Fungal Diversity

, Volume 58, Issue 1, pp 171–184

Expanded taxon sampling disentangles evolutionary relationships and reveals a new family in Peltigerales (Lecanoromycetidae, Ascomycota)



Lichens that incorporate cyanobacterial symbionts (cyanolichens) are an ecologically key group of species used as biomonitors at all latitudes. Cyanolichen evolution is however based on intense studies of few keystone species and the bulk of species diversity, especially of small species in cold climates, has yet to be accounted for in phylogenetic studies. We assembled an expanded data set including members of all nine currently accepted Peltigeralean families as well as hitherto undersampled representatives of small, radially symmetrical, placodioid cyanolichen genera from the Northern and Southern Hemispheres. Bayesian and maximum likelihood consensus trees from our multilocus analyses (nuSSU, nuLSU and mtSSU) recovered the genera Koerberia, Vestergrenopsis and Steinera as a new, fully supported, family-level clade within the Peltigerales. This clade is further supported by a posteriori morphological analysis and we describe it here as the new family Koerberiaceae. The recently described and physiognomically similar genus Steineropsis, by contrast, is recovered as sister to Protopannaria in the Pannariaceae (Collematineae). Previous analyses have recovered strong monophyletic groups around Pannariaceae, Lobariaceae and Peltigeraceae. We discuss in detail the phylogenetic relationships of all these taxa, provide a pan-Peltigeralean overview of phenotypic characteristics and illustrate all major ascus apical structures. Our topology provides strong backbone support for the sister relationship of Peltigerineae to Collematineae as well as for most currently recognized families of the Peltigerales. The following new combinations are made: Steinera symptychia (Tuck.) T. Sprib. & Muggia, and Vestergrenopsis sonomensis (Tuck.) T. Sprib. & Muggia.


Ascus types Cyanobacteria Lichen Koerberiaceae Phylogenetics Symbiosis Systematics 

Supplementary material

13225_2012_206_MOESM1_ESM.doc (89 kb)
ESM 1(DOC 89 kb)


  1. Arvidsson L, Galloway DJ (1981) Degelia, a new lichen genus in the Pannariaceae. Lichenologist 13:27–50CrossRefGoogle Scholar
  2. Bubrick P, Galun M (1984) Cyanobiont diversity in the Lichinaceae and Heppiaceae. Lichenologist 16:279–287CrossRefGoogle Scholar
  3. Buckley PTR, Arensburger CS, Chambers GK (2002) Combined data, Bayesian phylogenetics, and the origin of the New Zealand Cicada genera. Syst Biol 51:4–18PubMedCrossRefGoogle Scholar
  4. Crespo A, Kauff F, Divakar PK et al (2010) Phylogenetic generic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence. Taxon 59:1735–1753Google Scholar
  5. Crespo A, Divakar PK, Hawksworth DL (2011) Generic concepts in parmelioid lichens, and the phylogenetic value of characters used in their circumscription. Lichenologist 43:511–535CrossRefGoogle Scholar
  6. Cubero OF, Crespo A, Fatehi J, Bridge PD (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium stored and lichenized fungi. Plant Syst Evol 217:243–249CrossRefGoogle Scholar
  7. Ekman S, Andersen HL, Wedin M (2008) The limitations of ancestral state reconstruction and the evolution of the ascus in the Lecanorales (lichenized Ascomycota). Syst Biol 57:141–156PubMedCrossRefGoogle Scholar
  8. Ekman S, Jørgensen PM (2002) Towards a molecular phylogeny for the lichen family Pannariaceae (Lecanorales, Ascomycota). Can J Bot 80:625–634CrossRefGoogle Scholar
  9. Elix JA, Engkaninan U, Jones AJ, Raston CL, Sargent MV, White AH (1978) Chemistry and crystal structure of leprolomin, a novel diphenyl ether from the lichen Psoroma leprolomum. Austral J Chem 31:2057–2068CrossRefGoogle Scholar
  10. Eriksson O, Hawksworth DL (1986) Notes on Ascomycete systematics. Nos. 1–224. Systema Ascomycetum 5:113–174Google Scholar
  11. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes. Application for the identification of mycorrhizae and rust. Mol Ecol 2:113–118PubMedCrossRefGoogle Scholar
  12. Gargas A, Taylor JW (1992) Polymerase chain reaction (PCR) primers for amplifying, sequencing nuclear 18S rDNA from lichenized fungi. Mycologia 84:589–592CrossRefGoogle Scholar
  13. Gauslaa Y (1995) The Lobarion, an epiphytic community of ancient forests threatened by acid rain. Lichenologist 27:59–76Google Scholar
  14. Gaya E, Högnabba F, Holguin Á, Molnar K, Fernández-Brime S, Stenroos S, Arup U, Søchting U, van den Boom P, Lücking R, Sipman HJM, Lutzoni F (2012) Implementing a cumulative supermatrix approach for a comprehensive phylogenetic study of the Teloschistales (Pezizomycotina, Ascomycota). Mol Phyl Evol 63:374–387CrossRefGoogle Scholar
  15. Goffinet B, Bayer RJ (1997) Characterization of mycobionts of photomorph pairs in the Peltigeraceae (lichenized Ascomycetes) based on internal transcribed spacer sequences of the nuclear ribosomal DNA. Fungal Genetics and Biology 21:228–237PubMedCrossRefGoogle Scholar
  16. Goffinet B, Goward T (1998) Is Nephroma silvae-veteris the cyanomorph of Lobaria oregana? Insights from molecular, chemical and morphological characters. In: Glenn MG, Harris RC, Dirig R, Cole MS (eds) Lichenographia Thomsoniana: North American Lichenology in Honor of John W. Thomson. Mycotaxon Ltd., Ithaca, New York, pp 41–52Google Scholar
  17. Goffinet B, Miadlikowska J, Goward T (2003) Phylogenetic inferences based on nrDNA sequences support five morphospecies within the Peltigera didactyla complex (lichenized Ascomycota). Bryologist 106:349–364CrossRefGoogle Scholar
  18. Goward T, Arsenault A (2000) Cyanolichens and conifers: implications for global conservation. Forest, Snow and Landscape Research 75:303–318Google Scholar
  19. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  20. Hafellner J (1984) Studien in Richtung einer natürlicheren Gliederung der Sammelfamilien Lecanoraceae und Lecideaceae. Beiheft zur Nova Hedwigia 79:241–371Google Scholar
  21. Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41:95–98Google Scholar
  22. Henssen A (1963a) Study of the genus Koerberia. Can J Bot 41:1347–1357CrossRefGoogle Scholar
  23. Henssen A (1963b) A study of the genus Vestergrenopsis. Can J Bot 41:1359–1366CrossRefGoogle Scholar
  24. Henssen A (1963c) The North American species of Massalongia and generic relationships. Can J Bot 41:332–1346Google Scholar
  25. Henssen A (1963d) Eine Revision der Flechtenfamilien Lichinaceae und Ephebaceae. Symb Bot Upsal 18(1):1–123Google Scholar
  26. Henssen A (1963e) The North American species of Placynthium. Can J Bot 41:1687–1724CrossRefGoogle Scholar
  27. Henssen A (1981) Hyphomorpha als Phycobiont in Flechten. Pl Syst Evol 137:139–143CrossRefGoogle Scholar
  28. Henssen A (1997) Santessoniella, a new cyanophilic genus of lichenized ascomycetes. Symb Bot Upsal 32(1):75–93Google Scholar
