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Fungal Diversity

, Volume 80, Issue 1, pp 285–300 | Cite as

Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta)

  • Sergio Pérez-Ortega
  • Isaac Garrido-Benavent
  • Martin Grube
  • Rocío Olmo
  • Asunción de los Ríos
Article

Abstract

The fungal genus Collemopsidium comprises species that develop so-called borderline lichen symbioses with algae or cyanobacteria. Together with morphologically similar pyrenocarpous fungi it has been assigned to the family Xanthopyreniaceae. The adscription of this family to higher taxonomic ranks remain uncertain. Using sequence data of five nuclear genomic regions (nuLSU, nuSSU, tef1-α, rpb1 and rpb2) and one mitochondrial locus (mtSSU) we found that the studied representatives of this family are placed in the Dothideomyceta, yet relationships with the classes Dothideomycetes and Arthoniomycetes remain uncertain. We describe the new order Collemopsidiales to accommodate the genus Collemopsidium (paraphyletic as currently understood) and the lichenicolous genus Zwackhiomyces. Using five fungal fossils as calibrations points, we infer an age of c. 230 Mya for the crown of Collemopsidiales. Based on two molecular markers, we also provide insight into the global diversity of marine species of the genus Collemopsidium. According to the species delimitation algorithm GMYC, c. 26 putative species exist, far more than the six species recognized hitherto. We have confirmed this result by comparing the two alternative species models by means of Bayes factors, using path sampling and stepping-stone sampling algorithms to estimate the marginal likelihood of each model. Finally, our observations suggest rock-boring ability evolved in parallel in the different lineages within this group of fungi.

Keywords

Borderline lichens Dothideomycetes Endolithics Lichen-forming fungi Lichenicolous fungi Boring ability Marine fungi Model comparison 

Notes

Acknowledgments

The authors would like to thank Javier Etayo (Navarra), Victor J. Rico (Madrid), Mercedes Vivas (Concepción), María Arróniz-Crespo (Madrid), Cécile Gueidan (Canberra) for collecting fresh specimens, Toby Spribille (Graz), Alan Orange (Cardiff) and Karen Dillman (Petersburg) for assistance during field work, María José Malo (Madrid) for her help with lab work and Ana Burton for improving English. SPO, IGB and AdR were supported by grant CTM2012-38222-C02-02, IGB was supported by grant FPU AP2012-3556, SPO is currently supported by the grant RYC-2014-16784, all from the Spanish Ministry of Economy and Competitiveness. We also thank the staff of the microscopy facility of the ICA (CSIC, Madrid) for technical assistance and the three anonymous reviewers for their suggestions and insightful comments.

Supplementary material

13225_2016_361_MOESM3_ESM.docx (17 kb)
Suppl. Table 1 Specimen information and accession numbers for the Xanthopyreniaceae material used in the phylogenetic designations. (DOCX 16 kb)
13225_2016_361_MOESM4_ESM.doc (240 kb)
Suppl. Table 2 Specimen information and accession numbers for the marine Collemopsidium specimens. (DOC 240 kb)
13225_2016_361_MOESM5_ESM.doc (128 kb)
Suppl. Table 3 Accession numbers for the Ascomycota dataset (AC). (DOC 128 kb)
13225_2016_361_MOESM6_ESM.docx (30 kb)
Suppl. Table 4 Accession numbers for the Dothideomyceta dataset (DO). (DOCX 30 kb)
13225_2016_361_MOESM7_ESM.doc (41 kb)
Suppl. Table 5 Nodes and divergences times (DOC 41 kb)
13225_2016_361_Fig4_ESM.gif (117 kb)
Suppl. Fig. 1

Six-locus phylogeny (50 % majority rule consensus tree) depicting phylogenetic relationships among clades of Dothideomyceta including species of Xanthopyreniaceae (Collemopsidiales). Filled in circles on branches indicate Bayesian posterior probability (PP) ≥ 95 % and ML bootstrap values (B) ≥ 70 %. Left filled circles represent only PP support. Right filled circles represent only ML bootstrap support. Members of the Dothideomyceta are indicated in colour: red for Dothiodeomycetes, green for Arthoniomycetes and blue for Xanthopyreniaceae (Collemopsidiales). (GIF 116 kb)

13225_2016_361_MOESM1_ESM.tif (24.5 mb)
High resolution image (TIF 25136 kb)
13225_2016_361_Fig5_ESM.gif (195 kb)
Suppl. Fig. 2

Maximum clade credibility (MCC) cartoon tree with divergence times estimates for main clades of Ascomycota. Estimates were obtained using a Bayesian approach (BEAST) and five fossil calibration points. Bars correspond to 95 % highest posterior density intervals (HPD). Filled in circles on branches indicate Bayesian posterior probability (PP) ≥ 95 %. Estimated ages (median and HPD) for the nodes (1-12) are available in Suppl. Table 5. Abbreviations for geologic periods read as follow: Cam. = Cambrian, Ord. = Ordovician, Sil. = Silurian, Dev. = Devonian, Carb. = Carboniferous, Perm. = Permian, Trias. = Triassic; Jura. = Jurassic, Cenoz. = Cenozoic. (GIF 194 kb)

13225_2016_361_MOESM2_ESM.tif (507 kb)
High resolution image (TIF 506 kb)

References

  1. Ahmadjian V (1967) A guide to the algae occurring as lichen symbionts. Phycologia 6:127–160CrossRefGoogle Scholar
  2. Aptroot A (1998) Aspects of the integration of the taxonomy of lichenized and non-lichenized pyrenocarpous ascomycetes. Lichenologist 30:501–514CrossRefGoogle Scholar
  3. Bachmann E (1919) Der Thallus der Kalkflechten mit Chroolepus-, Scytonema- und Xanthocapsa-Gonidien. Nova Acta Abh Kais Leop-Carol Deutsch Akad f Naturf 105:1–80Google Scholar
  4. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29:2157–2167PubMedPubMedCentralCrossRefGoogle Scholar
  5. Beimforde C, Feldberg K, Nylinder S, Rikkinen J, Tuovila H, Dörfelt H, Gube M, Jackson DJ, Reitner J, Seyfullah LJ, Schmidt AR (2014) Estimating the Phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Mol Phylogenet Evol 78:386–398PubMedCrossRefGoogle Scholar
  6. Bungartz F, Garvie LAJ, Nash TH (2004) Anatomy of the endolithic Sonoran Desert lichen Verrucaria rubrocincta Breuss: implications for biodeterioration and biomineralization. Lichenologist 36:55–73CrossRefGoogle Scholar
  7. Calatayud V, Triebel D, Pérez-Ortega S (2007) Zwackhiomyces cervinae, a new lichenicolous fungus (Xanthopyreniaceae) on Acarospora, with a key to the known species of the genus. Lichenologist 39:129–134CrossRefGoogle Scholar
  8. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedCrossRefGoogle Scholar
  9. Cockell CS, Herrera A (2008) Why are some microorganisms boring? Trends Microbiol 16:101–106PubMedCrossRefGoogle Scholar
  10. Coppins BJ (1992) Pyrenocollema Reinke (1895). In: Purvis OW, Coppins BJ, Hawksworth DL, James PW, Moore DM (eds) The Lichen Flora of Great Britain and Ireland. Natural History Museum Publications, London, pp 515–518Google Scholar
  11. Coppins BJ, Aptroot A (2008) New species and combinations in The Lichens of the British Isles. Lichenologist 40:363–374Google Scholar
  12. Coppins BJ, James PW, Hawksworth DL (1992) New species and combinations in the lichen flora of Great Britain and Ireland. Lichenologist 24:351–369Google Scholar
  13. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/ Accessed 14th October 2014)
  14. Cubero O, Crespo A, Fatehi J, Bridge P (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Syst Evol 216:243–249CrossRefGoogle Scholar
  15. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772PubMedPubMedCentralCrossRefGoogle Scholar
  16. Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389CrossRefGoogle Scholar
  17. de los Ríos A, Wierzchos J, Ascaso C (2014) The lithic microbial ecosystems of Antarctica’s McMurdo Dry Valleys. Antarct Sci 26:459–477CrossRefGoogle Scholar
