usnea that are difficult to determine by traditional characters form a group of closely related but still genetically distinct entities, except U. diplotypus and U. substerilis which appear to be polyphyletic. The branch lengths differed largely between two parts of the ITS tree (sections Usnea and Ceratinae). Usnea intermedia is proposed as the sexually reproducing counterpart for the sorediate U. lapponica. Additionally, some new chemotypes of Usnea species were determined.

Keywords

beta-tubulinITSlichenized fungimolecular phylogeneticsParmeliaceae

Information

Type
Research Article
Information
The Lichenologist , Volume 43 , Issue 5 , September 2011 , pp. 427 - 444
Copyright
Copyright © British Lichen Society 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Aguileta, G., Marthey, S., Chiapello, H., Lebrun, M. H., Rodolphe, F., Fournier, E., Gendrault-Jacquemard, A. & Giraud, T. (2008) Assessing the performance of single-copy genes for recovering robust phylogenies. Systematic Biology 57: 613–627.CrossRefGoogle ScholarPubMed
Articus, K. (2004) Phylogenetic Studies in Usnea (Parmeliaceae) and Allied Genera. Acta Universitatis Upsaliensis. Comprehensive summaries of Uppsala Dissertations from the Faculty of Science and Technology 931.Google Scholar
Articus, K., Mattsson, J.-E., Tibell, L., Grube, M. & Wedin, M. (2002) Ribosomal DNA and [beta]-tubulin data do not support the separation of the lichens Usnea florida and U. subfloridana as distinct species. Mycological Research 106: 412–418.CrossRefGoogle Scholar
Blanco, O., Crespo, A., Divakar, P. K., Esslinger, T. L., Hawksworth, D. L. & Lumbsch, H. T. (2004 a) Melanelixia and Melanohalea, two new genera segregated from Melanelia (Parmeliaceae) based on molecular and morphological data. Mycological Research 108: 873–884.CrossRefGoogle ScholarPubMed
Blanco, O., Crespo, A., Elix, J. A., Hawksworth, D. L. & Lumbsch, H. T. (2004 b) A molecular phylogeny and a new classification of parmelioid lichens containing Xanthoparmelia-type lichenan (Ascomycota: Lecanorales). Taxon 53: 959–975.CrossRefGoogle Scholar
Blanco, O., Crespo, A., Ree, R. H. & Lumbsch, H. T. (2006) Major clades of parmelioid lichens (Parmeliaceae, Ascomycota) and the evolution of their morphological and chemical diversity. Molecular Phylogenetics and Evolution 39: 52–69.CrossRefGoogle ScholarPubMed
Boni, M. F., Posada, D. & Feldman, M. W. (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176: 1035–1047.CrossRefGoogle ScholarPubMed
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552.CrossRefGoogle ScholarPubMed
Clerc, P. (1987 a) Systematics of the Usnea fragilescens aggregate and its distribution in Scandinavia. Nordic Journal of Botany 7: 479–495.CrossRefGoogle Scholar
Clerc, P. (1987 b) On the morphology of soralia in the genus Usnea. Bibliotheca Lichenologica 25: 99–1027.Google Scholar
Clerc, P. (1997) Notes on the genus Usnea Dill. ex Adanson. Lichenologist 29: 209–215.CrossRefGoogle Scholar
Clerc, P. (1998) Species concepts in the genus Usnea. Lichenologist 30: 321–340.CrossRefGoogle Scholar
Clerc, P. (2004) Notes on the genus Usnea Adanson II. Bibliotheca Lichenologica 88: 79–90.Google Scholar
Clerc, P. & Herrera-Campos, M. (1997) Saxicolous species of Usnea subgenus Usnea (Lichenized Ascomycetes) in North America. Bryologist 100: 281–301.CrossRefGoogle Scholar
Crespo, A. & Pérez-Ortega, S. (2009) Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenies and morphological characters. Anales del Jardín Botánico de Madrid 66: 71–81.CrossRefGoogle Scholar
Crespo, A., Lumbsch, H. T., Mattsson, J. E., Blanco, O., Divakar, P. K., Articus, K., Wiklund, E., Bawingan, P. A. & Wedin, M. (2007) Testing morphology-based hypotheses of phylogenetic relationships in Parmeliaceae (Ascomycota) using three ribosomal markers and the nuclear RPB1 gene. Molecular Phylogenetics and Evolution 44: 812–824.CrossRefGoogle ScholarPubMed
Crespo, A., Kauff, F., Divakar, P. K., del Prado, R., Pérez-Ortega, S., Amo de Paz, G., Ferencova, Z., Blanco, O., Roca-Valiente, B., Núñez-Zapata, J. et al. (2010) Phylogenetic generic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological, and chemical evidence. Taxon 59: 1735–1753.CrossRefGoogle Scholar
Del-Prado, R., Cubas, P., Lumbsch, H. T., Divakar, P. K., Blanco, O., de Paz, G. A., Molina, M. C. & Crespo, A. (2010) Genetic distances within and among species in monophyletic lineages of Parmeliaceae (Ascomycota) as a tool for taxon delimitation. Molecular Phylogenetics and Evolution 56: 125–133.CrossRefGoogle ScholarPubMed
Divakar, P. K., Molina, M. C., Lumbsch, H. T. & Crespo, A. (2005) Parmelia barrenoae, a new lichen species related to Parmelia sulcata (Parmeliaceae) based on molecular and morphological data. Lichenologist 37: 37–46.CrossRefGoogle Scholar
Douady, C. J., Delsuc, F., Boucher, Y., Doolittle, W. F. & Douzery, E. J. P. (2003) Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Molecular Biology and Evolution 20: 248–254.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985) Phylogenies and the comparative method. American Naturalist 125: 1–15.CrossRefGoogle Scholar
Funk, D. J. & Omland, K. E. (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics 34: 397–423.CrossRefGoogle Scholar
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118.CrossRefGoogle Scholar
Gibbs, M. J., Armstrong, J. S. & Gibbs, A. J. (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16: 573–582.CrossRefGoogle ScholarPubMed
Glass, N. L. & Donaldson, G. C. (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous Ascomycetes. Applied and Environmental Microbiology 61: 1323–1330.CrossRefGoogle ScholarPubMed
Grube, M. & Kroken, S. (2000) Molecular approaches and the concept of species and species complexes in lichenized fungi. Mycological Research 104: 1284–1294.CrossRefGoogle Scholar
Halonen, P., Clerc, P., Goward, T., Brodo, I. M. & Wulff, K. (1998) Synopsis of the genus Usnea (lichenized Ascomycetes) in British Columbia, Canada. Bryologist 101: 36–60.CrossRefGoogle Scholar
Halonen, P., Myllus, L., Ahti, T. & Petrova, V. O. (1999) The lichen genus Usnea in East Fennoscandia. III. The shrubby species. Annales Botanici Fennici 36: 235–256.Google Scholar
Herrera-Campos, M. A., Clerc, P. & Nash, T. H. III (1998) Pendulous species of Usnea from the temperate forests in Mexico. Bryologist 101: 303–329.CrossRefGoogle Scholar
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P., Rannala, B. & Masly, J. P. (2000) Accommodating phylogenetic uncertainty in evolutionary studies. Science 288: 2349–2350.CrossRefGoogle ScholarPubMed
Katoh, K. & Toh, H. (2008) Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9: 286–298.CrossRefGoogle ScholarPubMed
Katoh, K., Asimenos, G. & Toh, H. (2009) Multiple alignment of DNA sequences with MAFFT. In Bioinformatics for DNA Sequence Analysis. Methods in Molecular Biology 537. (Posada, D., ed.): 39–64. New York: Humana Press.CrossRefGoogle Scholar
Keon, D. B. & Muir, P. S. (2002) Growth of Usnea longissima across a variety of habitats in the Oregon coast range. Bryologist 105: 233–242.CrossRefGoogle Scholar
Kirk, P. M., Cannon, P. F., Minter, D. W. & Stalpers, J. A. (2008) Dictionary of the Fungi. 10th Edition. Wallingford: CAB International.Google Scholar
Knowles, L. L. & Carstens, B. C. (2007) Delimiting species without monophyletic gene trees. Systematic Biology 56: 887–895.CrossRefGoogle ScholarPubMed
Landvik, S., Eriksson, O. E. & Berbee, M. L. (2001) Neolecta:—a fungal dinosaur? Evidence from Β-tubulin amino acid sequences. Mycologia 93: 1151–1163.CrossRefGoogle Scholar
Larget, B. & Simon, D. (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution 16: 750–759.CrossRefGoogle Scholar
Lutzoni, F., Wagner, P., Reeb, V. & Zoller, S. (2000) Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homology. Systematic Biology 49: 628–651.CrossRefGoogle ScholarPubMed
McCune, B. & Geiser, L. (2009) Macrolichens of the Pacific Northwest. Corvallis: Oregon State University Press.CrossRefGoogle Scholar
Maddison, D. R. & Maddison, W. P. (2000) MacClade 4: Analysis of Phylogeny and Character Evolution. Version 4.0. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Martin, D. & Rybicki, E. (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16: 562–563.CrossRefGoogle ScholarPubMed
Martin, D. P., Posada, D., Crandall, K. A. & Williamson, C. (2005 a) A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Research and Human Retroviruses 21: 98–102.CrossRefGoogle ScholarPubMed
Martin, D. P., Williamson, C. & Posada, D. (2005 b) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21: 260–262.CrossRefGoogle ScholarPubMed
Maynard Smith, J. (1992) Analyzing the mosaic structure of genes. Journal of Molecular Evolution 34: 126–129.Google Scholar
Molina, M. C., Crespo, A., Blanco, O., Lumbsch, H. T. & Hawksworth, D. L. (2004) Phylogenetic relationships and species concepts in Parmelia s.str. (Parmeliaceae) inferred from nuclear ITS rDNA and Β-tubulin sequences. Lichenologist 36: 37–54.CrossRefGoogle Scholar
Müller, K. (2005) SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Applied Bioinformatics 4: 65–69.CrossRefGoogle ScholarPubMed
