Organisms Diversity & Evolution

, Volume 16, Issue 3, pp 497–524 | Cite as

Evaluation of traditionally circumscribed species in the lichen-forming genus Usnea, section Usnea (Parmeliaceae, Ascomycota) using a six-locus dataset

  • Kristiina Mark
  • Lauri Saag
  • Steven D. Leavitt
  • Susan Will-Wolf
  • Matthew P. Nelsen
  • Tiiu Tõrra
  • Andres Saag
  • Tiina Randlane
  • H. Thorsten Lumbsch
Original Article

Abstract

Recent taxonomic and DNA sequence-based studies in several groups of lichen-forming fungi have revealed incongruence between the morphological and molecule-based circumscriptions of species. While the cosmopolitan genus Usnea is well-known and easily recognized by the yellowish beard-like thallus with central cord, delimitation of many Usnea species is difficult due to the high variation and complexity of diagnostic characters. In this study, we assessed the monophyly of 18 species from section Usnea occurring in North America and Europe, including sorediate and sexually reproducing taxa with both pendent and shrubby thalli. Six nuclear markers (ribosomal internal transcribed spacer (ITS) and intergenic spacer (IGS), and protein-coding beta-tubulin, MCM7, RPB1 and RPB2) were sequenced for 144 samples. All analyzed loci show weak genetic structure and short branch lengths in single-locus topologies, suggesting recent diversification history of the sampled taxa. Concatenated, multi-locus analyses conducted in Bayesian and maximum likelihood frameworks, as well as coalescent-based species delimitation and species tree methods, recover several distinct clades, some represent traditional morphology-based species (Usnea cavernosa, U. praetervisa, U. silesiaca, U. wasmuthii), while others form clusters of two or more species (Usnea floridaU. subfloridana, U. fulvoreagensU. glabrescens, U. barbataU. chaetophoraU. dasopogaU. diplotypus, U. barbataU. intermediaU. lapponicaU. substerilis). We propose synonymization of U. substerilis under U. lapponica. The status of several other species within intermixed clusters requires further evaluation with more extensive sampling and the inclusion of more variable markers before taxonomic consequences can be considered. A new species, Usnea parafloridana is described from Wisconsin, USA.

Keywords

Lichenized fungi Rapid radiation Species delimitation Species trees Taxonomy Usnea 

Supplementary material

13127_2016_273_MOESM1_ESM.pdf (339 kb)
Online Resource 1Fig. S1–S6 Majority rule consensus trees inferred from ML analysis on ITS (Fig. S1), IGS (Fig. S2), beta-tubulin (Fig. S3), MCM7 (Fig. S4), RPB1 (Fig. S5) and RPB2 (Fig. S6) datasets together with nonparametric bootstrap support (BP) and posterior probability (PP) values from Bayesian inference. Above branch is indicated ML bootstrap probabilities (BP) and below Bayesian posterior probability (PP) scores. Branches marked in bold indicate strong support (BP ≥ 70 and PP ≥ 0.95) for specified clade. Scale bar shows the number of substitutions per site (PDF 339 kb)
13127_2016_273_MOESM2_ESM.pdf (136 kb)
Online Resource 2Fig. S7 Majority rule consensus tree of all available Usnea fulvoreagens, U. glabrescens s.str. and U. pacificana sequences (Table 1) with U. silesiaca as an outgroup, based on six concatenated loci, inferred in RAxML. Clade bootsrap probabilites (BP) are given above branch and strongly supported clades (BP ≥ 70 %) are marked in bold. Scale bar shows the number of substitutions per site. In brackets are given specimen code, country, and secondary chemistry. Secondary metabolites in fulvoreagens-glabrescens clade: bar − barbatic acid; BMY − baeomycesic acid; NSTI − norstictic acid; pro − protocetraric acid; SAL − salazinic acid; SQU − squamatic acid; STI-comp − stictic acid complex with connorstictic cryptostictic acids; unid rfcl x − unidentified substance from reference class x. Capital letters denotes major compounds in chemotype, lower case accessory substances (PDF 136 kb)
13127_2016_273_MOESM3_ESM.pdf (274 kb)
Online Resource 3Fig. S8 Majority rule consensus tree of all studied Usnea parafloridana specimens with some representatives from florida-subfloridana and wasmuthii clades, based on six concatenated loci, inferred in RAxML. Clade bootsrap probabilites (BP) are given above branch and strongly supported clades (BP ≥ 70 %) are marked in bold. Scale bar shows the number of substitutions per site. In brackets are given specimen codes and secondary chemistry. Secondary metabolites in U. parafloridana: NSTI − norstictic acid; SAL − salazinic acid; unid rfcl x − unidentified substance from reference class x. Capital letters denotes major compounds in chemotype, lower case accessory substances (PDF 274 kb)
13127_2016_273_MOESM4_ESM.pdf (1.4 mb)
Online Resource 4Fig. S9 Examples of lichen substances of some studied Usnea specimens, incl. U. parafloridana sp. nov., identified in thin layer chromatography analyses. Secondary metabolites are visualized in solvent system A, after treatment with sulphuric acid and heating (Orange et al. 2001). Identified secondary metabolites: al – alectorialic acid; bar − barbatic acid; bmy − baeomycesic acid; cnsti – connorstictic acid; csti – cryptostictic acid; nsti – norstictic acid; sal – salazinic acid; squ − squamatic acid; sti – stictic acid; tha – thamnolic acid; usn − usnic acid (PDF 1398 kb)