  18. Diederich P, Schultz M (2009) Zwackhiomyces namibiensis, a new lichenicolous ascomycete (Xanthopyreniaceae) on Psorotichia from Namibia. Herzogia 22:173–176Google Scholar
  19. Doppelbaur HW (1959) Studien zur Anatomie und Entwicklungsgeschichte einiger endolitischen pyrenocarpen Flechten. Planta 53:246–292CrossRefGoogle Scholar
  20. Drummond A, Ho S, Phillips M, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88PubMedPubMedCentralCrossRefGoogle Scholar
  21. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973PubMedPubMedCentralCrossRefGoogle Scholar
  22. Egidi E, De Hoog GS, Isola D, Onofri S, Quaedvlieg W, De Vries M, Verkley GJM, Stielow JB, Zucconi L, Selbmann L (2014) Phylogeny and taxonomy of meristematic rock-inhabiting black fungi in the Dothideomycetes based on multi-locus phylogenies. Fungal Divers 65:127–165CrossRefGoogle Scholar
  23. Ezard T, Fujisawa T, Baraclough T et al. (2009) SPLITS: SPecies’ LImits by Threshold Statistics. http://R-Forge.R-project.org/projects/splits/
  24. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  25. Fontaneto D, Herniou EA, Boschetti C, Caprioli M, Melone G, Ricci C, Barraclough TG (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biol 5:914–921CrossRefGoogle Scholar
  26. Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:1045–1053PubMedCrossRefGoogle Scholar
  27. Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol 65:707–724CrossRefGoogle Scholar
  28. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application for the identification of mycorrhizae and rusts. Mol Ecol 2:113–118PubMedCrossRefGoogle Scholar
  29. Gareth Jones EB, Suetrong S, Sakayaroi J, Bahkali AH, Abdel-Wahab MA, Boekhout T, Pang KL (2015) Classification of marine Ascomycota, Basiciomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers 73:1–72CrossRefGoogle Scholar
  30. Gargas A, Taylor JW (1992) Polymerase chain reaction (PCR) primers for amplifying and sequencing nuclear 18S rDNA from lichenized fungi. Mycologia 84:589–592CrossRefGoogle Scholar
  31. Gargas A, Depriest PT, Grube M, Tehler A (1995) Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny. Science 268:1492–1495PubMedCrossRefGoogle Scholar
  32. Gazis R, Miadlikowska J, Lutzoni F, Arnold AE, Chaverri P (2012) Culture-based study of endophytes associated with rubber trees in Peru reveals a new class of Pezizomycotina: Xylonomycetes. Mol Phylogenet Evol 65:294–30PubMedCrossRefGoogle Scholar
  33. Geiser DV, Gueidan C, Miadlikowska J, Lutzoni F, Kauff F, Hofstetter V, Fraker E, Schoch CL, Tibell L, Untereiner WA, Aptroot A (2006) Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae. Mycologia 98:1053–1064PubMedCrossRefGoogle Scholar
  34. Golubic S, Friedmann EI, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Res 51:475–478Google Scholar
  35. Grube RBD (2002) Collemopsidium. In: Nash TH, Ryan BD, Gries C, Bungartz F (eds) Lichen flora of the Greater Sonoran Desert Region. Lichens Unlimited, Tempe, pp 1162–1164Google Scholar
  36. Grube M (2005) Frigidopyrenia: a new genus for a peculiar subarctic lichen, with notes on similar taxa. Phyton 45:305–318Google Scholar
  37. Grube M, Hafellner J (1990) Studien an flechtenbewohnenden Pilzen der Sammelgattung Didymella (Ascomycetes, Dothideales). Nova Hedwigia 51:283–360Google Scholar
  38. Gueidan C, Ruibal CV, de Hoog GS, Gorbushina AA, Untereiner WA, Lutzoni F (2008) An extremotolerant rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud Mycol 62:111–119CrossRefGoogle Scholar
  39. Gueidan C, Ruibal C, de Hoog S, Schneider H (2011) Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biol 115:987–996PubMedCrossRefGoogle Scholar
