Skip to main content Accessibility help

Phylogenetic relations of European shrubby taxa of the genus Usnea

  • Lauri SAAG (a1), Tiiu TÕRRA (a2), Andres SAAG (a2), Ruth DEL-PRADO (a3) and Tiina RANDLANE (a2)...


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.



Hide All
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: 613627.
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.
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: 412418.
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: 873884.
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: 959975.
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: 5269.
Boni, M. F., Posada, D. & Feldman, M. W. (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176: 10351047.
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540552.
Clerc, P. (1987 a) Systematics of the Usnea fragilescens aggregate and its distribution in Scandinavia. Nordic Journal of Botany 7: 479495.
Clerc, P. (1987 b) On the morphology of soralia in the genus Usnea. Bibliotheca Lichenologica 25: 991027.
Clerc, P. (1997) Notes on the genus Usnea Dill. ex Adanson. Lichenologist 29: 209215.
Clerc, P. (1998) Species concepts in the genus Usnea. Lichenologist 30: 321340.
Clerc, P. (2004) Notes on the genus Usnea Adanson II. Bibliotheca Lichenologica 88: 7990.
Clerc, P. & Herrera-Campos, M. (1997) Saxicolous species of Usnea subgenus Usnea (Lichenized Ascomycetes) in North America. Bryologist 100: 281301.
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: 7181.
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: 812824.
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: 17351753.
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: 125133.
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: 3746.
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: 248254.
Felsenstein, J. (1985) Phylogenies and the comparative method. American Naturalist 125: 115.
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: 397423.
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113118.
Gibbs, M. J., Armstrong, J. S. & Gibbs, A. J. (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16: 573582.
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: 13231330.
Grube, M. & Kroken, S. (2000) Molecular approaches and the concept of species and species complexes in lichenized fungi. Mycological Research 104: 12841294.
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: 3660.
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: 235256.
Herrera-Campos, M. A., Clerc, P. & Nash, T. H. III (1998) Pendulous species of Usnea from the temperate forests in Mexico. Bryologist 101: 303329.
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754755.
Huelsenbeck, J. P., Rannala, B. & Masly, J. P. (2000) Accommodating phylogenetic uncertainty in evolutionary studies. Science 288: 23492350.
Katoh, K. & Toh, H. (2008) Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9: 286298.
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.): 3964. New York: Humana Press.
Keon, D. B. & Muir, P. S. (2002) Growth of Usnea longissima across a variety of habitats in the Oregon coast range. Bryologist 105: 233242.
Kirk, P. M., Cannon, P. F., Minter, D. W. & Stalpers, J. A. (2008) Dictionary of the Fungi. 10th Edition. Wallingford: CAB International.
Knowles, L. L. & Carstens, B. C. (2007) Delimiting species without monophyletic gene trees. Systematic Biology 56: 887895.
Landvik, S., Eriksson, O. E. & Berbee, M. L. (2001) Neolecta:—a fungal dinosaur? Evidence from Β-tubulin amino acid sequences. Mycologia 93: 11511163.
Larget, B. & Simon, D. (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution 16: 750759.
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: 628651.
McCune, B. & Geiser, L. (2009) Macrolichens of the Pacific Northwest. Corvallis: Oregon State University Press.
Maddison, D. R. & Maddison, W. P. (2000) MacClade 4: Analysis of Phylogeny and Character Evolution. Version 4.0. Sunderland, Massachusetts: Sinauer Associates.
Martin, D. & Rybicki, E. (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16: 562563.
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: 98102.
Martin, D. P., Williamson, C. & Posada, D. (2005 b) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21: 260262.
Maynard Smith, J. (1992) Analyzing the mosaic structure of genes. Journal of Molecular Evolution 34: 126129.
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: 3754.
Müller, K. (2005) SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Applied Bioinformatics 4: 6569.
Müller, K. (2006) Incorporating information from length-mutational events into phylogenetic analysis. Molecular Phylogenetics and Evolution 38: 667676.
Nylander, J. A. A. (2004) MrModeltest v2. Uppsala: Evolutionary Biology Centre, Uppsala University. Program distributed by the author.
Ohmura, Y. (2001) Taxonomic study of the genus Usnea (lichenized Ascomycetes) in Japan and Taiwan. Journal of Hattori Botanical Laboratory 90: 196.
Ohmura, Y. (2002) Phylogenetic evaluation of infrageneric groups of the genus Usnea based on ITS regions in rDNA. Journal of Hattori Botanical Laboratory 92: 231243.
Ohmura, Y. (2008) Taxonomy and molecular phylogeny of Usnea rubicunda and U. rubrotincta (Parmeliaceae, lichenized Ascomycotina). Journal of Japanese Botany 83: 347355.
Ohmura, Y. & Kanda, H. (2004) Taxonomic status of section Neuropogon in the genus Usnea elucidated by morphological comparisons and ITS rDNA sequences. Lichenologist 36: 217225.
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.
Padidam, M., Sawyer, S. & Fauquet, C. M. (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265: 218225.
Peck, J. L. E. & McCune, B. (1997) Remnant trees and canopy lichen communities in western Oregon: a retrospective approach. Ecological Applications 7: 11811187.
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: 1375713762.
Rambaut, A. (2009) FigTree v1.3.1. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh. Program distributed by the author.
Randlane, T., Tõrra, T., Saag, A. & Saag, L. (2009) Key to European Usnea species. Bibliotheca Lichenologica 100: 419462.
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 15721574.
Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502504.
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: 7182.
Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16: 11141116.
Simmons, M. P. & Ochoterena, H. (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49: 369381.
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: 137142.
Swofford, D. L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0 b10. Sunderland, Massachusetts: Sinauer Associates.
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: 2132.
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: 489511.
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: 415438.
Weiller, G. F. (1998) Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Molecular Biology and Evolution 15: 326335.
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): 315322. New York: Academic Press Inc.
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): 203222. Dordrecht: Kluwer Academic Publishers.
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: 472484.
Wirtz, N., Printzen, C., Sancho, L. G. & Lumbsch, H. T. (2006) The phylogeny and classification of Neuropogon and Usnea (Parmeliaceae, Ascomycota) revisited. Taxon 55: 367376.


Phylogenetic relations of European shrubby taxa of the genus Usnea

  • Lauri SAAG (a1), Tiiu TÕRRA (a2), Andres SAAG (a2), Ruth DEL-PRADO (a3) and Tiina RANDLANE (a2)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed