Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-25T16:17:50.589Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogeny of Cladonia uncialis (Cladoniaceae, Lecanoromycetes) and its allies

Published online by Cambridge University Press:  23 July 2015

Soili Stenroos ,
Raquel Pino-Bodas ,
Diana Weckman  and
Teuvo Ahti
Soili Stenroos*
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P. O. Box 7, FI-00014 University of Helsinki, Finland
Raquel Pino-Bodas
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P. O. Box 7, FI-00014 University of Helsinki, Finland
Diana Weckman
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P. O. Box 7, FI-00014 University of Helsinki, Finland
Teuvo Ahti
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P. O. Box 7, FI-00014 University of Helsinki, Finland
*
Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The species from Cladonia section Unciales are characterized by the absence of squamules and soredia on the corticate podetia and the presence of usnic acid. Different subspecies, varieties and forms have been distinguished in the type species C. uncialis. In this study, a molecular phylogeny of Cladonia uncialis and members of the traditionally recognized section Unciales, along with additional potentially allied species, was constructed. DNA sequences from three gene loci, namely ITS rDNA, IGS rDNA and ß-tubulin, were analyzed using Maximum Parsimony, Maximum Likelihood, and Bayesian methods. Eleven species were analyzed for the first time using DNA sequence data. Cladonia uncialis subsp. uncialis and subsp. biuncialis were recognized as distinct taxa. The recognition of C. pseudostellata as a species was not supported by the analyses, but it represents a hypothamnolic acid chemotype, which is reported here as new to Europe (Scotland). The presence of subsp. biuncialis in North America (Newfoundland) was substantiated. The subsp. uncialis usually lacks squamatic acid, but in the eastern United States a morph referred to as subsp. uncialis does normally contain that acid. However, this morph did not attain taxonomic recognition based on phylogenetic analyses. All the other taxa formerly included in sect. Unciales turned out to belong to other groups of Cladonia, mainly Amaurocraeae, Borya, Divaricatae, and Perviae. The formerly recognized genus Cladina (reindeer lichens) is non-monophyletic, consisting of three groups within Cladonia, making the concept Cladina even nomenclaturally useless. Alternative topology tests rejected the monophyly of C. pseudostellata, section Unciales and Cladina.

Keywords

ß-tubulinCladinaCladonia pseudostellataCladonia uncialis subsp. biuncialisIGS rDNAinfrageneric taxonomyITS rDNAlichens
Type
Articles
Information
The Lichenologist , Volume 47 , Issue 4 , July 2015 , pp. 215 - 231
Copyright
© British Lichen Society, 2015 