References

  1. Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716–723.CrossRefGoogle Scholar
  2. Articus, K. (2004a). Neuropogon and the phylogeny of Usnea s.l. (Parmeliaceae, Lichenized Ascomycetes). Taxon, 53(4), 925–934.CrossRefGoogle Scholar
  3. Articus, K. (2004b). Phylogenetic studies in Usnea (Parmeliaceae) and allied genera (Vol. 931, Acta Universitatis Upsaliensis. Comprehensive summaries of Uppsala Dissertations from the Faculty of Science and Technology). Uppsala: Acta Universitatis Upsaliensis.Google Scholar
  4. Articus, K., Mattsson, J.-E., Tibell, L., Grube, M., & Wedin, M. (2002). Ribosomal DNA and β-tubulin data do not support the separation of the lichens Usnea florida and U. subfloridana as distinct species. Mycological Research, 106(4), 412–418.CrossRefGoogle Scholar
  5. Boni, M. F., Posada, D., & Feldman, M. W. (2007). An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics, 176, 1035–1047.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., et al. (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10(4), e1003537. doi:10.1371/journal.pcbi.1003537.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous Ascomycetes. Mycologia, 91(3), 553–556.CrossRefGoogle Scholar
  8. Carstens, B. C., & Knowles, L. L. (2007). Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Systematic Biology, 56(3), 400–411.PubMedCrossRefGoogle Scholar
  9. Carstens, B. C., Pelletier, T. A., Reid, N. M., & Satler, J. D. (2013). How to fail at species delimitation. Molecular Ecology, 22(17), 4369–4383.PubMedCrossRefGoogle Scholar
  10. Clerc, P. (1984). Contribution à la revision de la systématique des Usnées (Ascomycotina, Usnea) d'Europe. I. Usnea florida (L.) Wigg. emend. Clerc. Cryptogamie. Bryologie and Lichénologie, 5, 333–360.Google Scholar
  11. Clerc, P. (1987). Systematics of the Usnea fragilescens aggregate and its distribution in Scandinavia. Nordic Journal of Botany, 7(4), 479–495.CrossRefGoogle Scholar
  12. Clerc, P. (1998). Species concepts in the genus Usnea (lichenized Ascomycetes). The Lichenologist, 30(4–5), 321–340.Google Scholar
  13. Clerc, P. (2004). Notes on the genus Usnea Adanson. II. Bibliotheca Lichenologica, 88, 79–90.Google Scholar
  14. Clerc, P. (2007). Usnea. In T. H. Nash III, C. Gries, & F. Bungartz (Eds.), Lichen flora of the Greater Sonoran Desert Region (Vol. 3) (p. 327). Tempe: Arizona State.Google Scholar
  15. Clerc, P. (2011). Usnea. In A. Thell, & R. Moberg (Eds.), Nordic Lichen Flora 4. (pp. 107–127): Museum of Evolution, Uppsala University.Google Scholar
  16. R Core Team (2014). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
  17. Cornejo, C., Chabanenko, S., & Scheidegger, C. (2009). Phylogenetic analysis indicates transitions from vegetative to sexual reproduction in the Lobaria retigera group (Lecanoromycetidae, Ascomycota). The Lichenologist, 41(03), 275–284.CrossRefGoogle Scholar
  18. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772–772.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Delport, W., Poon, A. F., Frost, S. D., & Pond, S. L. (2010). Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics, 26, 2455–2457.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Drummond, A. J., Ho, S. Y., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology, 4(5), e88. doi:10.1371/journal.pbio.0040088.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969–1973.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution, 63(1), 1–19.PubMedCrossRefGoogle Scholar
  23. Edwards, D. L., & Knowles, L. L. (2014). Species detection and individual assignment in species delimitation: can integrative data increase efficacy? Proceedings of the Royal Society B, 281(1777), 20132765. doi:10.1098/rspb.2013.2765.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Elix, J. A., Corush, J., & Lumbsch, H. T. (2009). Triterpene chemosyndromes and subtle morphological characters characterise lineages in the Physcia aipolia group in Australia (Ascomycota). Systematics and Biodiversity, 7(4), 479–487.CrossRefGoogle Scholar
  25. Fos, S., & Clerc, P. (2000). The lichen genus Usnea on Quercus suber in Iberian cork-oak forests. The Lichenologist, 32(1), 67–88.CrossRefGoogle Scholar
  26. Fujita, M. K., Leaché, A. D., Burbrink, F. T., McGuire, J. A., & Moritz, C. (2012). Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology & Evolution, 27(9), 480–488.CrossRefGoogle Scholar
  27. Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology, 2(2), 113–118.PubMedCrossRefGoogle Scholar
  28. Giarla, T. C., & Esselstyn, J. A. (2015). The challenges of resolving a rapid, recent radiation: empirical and simulated phylogenomics of Philippine shrews. Systematic Biology. doi:10.1093/sysbio/syv029.PubMedGoogle Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. Givnish, T. J. (2015). Adaptive radiation versus ‘radiation’ and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution. New Phytologist, 207(2), 297–303.PubMedCrossRefGoogle Scholar
  31. 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(4), 1323–1330.PubMedPubMedCentralGoogle Scholar
  32. Halonen, P. (2000). Usnea pacificana, sp. nov. and U. wasmuthii (Lichenized Ascomycetes) in Pacific North America. The Bryologist, 103(1), 38–43.CrossRefGoogle Scholar
  33. 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
  34. Halonen, P., Myllys, L., Ahti, T., & Petrova, O. V. (1999). The lichen genus Usnea in East Fennoscandia. III. The shrubby species. Annales Botanici Fennici, 36, 235–256.Google Scholar
  35. Heled, J., & Drummond, A. J. (2010). Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27(3), 570–580.PubMedCrossRefGoogle Scholar
  36. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8), 754–755.PubMedCrossRefGoogle Scholar
  37. Jones, G. R. (2015). STACEY: species delimitation and phylogeny estimation under the multispecies coalescent. doi:10.1101/010199. Preprint in biorxiv.org.Google Scholar
  38. Jones, G., Zeynep, A., & Oxelman, B. (2014). DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics, 31, 991–998.PubMedCrossRefGoogle Scholar
  39. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Katoh, K., & Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics, 9(4), 286–298.PubMedCrossRefGoogle Scholar
  41. Kelly, L. J., Hollingsworth, P. M., Coppins, B. J., Ellis, C. J., Harrold, P., Tosh, J., et al. (2011). DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context. New Phytologist, 191(1), 288–300.PubMedCrossRefGoogle Scholar
  42. Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.PubMedCrossRefGoogle Scholar
  43. Knowles, L. L., & Kubatko, L. S. (2010). Estimating species trees: practical and theoretical aspects. Hoboken: Wiley-Blackwell.Google Scholar
  44. Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H., & Frost, S. D. W. (2006). GARD: a genetic algorithm for recombination detection. Bioinformatics, 22(24), 3096–3098.PubMedCrossRefGoogle Scholar
  45. Kraichak, E., Divakar, P. K., Crespo, A., Leavitt, S. D., Nelsen, M. P., Lücking, R., et al. (2015a). A tale of two hyper-diversities: diversification dynamics of the two largest families of lichenized fungi. Scientific Reports, 5, 10028. doi:10.1038/srep10028.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kraichak, E., Lücking, R., Aptroot, A., Beck, A., Dornes, P., John, V., et al. (2015b). Hidden diversity in the morphologically variable script lichen (Graphis scripta) complex (Ascomycota, Ostropales, Graphidaceae). Organisms Diversity & Evolution, 15(3), 447–458.CrossRefGoogle Scholar