  40. Gueidan C, Aptroot A, da Silva Cáceres ME, Badali H, Stenroos S (2014) A reappraisal of orders and families within the subclass Chaetothyriomycetidae (Eurotiomycetes, Ascomycota). Mycol Prog 13:1027–1039CrossRefGoogle Scholar
  41. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  42. Harris RC (1995) More Florida lichens. including the 10c Tour of the Pyrenolichens. Published by the author, BronxGoogle Scholar
  43. Hasegawa M, Kishino H, Yano TA (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedCrossRefGoogle Scholar
  44. Hawksworth DL (2015) Lichenization: the origins of a fungal life-style. In: Upreti DK, Divakar PK, Shukla V, Bajpai R (eds) Recent advances in lichenology. Springer, India, pp 1–10CrossRefGoogle Scholar
  45. Hawksworth DL, Eriksson OE (1988) Proposals to conserve 11 family names in the Ascomycotina (Fungi). Taxon 37:190–193CrossRefGoogle Scholar
  46. Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580PubMedCrossRefGoogle Scholar
  47. Hibbett DS, Binder M, Bischoff JF et al (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547PubMedCrossRefGoogle Scholar
  48. Hofstetter V, Miadlikowska J, Kauff F, Lutzoni F (2007) Phylogenetic comparison of protein-coding versus ribosomal RNA-coding sequence data: a case study of the Lecanoromycetes (Ascomycota). Mol Phylogenet Evol 44:412–426PubMedCrossRefGoogle Scholar
  49. Honegger R (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts. In: Hock B (ed) The Mycota – a comprehensive treatise on fungi as experimental system for basic and applied research. Fungal association IX, 2nd edn. Springer, Berlin, pp 288–339Google Scholar
  50. Hug LA, Roger AJ (2007) The impact of fossils and taxon sampling on ancient molecular dating analyses. Mol Biol Evol 24:1889–1897PubMedCrossRefGoogle Scholar
  51. Hyde KD, Jones EBG, Liu J-K et al (2013) Families of Dothideomycetes. Fungal Divers 63:1–313CrossRefGoogle Scholar
  52. Jones EBG, Sakayaroj J, Suetrong S, Somrithipol S, Pang KL (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:1–187Google Scholar
  53. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795CrossRefGoogle Scholar
  54. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298PubMedCrossRefGoogle Scholar
  55. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066PubMedPubMedCentralCrossRefGoogle Scholar
  56. 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 Phylogenet Evol 25:138–156PubMedCrossRefGoogle Scholar
  57. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth & Bisby’s dictionary of the fungi, 10th edn. CAB International, WallingfordGoogle Scholar
  58. Kohlmeyer J, Hawksworth D, Volkmann-Kohlmeyer B (2004) Observations on two marine and maritime “borderline” lichens: Mastodia tessellata and Collemopsidium pelvetiae. Mycol Progress 3:51–56CrossRefGoogle Scholar
  59. Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701PubMedCrossRefGoogle Scholar
  60. Lange OL, Schulze E-D, Koch W (1970) Experimentell-ökologische Untersuchungen an Flechten der Negev-Wüste. III. CO2-Gaswechsel und Wasserhaushalt von Krusten- und Blattflechten am natürlichen Standort während der sommerlichen Trockenperiode. Flora 159:525–538Google Scholar
  61. Lartillot N, Philippe H (2006) Computing Bayes factors using thermodynamic integration. Syst Biol 55:195–207PubMedCrossRefGoogle Scholar
  62. Le Campion-Alsumard T, Golubic S (1985) Hyella caespitosa Bornet et Flahault and Hyella balani Lehman (Pleurocapsales, Cyanophyta): a comparative study, Arch. Hydrobiol. Suppl. 71 (1/2). Algol Stud 38(39):119–148Google Scholar