  29. Henssen A, Jahns HM (1974) Lichenes. Georg Thieme Verlag, Stuttgart, 467 ppGoogle Scholar
  30. Henssen A, James PW (1982) The lichen genus Steinera. Bulletin of the British Museum (Natural History). Botany Series 10:227–256Google Scholar
  31. Huelsenbeck JP, Ronquist F (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  32. Jørgensen PM (1994) Studies in the lichen family Pannariaceae VI: The taxonomy and phytogeography of Pannaria Del. s. lat. J. Hattori Bot. Lab 76:197–206Google Scholar
  33. Jørgensen PM (2000) Survey of the lichen family Pannariaceae on the American continent, north of Mexico. Bryologist 103:670–704CrossRefGoogle Scholar
  34. Jørgensen PM (2001) New species and records of the lichen family Pannariaceae from Australia. Bibliotheca Lichenologica 78:109–139Google Scholar
  35. Jørgensen PM (2004) Further contributions to the Pannariaceae (lichenized Ascomycetes) of the Southern Hemisphere. Bibliotheca Lichenologica 88:229–253Google Scholar
  36. Jørgensen PM (2007) Pannariaceae. Nordic Lichen Flora 3:96–112Google Scholar
  37. Jørgensen PM (2008) Vahliella, a new lichen genus. Lichenologist 40:221–225Google Scholar
  38. Jørgensen PM, James PW (1990) Studies in the lichen family Pannariaceae. IV. The genus Degelia. Bibliotheca Lichenologica 38:253–276Google Scholar
  39. Jørgensen PM, Sipman H (2006) The lichen family Pannariaceae in the montane regions of New Guinea. J Hattori Bot Laboratory 100:695–720Google Scholar
  40. Kauff F, Lutzoni F (2002) Phylogeny of the Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Mol Phyl Evol 25:138–156CrossRefGoogle Scholar
  41. Keuck G (1977) Ontogenetisch-systematische Studie über Erioderma. Bibliotheca Lichenologica 6:1–175Google Scholar
  42. Körber GW (1865) Parerga lichenologica: Ergänzungen zum Systema Lichenum Germaniae. E. Trewendt, Breslau, 501 ppGoogle Scholar
  43. Lange OL, Wagenitz G (2003) What is a ‘phycolichen’? Differences and changes in the meaning of an old lichenological term. Lichenologist 35:341–345CrossRefGoogle Scholar
  44. Letrouit-Galinou MA (1971) Études sur le “Lobaria laetevirens” (Lght.) Zahlb. (discolichen, Stictacee). I. Le thalle, les apothécies, les asques. Le Botaniste 54:189–234Google Scholar
  45. Lohtander K, Oksanen I, Rikkinen J (2002) A phylogenetic study of Nephroma (lichen-forming Ascomycota). Mycol Res 106:777–787CrossRefGoogle Scholar
  46. Lumbsch HT, Huhndorf SM (2010) Myconet volume 14. Part one. Outline of ascomycota–2009. Part two. Notes on ascomycete systematics. Nos. 4751–5113. Fieldiana Life and Earth Sciences 1:1–64CrossRefGoogle Scholar
  47. Lumbsch HT, Schmitt I, Lindemuth R, Miller A, Mangold A, Fernandez F, Huhndorf S (2005) Performance of four ribosomal DNA regions to infer higher-level phylogenetic relationships of inoperculate euascomycetes (Leotiomycota). Mol Phyl Evol 34:512–524CrossRefGoogle Scholar
  48. Lumbsch HT, Schmitt I, Mangold A, Wedin M (2007) Ascus types are phylogenetically misleading in Trapeliaceae and Agyriaceae (Ostropomycetidae, Ascomycota). Mycol Res 111:1133–1141PubMedCrossRefGoogle Scholar
  49. Lumbsch HT, Schmitt I, Palice Z, Wiklund E, Ekman S, Wedin M (2004) Supraordinal phylogenetic relationships of Lecanoromycetes based on a Bayesian analysis of combined nuclear and mitochondrial sequences. Mol Phyl Evol 31:822–832CrossRefGoogle Scholar
  50. Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J, Reeb V, Hodkinson BP, Kukwa M, Lücking R et al (2006) New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98:1088–1103PubMedCrossRefGoogle Scholar
  51. Miadlikowska J, Lutzoni F (2000) Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. Int J Plant Sci 161:925–958CrossRefGoogle Scholar
  52. Miadlikowska J, Lutzoni F (2004) Phylogenetic classification of Peltigeralean fungi (Peltigerales, Ascomycota) based on ribosomal RNA small and large subunits. Am J Bot 91:449–464PubMedCrossRefGoogle Scholar
  53. Miadlikowska J, Lutzoni F, Goward T, Zoller S, Posada D (2003) New approach to an old problem: incorporating signal from gap-rich regions of ITS and rDNA large subunit into phylogenetic analyses to resolve the Peltigera canina species complex. Mycologia 95:1181–1203PubMedCrossRefGoogle Scholar
  54. Muggia L, Gueidan C, Grube M (2010) Phylogenetic placement of some morphologically unusual members of Verrucariales. Mycologia 102:835–846PubMedCrossRefGoogle Scholar
  55. Muggia L, Nelson P, Wheeler T, Yakovchenko LS, Tønsberg T, Spribille T (2011) Convergent evolution of a symbiotic duet: the case of the lichen genus Polychidium (Peltigerales, Ascomycota). Am J Bot 98:1647–1656PubMedCrossRefGoogle Scholar
  56. Otálora MAG, Aragón G, Molina MC, Martínez I, Lutzoni F (2010) Disentangling the Collema-Leptogium complex through a molecular phylogenetic study of the Collemataceae (Peltigerales, lichen-forming Ascomycota). Mycologia 102:279–290PubMedCrossRefGoogle Scholar