Müller, K. (2006) Incorporating information from length-mutational events into phylogenetic analysis. Molecular Phylogenetics and Evolution 38: 667–676.CrossRefGoogle ScholarPubMed
Nylander, J. A. A. (2004) MrModeltest v2. Uppsala: Evolutionary Biology Centre, Uppsala University. Program distributed by the author.Google Scholar
Ohmura, Y. (2001) Taxonomic study of the genus Usnea (lichenized Ascomycetes) in Japan and Taiwan. Journal of Hattori Botanical Laboratory 90: 1–96.Google Scholar
Ohmura, Y. (2002) Phylogenetic evaluation of infrageneric groups of the genus Usnea based on ITS regions in rDNA. Journal of Hattori Botanical Laboratory 92: 231–243.Google Scholar
Ohmura, Y. (2008) Taxonomy and molecular phylogeny of Usnea rubicunda and U. rubrotincta (Parmeliaceae, lichenized Ascomycotina). Journal of Japanese Botany 83: 347–355.Google Scholar
Ohmura, Y. & Kanda, H. (2004) Taxonomic status of section Neuropogon in the genus Usnea elucidated by morphological comparisons and ITS rDNA sequences. Lichenologist 36: 217–225.CrossRefGoogle Scholar
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Padidam, M., Sawyer, S. & Fauquet, C. M. (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265: 218–225.CrossRefGoogle ScholarPubMed
Peck, J. L. E. & McCune, B. (1997) Remnant trees and canopy lichen communities in western Oregon: a retrospective approach. Ecological Applications 7: 1181–1187.CrossRefGoogle Scholar
Posada, D. & Crandall, K. A. (2001) Evaluation of methods for detecting recombination from DNA sequences: Computer simulations. Proceedings of the National Academy of Sciences, USA 98: 13757–13762.CrossRefGoogle ScholarPubMed
Rambaut, A. (2009) FigTree v1.3.1. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh. Program distributed by the author.Google Scholar
Randlane, T., Tõrra, T., Saag, A. & Saag, L. (2009) Key to European Usnea species. Bibliotheca Lichenologica 100: 419–462.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefGoogle ScholarPubMed
Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.CrossRefGoogle ScholarPubMed
Seymour, F. A., Crittenden, P. D., Wirtz, N., Øvstedal, D. O., Dyer, P. S. & Lumbsch, H. T. (2007) Phylogenetic and morphological analysis of Antarctic lichen-forming Usnea species in the group Neuropogon. Antarctic Science 19: 71–82.CrossRefGoogle Scholar
Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16: 1114–1116.CrossRefGoogle Scholar
Simmons, M. P. & Ochoterena, H. (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49: 369–381.CrossRefGoogle ScholarPubMed
Strimmer, K. & Rambaut, A. (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the Royal Society of London, Series B: Biological Sciences 269: 137–142.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0 b10. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S. & Fisher, M. C. (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31: 21–32.CrossRefGoogle ScholarPubMed
Thell, A., Högnabba, F., Elix, J. A., Feuerer, T., Kärnefelt, I., Myllys, L., Randlane, T., Saag, A., Stenroos, S., Ahti, T. et al. (2009) Phylogeny of the cetrarioid core (Parmeliaceae) based on five genetic markers. Lichenologist 41: 489–511.CrossRefGoogle Scholar
Tõrra, T. & Randlane, T. (2007) The lichen genus Usnea (lichenized Ascomycetes, Parmeliaceae) in Estonia with a key to the species in the Baltic countries. Lichenologist 39: 415–438.CrossRefGoogle Scholar
Weiller, G. F. (1998) Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Molecular Biology and Evolution 15: 326–335.CrossRefGoogle ScholarPubMed
White, T. J., Bruns, T., Lee, S. & Taylor, J. W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: a Guide to Methods and Applications (Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J., eds): 315–322. New York: Academic Press Inc.Google Scholar
Will-Wolf, S., Esseen, P.-A. & Neitlich, P. (2002) Monitoring biodiversity and ecosystem function: forests. In Monitoring with Lichens – Monitoring Lichens (Nimis, P. L., Scheidegger, C. & Wolseley, P. A., eds): 203–222. Dordrecht: Kluwer Academic Publishers.CrossRefGoogle Scholar
Wirtz, N., Printzen, C. & Lumbsch, H. T. (2008) The delimitation of Antarctic and bipolar species of neuropogonoid Usnea (Ascomycota, Lecanorales): a cohesion approach of species recognition for the Usnea perpusilla complex. Mycological Research 112: 472–484.CrossRefGoogle ScholarPubMed
Wirtz, N., Printzen, C., Sancho, L. G. & Lumbsch, H. T. (2006) The phylogeny and classification of Neuropogon and Usnea (Parmeliaceae, Ascomycota) revisited. Taxon 55: 367–376.CrossRefGoogle Scholar