  63. Leavitt SD, Esslinger TL, Lumbsch HT (2012a) Neogene-dominated diversification in neotropical montane lichens: dating divergence events in the lichen-forming fungal genus Oropogon (Parmeliaceae). Am J Bot 99:1764–1777PubMedCrossRefGoogle Scholar
  64. Leavitt SD, Esslinger TL, Divakar PK, Lumbsch HT (2012b) Miocene 111Q09 divergence, phenotypically cryptic lineages, and contrasting distribution patterns in common lichen-forming fungi (Ascomycota: Parmeliaceae). Biol J Linn Soc 107:920–937Google Scholar
  65. Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol 16:1799–1808PubMedCrossRefGoogle Scholar
  66. Lücking R, Dal-Forno M, Sikaroodi M, Gillevet PM, Bungartz F, Moncada B, Yáñez-Ayabaca A, Chaves JL, Coca LF, Lawrey JD (2014) A single macrolichen constitutes hundreds of unrecognized species. Proc Natl Acad Sci U S A 111:11091–11096PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lumbsch HT, Huhndorf SM (2010) Myconet volume 14, part two. notes on ascomycete systematics. nos. 4751–5113. Fieldiana: Life and Earth Sciences, N.S. 1:42–64Google Scholar
  68. Lutzoni F, Pagel M, Reeb V (2001) Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411:937–940PubMedCrossRefGoogle Scholar
  69. Lutzoni F, Kauff F, Cox CJ et al (2004) Assembling the fungal tree of life: progress, classification and evolution of subcellular traits. Am J Bot 91:1446–1480PubMedCrossRefGoogle Scholar
  70. Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am J Bot 89:688–698PubMedCrossRefGoogle Scholar
  71. McElwain JC, Punyasena SW (2007) Mass extinction events and the plant fossil record. Trends Ecol Evol 22:548–557PubMedCrossRefGoogle Scholar
  72. McWilliam H, Li W, Uludag M et al (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41:597–600CrossRefGoogle Scholar
  73. Miadlikowska J, Kauff F, Hofstetter V 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
  74. Miadlikowska J, Kauff F, Högnabba F et al (2014) A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Mol Phylogenet Evol 79:132–168PubMedCrossRefGoogle Scholar
  75. Millanes AM, Truong C, Westberg M, Diederich P, Wedin M (2014) Host switching promotes diversity in host-specialized mycoparasitic fungi: uncoupled evolution in the Biatoropsis-Usnea system. Evolution 68:1576–1593PubMedCrossRefGoogle Scholar
  76. Mohr F, Ekman S, Heegaard E (2004) Evolution and taxonomy of the marine Collemopsidium species (lichenized Ascomycota) in north-west Europe. Mycol Res 108:515–532PubMedCrossRefGoogle Scholar
  77. Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, Inward DJG, Lees DC, Ranaivosolo R, Eggleton P, Barraclough TG, Vogler AP (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Syst Biol 58:298–311PubMedCrossRefGoogle Scholar
  78. Moncalvo J-M, Rehner SA, Vilgalys R (1993) Systematics of Lyophyllum section Difformia based on evidence from culture studies and ribosomal DNA sequences. Mycologia 85:788–794CrossRefGoogle Scholar
  79. Moore D (2013) Fungal biology in the origin and emergence of life. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  80. Moreno PP, Egea JM (1991) Biología y taxonomía de la familia Lichinaceae, con especial referencia a las especies del SE España y norte de Africa. Secretariado de Publicaciones, Universidad de MurciaGoogle Scholar
  81. Myllys L, Lohtander K, Källersjö M, Tehler A (1999) Sequence insertions and ITS data provide congruent information on Roccella canariensis and R. tuberculata (Arthoniales, Euascomycetes) phylogeny. Mol Phylogenet Evol 12:295–309PubMedCrossRefGoogle Scholar