  47. Leaché, A. D. (2009). Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards (Sceloporus). Systematic Biology, 58(6), 547–559.PubMedCrossRefGoogle Scholar
  48. Leavitt, S. D., Fankhauser, J. D., Leavitt, D. H., Porter, L. D., Johnson, L. A., & St. Clair, L. L. (2011a). Complex patterns of speciation in cosmopolitan "rock posy" lichens – discovering and delimiting cryptic fungal species in the lichen-forming Rhizoplaca melanophthalma species-complex (Lecanoraceae, Ascomycota). Molecular Phylogenetics and Evolution, 59(3), 587–602.PubMedCrossRefGoogle Scholar
  49. Leavitt, S. D., Johnson, L., & St. Clair, L. L. (2011b). Species delimitation and evolution in morphologically and chemically diverse communities of the lichen-forming genus Xanthoparmelia (Parmeliaceae, Ascomycota) in western North America. American Journal of Botany, 98(2), 175–188.PubMedCrossRefGoogle Scholar
  50. Linda in Arcadia. (2013). Usnea dasopoga, a name to be reinstated for U. filipendula, and its orthography. Taxon, 62(3), 604–605.CrossRefGoogle Scholar
  51. Lindblom, L., & Ekman, S. (2006). Genetic variation and population differentiation in the lichen-forming ascomycete Xanthoria parietina on the island Storfosna, central Norway. Molecular Ecology, 15(6), 1545–1559.PubMedCrossRefGoogle Scholar
  52. Liu, Y. L., Whelen, S., & Hall, B. D. (1999). Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution, 16, 1799–1808.PubMedCrossRefGoogle Scholar
  53. Lumbsch, H. T., & Wirtz, N. (2011). Phylogenetic relationships of the neuropogonoid core group in the genus Usnea (Ascomycota: Parmeliaceae). The Lichenologist, 43(6), 553–559.CrossRefGoogle Scholar
  54. Lumbsch, H. T., Ahti, T., Altermann, S., Amo De Paz, G., Aptroot, A., Arup, U., et al. (2011). One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa, 18, 1–127.CrossRefGoogle Scholar
  55. Madden, T. (2002). The BLAST sequence analysis tool. In J. McEntyre & J. Ostell (Eds.), The NCBI handbook. Bethesda: National Center for Biotechnology Information.Google Scholar
  56. Maddison, W. P. (1997). Gene trees in species trees. Systematic Biology, 46(3), 523–536.CrossRefGoogle Scholar
  57. Maddison, W. P., & Maddison, D. R. (2011). Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org.Google Scholar
  58. Martin, D., & Rybicki, E. (2000). RDP: detection of recombination amongst aligned sequences. Bioinformatics, 16, 562–563.PubMedCrossRefGoogle Scholar
  59. Martin, D. P., Posada, D., Crandall, K. A., & Williamson, C. (2005). A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Research and Human Retroviruses, 21, 98–102.PubMedCrossRefGoogle Scholar
  60. Martin, D. P., Lemey, P., Lott, M., Moulton, V., Posada, D., & Lefeuvre, P. (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics, 26(19), 2462–2463.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Mason-Gamer, R. J., & Kellogg, E. A. (1996). Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology, 45(4), 524–545.CrossRefGoogle Scholar
  62. Matheny, P. B., Liu, Y. J., Ammirati, J. F., & Hall, B. D. (2002). Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). American Journal of Botany, 89(4), 688–698.PubMedCrossRefGoogle Scholar
  63. Maynard Smith, J. (1992). Analyzing the mosaic structure of genes. Journal of Molecular Evolution, 34, 126–129.Google Scholar
  64. McCune, B. (2005). Usnea in Pacific Northwest. http://people.oregonstate.edu/~mccuneb/Usnea.PDF Accessed 25 Feb 2015.
  65. McEvoy, M., Nybakken, L., Solhaug, K. A., & Gauslaa, Y. (2006). UV triggers the synthesis of the widely distributed secondary lichen compound usnic acid. Mycological Progress, 5(4), 221–229.CrossRefGoogle Scholar
  66. Molina, M. C., Del-Prado, R., Divakar, P. K., Sánchez-Mata, D., & Crespo, A. (2011). Another example of cryptic diversity in lichen-forming fungi: the new species Parmelia mayi (Ascomycota: Parmeliaceae). Organisms Diversity & Evolution, 11(5), 331–342.CrossRefGoogle Scholar
  67. Motyka, J. (1936). Lichenum generis Usnea studium monographicum. Pars systematica (2 vol. in 1 bd.). Lublin: Editio et proprietas auctoris.Google Scholar
  68. 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
  69. 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
  70. Ohmura, Y., & Kanda, H. (2004). Taxonomic status of section Neuropogon in the genus Usnea elucidated by morphological comparisons and ITS rDNA sequences. The Lichenologist, 36(3–4), 217–225.CrossRefGoogle Scholar
  71. O'Meara, B. C., Ané, C., Sanderson, M. J., & Wainwright, P. C. (2006). Testing for different rates of continuous trait evolution using likelihood. Evolution, 60(5), 922–933.PubMedCrossRefGoogle Scholar
  72. Orange, A., James, P. W., & White, F. J. (2001). Microchemical methods for the identification of Lichens. London: British Lichen Society.Google Scholar
  73. Padidam, M., Sawyer, S., & Fauquet, C. M. (1999). Possible emergence of new geminiviruses by frequent recombination. Virology, 265, 218–225.PubMedCrossRefGoogle Scholar
  74. Poelt, J. (1970). Das Konzept der Artenpaare bei den Flechten. Vorträge aus dem Gesamtgebiet der Botanik, Neue Folge, 4, 187–198.Google Scholar
  75. Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., et al. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55(4), 595–609.PubMedCrossRefGoogle Scholar
  76. Posada, D., & Crandall, K. A. (2001). Evaluation of methods for detecting recombination from DNA sequences: computer simulations. PNAS, 98, 13757–13762.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Rambaut, A. (2009). FigTree. Version 1.3.1. http://tree.bio.ed.ac.uk/software/figtree. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh.
  78. Rambaut, A., & Drummond, A. (2007). Tracer. Version 1.4. http://beast.bio.ed.ac.uk.Google Scholar
  79. Rambaut, A., & Drummond, A. (2012a). LogCombiner Version 1.7.2. http://beast.bio.ed.ac.uk.Google Scholar
  80. Rambaut, A., & Drummond, A. (2012b). TreeAnnotator Version 1.7.2. http://beast.bio.ed.ac.uk.Google Scholar
  81. Randlane, T., Tõrra, T., Saag, A., & Saag, L. (2009). Key to European Usnea species. The Diversity of Lichenology: Jubilee Volume, 100(100), 419–462.Google Scholar
  82. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Saag, L., Tõrra, T., Saag, A., Del-Prado, R., & Randlane, T. (2011). Phylogenetic relations of European shrubby taxa of the genus Usnea. The Lichenologist, 43(05), 427–444.CrossRefGoogle Scholar
  84. Saag, L., Mark, K., Saag, A., & Randlane, T. (2014). Species delimitation in the lichenized fungal genus Vulpicida (Parmeliaceae, Ascomycota) using gene concatenation and coalescent-based species tree approaches. American Journal of Botany, 101(12), 2169–2182.PubMedCrossRefGoogle Scholar
  85. Sanderson, M. J., & Donoghue, M. J. (1996). Reconstructing shifts in diversification rates on phylogenetic trees. Trends in Ecology & Evolution, 11(1), 15–20.CrossRefGoogle Scholar
  86. Scherrer, S., Zippler, U., & Honegger, R. (2005). Characterisation of the mating-type locus in the genus Xanthoria (lichen-forming ascomycetes, Lecanoromycetes). Fungal Genetics and Biology, 42(12), 976–988.PubMedCrossRefGoogle Scholar
  87. Schmitt, I., & Lumbsch, H. T. (2004). Molecular phylogeny of the Pertusariaceae supports secondary chemistry as an important systematic character set in lichen-forming ascomycetes. Molecular Phylogenetics and Evolution, 33(1), 43–55.PubMedCrossRefGoogle Scholar
  88. Schmitt, I., Crespo, A., Divakar, P. K., Fankhauser, J. D., Herman-Sackett, E., Kalb, K., et al. (2009). New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia, 23, 35–40.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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(1), 71–82.CrossRefGoogle Scholar
  90. Singh, G., Dal Grande, F., Divakar, P. K., Otte, J., Leavitt, S. D., Szczepanska, K., et al. (2015). Coalescent-based species delimitation approach uncovers high cryptic diversity in the cosmopolitan lichen-forming fungal genus Protoparmelia (Lecanorales, Ascomycota). PLoS One, 10(5), e0124625. doi:10.1371/journal.pone.0124625.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Sistrom, M., Donnellan, S. C., & Hutchinson, M. N. (2013). Delimiting species in recent radiations with low levels of morphological divergence: a case study in Australian Gehyra geckos. Molecular Phylogenetics and Evolution, 68(1), 135–143.PubMedCrossRefGoogle Scholar
  92. Spinks, P. Q., Thomson, R. C., Pauly, G. B., Newman, C. E., Mount, G., & Shaffer, H. B. (2013). Misleading phylogenetic inferences based on single-exemplar sampling in the turtle genus Pseudemys. Molecular Phylogenetics and Evolution, 68, 269–281.PubMedCrossRefGoogle Scholar
  93. Spitzer, M., Wildenhain, J., Rappsilber, J., & Tyers, M. (2014). BoxPlotR: a web tool for generation of box plots. Nature Methods, 11(2), 121–122.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Spribille, T., Klug, B., & Mayrhofer, H. (2011). A phylogenetic analysis of the boreal lichen Mycoblastus sanguinarius (Mycoblastaceae, lichenized Ascomycota) reveals cryptic clades correlated with fatty acid profiles. Molecular Phylogenetics and Evolution, 59(3), 603–614.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688–2690.PubMedCrossRefGoogle Scholar
  96. Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology, 57(5), 758–771.PubMedCrossRefGoogle Scholar
  97. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.PubMedPubMedCentralCrossRefGoogle Scholar
  98. Tehler, A., & Irestedt, M. (2007). Parallel evolution of lichen growth forms in the family Roccellaceae (Arthoniales, Ascomycota). Cladistics, 23(5), 432–454.CrossRefGoogle Scholar
  99. Thell, A., Crespo, A., Divakar, P. K., Kärnefelt, I., Leavitt, S. D., Lumbsch, H. T., et al. (2012). A review of lichen family Parmeliaceae – history, phylogeny and current taxonomy. Nordic Journal of Botany, 30, 641–664.CrossRefGoogle Scholar
  100. Tõrra, T., & Randlane, T. (2007). The lichen genus Usnea (lichenized Ascomycetes, Parmeliaceae) in Estonia with a key to the species in the Baltic countries. The Lichenologist, 39, 415–438.CrossRefGoogle Scholar
  101. Trest, M. T., Will-Wolf, S., Keuler, R., Shay, N., Hill, K., Studer, A., et al. (2015). Potential impacts of UV exposure on lichen communities: a pilot study of Nothofagus dombeyi trunks in southernmost Chile. Ecosystem Health and Sustainability, 1(4), art14. doi:10.1890/EHS15-0008R1.1.CrossRefGoogle Scholar
  102. Truong, C., Divakar, P. K., Yahr, R., Crespo, A., & Clerc, P. (2013). Testing the use of ITS rDNA and protein-coding genes in the generic and species delimitation of the lichen genus Usnea (Parmeliaceae, Ascomycota). Molecular Phylogenetics and Evolution, 68(2), 357–372.PubMedCrossRefGoogle Scholar
  103. Velmala, S., Myllys, L., Halonen, P., Goward, T., & Ahti, T. (2009). Molecular data show that Bryoria fremontii and B. tortuosa (Parmeliaceae) are conspecific. The Lichenologist, 41(03), 231–242.CrossRefGoogle Scholar
  104. Velmala, S., Myllys, L., Goward, T., Holien, H., & Halonen, P. (2014). Taxonomy of Bryoria section Implexae (Parmeliaceae, Lecanoromycetes) in North America and Europe, based on chemical, morphological and molecular data. Annales Botanici Fennici, 51, 345–371.CrossRefGoogle Scholar
  105. Wagner, C. E., Keller, I., Wittwer, S., Selz, O. M., Mwaiko, S., Greuter, L., et al. (2013). Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Molecular Ecology, 22(3), 787–798.PubMedCrossRefGoogle Scholar
  106. Wedin, M., Westberg, M., Crewe, A. T., Tehler, A., & Purvis, O. W. (2009). Species delimitation and evolution of metal bioaccumulation in the lichenized Acarospora smaragdula (Ascomycota, Fungi) complex. Cladistics, 25(2), 161–172.CrossRefGoogle Scholar
  107. Weiller, G. F. (1998). Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Molecular Biology and Evolution, 15, 326–335.PubMedCrossRefGoogle Scholar
  108. White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315–322). New York: Academic Press.Google Scholar
  109. Wiens, J. J. (1998). Combining data sets with different phylogenetic histories. Systematic Biology, 47(4), 568–581.PubMedCrossRefGoogle Scholar
  110. Willis, S. C., Farias, I. P., & Ortí, G. (2013). Multi-locus species tree for the Amazonian peacock basses (Cichlidae: Cichla): emergent phylogenetic signal despite limited nuclear variation. Molecular Phylogenetics and Evolution, 69(3), 479–490.PubMedCrossRefGoogle Scholar
  111. Wirtz, N., Printzen, C., Sancho, L. G., & Lumbsch, H. T. (2006). The phylogeny and classification of Neuropogon and Usnea (Parmeliaceae, Ascomycota) revisited. Taxon, 55(2), 367–376.CrossRefGoogle Scholar
  112. 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.PubMedCrossRefGoogle Scholar
  113. Wirtz, N., Printzen, C., & Lumbsch, H. T. (2012). Using haplotype networks, estimation of gene flow and phenotypic characters to understand species delimitation in fungi of a predominantly Antarctic Usnea group (Ascomycota, Parmeliaceae). Organisms Diversity & Evolution, 12(1), 17–37.CrossRefGoogle Scholar
  114. Yang, Z., & Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences, 107(20), 9264–9269.CrossRefGoogle Scholar
  115. Yang, Z., & Rannala, B. (2014). Unguided species delimitation using DNA sequence data from multiple loci. Molecular Biology and Evolution, 31(12), 3125–3135.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Zhang, J., Kapli, P., Pavlidis, P., & Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29(22), 2869–2876.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2016

Authors and Affiliations

  • Kristiina Mark
    • 1
  • Lauri Saag
    • 2
  • Steven D. Leavitt
    • 3
  • Susan Will-Wolf
    • 4
  • Matthew P. Nelsen
    • 5
  • Tiiu Tõrra
    • 6
  • Andres Saag
    • 1
  • Tiina Randlane
    • 1
  • H. Thorsten Lumbsch
    • 3
  1. 1.Institute of Botany and EcologyUniversity of TartuTartuEstonia
  2. 2.Department of Evolutionary BiologyEstonian BiocentreTartuEstonia
  3. 3.Science and EducationThe Field MuseumChicagoUSA
  4. 4.Estonia Department of BotanyUniversity of Wisconsin-MadisonMadisonUSA
  5. 5.Department of Geological SciencesStanford UniversityStanfordUSA
  6. 6.Estonian Marine InstituteUniversity of TartuTallinnEstonia

Personalised recommendations