  57. Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  58. Passo A, Calvelo S (2006) New reports and combinations in the family Pannariaceae (Lecanorales, lichenized Ascomycota). Lichenologist 38:549–555CrossRefGoogle Scholar
  59. Passo A, Stenroos S, Calvelo S (2008) Joergensenia, a new genus to accommodate Psoroma cephalodinum (lichenized Ascomycota). Mycol Res 112:1465–1474PubMedCrossRefGoogle Scholar
  60. Rambaut A, Drummond A (2007) Tracer. Available from: Scholar
  61. Reeb V, Lutzoni F, Roux C (2004) Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phyl Evol 32:1036–1060CrossRefGoogle Scholar
  62. Reinke J (1895) Abhandlungen über Flechten IV. Skizzen zu einer vergleichenden Morphologie des Flechtenthallus (Schluss). Parmeliaceen, Verrucariaceen. Jahrbuch für wissenschaftliche Botanik 28:359–486Google Scholar
  63. Reinke J (1896) Abhandlungen über Flechten V. Das natürliche Flechtensystem. Jahrbuch für wissenschaftliche Botanik 29:171–236Google Scholar
  64. Richardson DHS, Cameron RP (2004) Cyanolichens: their response to pollution and possible management strategies for their conservation in northeastern North America. Northeast Nat 11:1–22CrossRefGoogle Scholar
  65. Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501PubMedCrossRefGoogle Scholar
  66. Ronquist F, Huelsenbeck JP, van der Mark P. (2005) MyBayes 3.1 Manual. Available from:
  67. Schmitt I, del Prado R, Grube M, Lumbsch HT (2009) Repeated evolution of closed fruiting bodies is linked to ascoma development in the largest group of lichenized fungi (Lecanoromycetes, Ascomycota). Mol Phyl Evol 52:34–44CrossRefGoogle Scholar
  68. Schmitt I, Fankhauser JD, Sweeney K, Spribille T, Kalb K, Lumbsch HT (2010) Gyalectoid Pertusaria species from a sister-clade to Coccotrema (Ostropomycetidae, Ascomycota) and comprise the new lichen genus Gyalectaria. Mycology 1:75–83Google Scholar
  69. Schwendener S (1869) Die Algentypen der Flechtengonidien. Universitaetsbuchdruckerei, Basel, 42 ppGoogle Scholar
  70. Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (2009) The Lichens of Great Britain and Ireland. British Lichen Society, London, 1046 ppGoogle Scholar
  71. Spribille T, Jørgensen PM, Schultz M, Houde I (2007) Santessoniella saximontana, a new lichen species from British Columbia. Bibliotheca Lichenologica 96:287–297Google Scholar
  72. Spribille T, Pérez-Ortega S, Tønsberg T, Schirokauer D (2010) Lichens and lichenicolous fungi of the Klondike Gold Rush National Historic Park, Alaska, in a global biodiversity context. Bryologist 113:439–515CrossRefGoogle Scholar
  73. Stamatakis A, Ludwig T, Meier H (2005) RAxML-iii: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463PubMedCrossRefGoogle Scholar
  74. Tuckerman E (1877) Observationes lichenologicae, no. 4. Observations on North American and other lichens. Proc Amer Acad Arts Sci 12(4):166–185Google Scholar
  75. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacter 172:4238–4246Google Scholar
  76. Vitikainen O (2007) Peltigeraceae. Nordic Lichen Flora 3:113–131Google Scholar
  77. Watson W (1929) The classification of lichens. Part I. New Phytol 28:1–36CrossRefGoogle Scholar
  78. Wedin M, Jørgensen PM, Ekman S (2011) Vahliellaceae, a new family of cyanobacterial lichens (Peltigerales, Ascomycetes). Lichenologist 43:67–72CrossRefGoogle Scholar
  79. Wedin M, Jørgensen PM, Wiklund E (2007) Massalongiaceae fam. nov., an overlooked monophyletic group among the cyanobacterial lichens (Peltigerales, Lecanoromycetes, Ascomycota). Lichenologist 39:61–67CrossRefGoogle Scholar
  80. Wedin M, Wiklund E, Jørgensen PM, Ekman S (2009) Slippery when wet: phylogeny and character evolution in the gelatinous cyanobacterial lichens (Peltigerales, Ascomycetes). Mol Phyl Evol 53:862–871CrossRefGoogle Scholar
  81. Wiklund E, Wedin M (2003) The phylogenetic relationships of the cyanobacterial lichens in the Lecanorales suborder Peltigerineae. Cladistics 19:419–431CrossRefGoogle Scholar
  82. Wolseley PA (1991) Observations on the composition and distribution of the ‘Lobarion’ in forests of South East Asia. In: Galloway DJ (ed) Tropical Lichens: Their Systematics, Conservation, and Ecology. Systematics Association Special Volume. Clarendon, Oxford, pp 217–243Google Scholar
  83. Zoller S, Scheidegger C, Sperisen C (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31:511–516Google Scholar

Copyright information

© Mushroom Research Foundation 2012

Authors and Affiliations

  1. 1.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  2. 2.Institute of Plant SciencesKarl-Franzens University of GrazGrazAustria

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