  82. Nimis PL (1993) The lichens of Italy. an annotated catalogue. Museo Regionale di Scienze Naturali, Monografia XII, TurinGoogle Scholar
  83. Nimis P, Zappa L (1988) I licheni endolitici calcicoli su monumenti. In: Nimis PL, Monte M (eds) Lichens and Monuments. Stud Geobot 8:125–133Google Scholar
  84. Nordin A (2002) Collemopsidium angermannicum, a widespread but rarely collected aquatic lichen. Graphis Scripta 13:39–41Google Scholar
  85. Nylander W (1881) Addenda nova ad Lichenographiam europaeam. Contin XXXV Flora 64:2–8Google Scholar
  86. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290PubMedCrossRefGoogle Scholar
  87. Pérez-Ortega S, Ortiz-Álvarez R, Allan Green TG, de los Ríos A (2012) Lichen myco- and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiol Ecol 82:429–448PubMedCrossRefGoogle Scholar
  88. Pinna D, Salvadori O, Tretiach M (1998) An anatomical investigation of calcicolous endolithic lichens from the Trieste karst (NE Italy). Plant Biosyst 132:183–195CrossRefGoogle Scholar
  89. Poelt J (1974) Classification. In: Ahmadjian V, Hale ME (eds) The lichens. Academic, New York, pp 599–630Google Scholar
  90. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55: 595–609Google Scholar
  91. Prieto M, Wedin M (2013) Dating the diversification of the major lineages of Ascomycota (Fungi). PLoS ONE 8:e65576PubMedPubMedCentralCrossRefGoogle Scholar
  92. Prieto M, Baloch E, Tehler A, Wedin M (2013) Mazaedium evolution in the Ascomycota (Fungi) and the classification of mazaediate groups of formerly unclear relationship. Cladistics 29:296–308CrossRefGoogle Scholar
  93. Rambaut A, Suchard MA, Drummond AJ (2014) Tracer v 1.6, available from: http://tree.bio.ed.ac.uk/software/tracer/Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycol Res 98:625–634Google Scholar
  94. Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycol Res 98:625–634Google Scholar
  95. Renobales G (1996) Contribución al conocimiento de los líquenes calcícolas del occidente de Vizcaya y parte oriental de Cantabria (N-España). Guineana 2:1–310Google Scholar
  96. Rikkinen J (2003) Calicioid lichens from European Tertiary amber. Mycologia 95:1032–1036PubMedCrossRefGoogle Scholar
  97. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and Mocel Choide across a large model space. Syst Biol 61:539–542PubMedPubMedCentralCrossRefGoogle Scholar
  98. Rosling A, Cox F, Cruz-Martinez K et al (2011) Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 333:876–879PubMedCrossRefGoogle Scholar
  99. Santesson R (1939) Amphibious pyrenolichens I. Arkiv för Botanik 29a(10):1–68Google Scholar
  100. Santesson R (1992) Pyrenocollema elegans, a new marine lichen. Lichenologist 24:7–11CrossRefGoogle Scholar
  101. Schmidt AR, Beimforde C, Seyfullah LJ et al (2014) Amber fossils of sooty moulds. Rev Palaeobot Palyno 200:53–64CrossRefGoogle Scholar
  102. Schoch CL, Wang Z, Townsend JP, Spatafora JW (2009a) Geoglossomycetes cl. nov., Geoglossales ord. nov. and taxa above class rank in the Ascomycota tree of life. Persoonia 22:129–138PubMedPubMedCentralCrossRefGoogle Scholar
  103. Schoch CL, Sung GH, López-Giráldez F, Townsend JP, Miadlikowska J et al (2009b) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239PubMedCrossRefGoogle Scholar
  104. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium, Fungal Barcoding Consortium Author List (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 109:6241–6246PubMedPubMedCentralCrossRefGoogle Scholar
  105. Smith AL (1921) Lichens. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  106. 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, LondonGoogle Scholar
  107. Spatafora JW, Johnson D, Sung G-H et al (2006) A five-gene phylogenetic analysis of the Pezizomycotina. Mycologia 98:1020–1030CrossRefGoogle Scholar
  108. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771PubMedCrossRefGoogle Scholar
  109. Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. PNAS 94:4520–4525PubMedPubMedCentralCrossRefGoogle Scholar
  110. Swinscow TDV (1965) Pyrenocarpous lichens: 9. Lichenologist 3:72–83CrossRefGoogle Scholar
  111. Tavaré S (1986) Some probabilistic and statisical problems on the analysis of DNA sequences. Lect Math Life Sci 17:57–86Google Scholar
  112. Taylor TN, Hass H, Kerp H, Krings M, Hanlin RT (2005) Perithecial ascomycetes from the 400 million year old Rhynie chert: an example of ancestral polymorphism. Mycologia 97:269–285PubMedCrossRefGoogle Scholar
  113. Tucker SC, Harris RC (1980) New or noteworthy pyrenocarpous lichens from Louisiana and Florida. Bryologist 83:1–20CrossRefGoogle Scholar
  114. van den Boom PPG (2010) New or interesting lichens and lichenicolous fungi of Gran Canaria (Canary Islands, Spain). Willdenowia 40:359–367CrossRefGoogle Scholar
  115. van den Boom P, Etayo J (2014) New records of lichenicolous fungi and lichenicolous lichens from the Iberian Peninsula, with the description of four new species and one new genus. Opusc Philolichenum 13:44–79Google Scholar
  116. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246PubMedPubMedCentralGoogle Scholar
  117. Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968CrossRefGoogle Scholar
  118. Visscher H, Brinkhuis H, Dilcher DL, Elsik WC, Eshet Y, Looy CV, Rampino MR, Traverse A (1996) The terminal Paleozoic fungal event: evidence of terrestrial ecosystem destabilization and collapse. PNAS 93:2155–2158PubMedPubMedCentralCrossRefGoogle Scholar
  119. Watson W (1929) The classification of lichens. New Phytol 28:85–116CrossRefGoogle Scholar
  120. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetic. In: Innis MA, Gelfand DH, White JJSJ (eds) PCR protocols. Academic, San Diego, pp 315–322Google Scholar
  121. Wierzchos J, Ascaso C (1994) Application of back-scattered electron imaging to the study of the lichen-rock interface. J Microsc 175:54–59CrossRefGoogle Scholar
  122. Xie W, Lewis PO, Fan Y, Kuo L, Chen MH (2010) Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol 60:150–160PubMedPubMedCentralCrossRefGoogle Scholar
  123. Zahlbruckner A (1926) Lichenes (Flechten). B. Spezieller Teil. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien, vol 8, 2nd edn. W Engelmann, Leipzig, pp 61–270Google Scholar
  124. Zharkikh A (1994) Estimation of evolutionary distances between nucleotide sequences. J Mol Evol 39:315–329PubMedCrossRefGoogle Scholar
  125. Zoller S, Scheidegger C, Sperisen C (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31:511–516CrossRefGoogle Scholar

Copyright information

© School of Science 2016

Authors and Affiliations

  • Sergio Pérez-Ortega
    • 1
    • 2
  • Isaac Garrido-Benavent
    • 1
  • Martin Grube
    • 3
  • Rocío Olmo
    • 1
    • 4
  • Asunción de los Ríos
    • 1
  1. 1.Museo Nacional de Ciencias Naturales (CSIC)MadridSpain
  2. 2.Real Jardín Botánico de Madrid (CSIC)MadridSpain
  3. 3.Institute of Plant SciencesUniversity of GrazGrazAustria
  4. 4.Facultad de Ciencias Ambientales y BioquímicaUniversidad de Castilla-La ManchaToledoSpain

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