Access options

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

References

Aasamaa, H. (1961) Classification of the genus Cladonia Hill. Eesti NSV Teaduste Akadeemia Juures Asuva Loodusuurijate Seltsi Aastaraamat 54: 104–117. (In Russian).Google Scholar
Ahti, T. (1973) Taxonomic notes on some species of Cladonia, subsect. Unciales. Annales Botanici Fennici 10 : 163–184.Google Scholar
Ahti, T. (1978) Nomenclatural and taxonomic remarks on European species of Cladonia. Annales Botanici Fennici 15 : 7–14.Google Scholar
Ahti, T. (1984) The status of Cladina as a genus segregated from Cladonia. Nova Hedwigia 79 : 25–61.Google Scholar
Ahti, T. (1993) Names in current use in the Cladoniaceae (lichen-forming ascomycetes) in the ranks of genus to variety. In Names in Current Use in the Families Trichocomaceae, Cladoniaceae, Pinaceae, and Lemnaceae, Regnum Vegetabile Vol. 128 (W. Greuter, ed.): 58–106. Königstein: Koeltz Scientific Books.Google Scholar
Ahti, T. (2000) Cladoniaceae. Flora Neotropica Monograph 78 : 1–362.Google Scholar
Ahti, T. & DePriest, P. T. (2001) New combinations of Cladina epithets in Cladonia (Ascomycotina: Cladoniaceae). Mycotaxon 78 : 499–502.Google Scholar
Ahti, T. & Stenroos, S. (2013) Cladoniaceae. In Nordic Lichen Flora Vol. 5 (T. Ahti, S. Stenroos & R. Moberg, eds.): 1–117. Uppsala: Museum of Evolution, Uppsala University.Google Scholar
Brodo, I. M. & Ahti, T. (1996) Lichens and lichenicolous fungi of the Queen Charlotte Islands, British Columbia, Canada. 2. The Cladoniaceae. Canadian Journal of Botany 74 : 1147–1180.CrossRefGoogle Scholar
Burgaz, A. R. & Ahti, T. (2009) Cladoniaceae. Flora Ibérica Liquenológica 4 : 1–111.Google Scholar
Carlin, G. (1981) De svenska bägarlavarna (Cladonia undersläktet Cladonia). Svensk Botanisk Tidskrift 75 : 361–396.Google Scholar
Choisy, M. (1928) Sur le phylétisme des Ascomycètes du genre Cladonia (Lichens). Bulletin de la Société Mycologique de France 43 : 267–271.Google Scholar
Coppins, B. J. (1978) H. M. Livens lichen collection at Bolton Museum: notes on some interesting specimens. Naturalist 103 : 105–107.Google Scholar
Dahl, E. (1952) On the use of lichen chemistry in lichen systematics. Revue Bryologique et Lichénologique 21 : 119–134.Google Scholar
Del-Prado, R., Cubas, P., Lumbsch, H. T., Divakar, P. K., Blanco, O., Amo de Paz, G., Molina, M. C. & Crespo, A. (2010) Genetic distances within and among species in monophyletic lineages of Parmeliaceae (Ascomycota) as a tool for taxon delimitation. Molecular Phylogenetics and Evolution 56 : 125–133.CrossRefGoogle ScholarPubMed
DePriest, P. T., Piercey-Normore, M., Sikaroodi, M., Kärkkäinen, K. & Oksanen, I. (1999) Phylogenetic analyses of Cladonia and Cladina (lichen-forming Ascomycota). In Abstracts of XVI International Botanical Congress, 1–7 August, 1999, St. Louis, Missouri, USA, p. 325.Google Scholar
DePriest, P. T., Piercey-Normore, M., Sikaroodi, M., Kärkkäinen, K., Oksanen, I., Yahr, R. & Ahti, T. (2000) Phylogenetic relationships among sections of Cladonia and Cladina. In Abstracts of the 4th International Lichenological Symposium, 3–8 September, 2000, Barcelona, Spain, p. 14.Google Scholar
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2 : 113–118.CrossRefGoogle Scholar
Guo, S. & Kashiwadani, H. (2004) Recent study on the phylogeny of the genus Cladonia (s. lat.) with the emphasis on the integrative biology. National Science Museum Monographs, Tokyo 24 : 207–225.Google Scholar
Hawksworth, D. L. (1973) Ecological factors and species delimitation in the lichens. In Taxonomy and Ecology. Systematics Association Special Volume No. 5 (V. H. Heywood, ed.): 31–69. London & New York: Academic Press.Google Scholar
Hinds, J. W. & Hinds, P. L. (2007) The macrolichens of New England. Memoirs of the New York Botanical Garden 96 : 1–584.Google Scholar
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 : 754–755.CrossRefGoogle ScholarPubMed
Huovinen, K. & Ahti, T. (1986 a) The composition and contents of aromatic lichen substances in Cladonia, section Unciales. Annales Botanici Fennici 23 : 173–188.Google Scholar
Huovinen, K. & Ahti, T. (1986 b) The composition and contents of aromatic lichen substances in the genus Cladina. Annales Botanici Fennici 23 : 93–106.Google Scholar
Hyvönen, J., Ahti, T., Stenroos, S. & Gowan, S. (1995) The genus Cladina and the section Unciales of the genus Cladonia (Cladoniaceae, lichenized Ascomycotina), a preliminary phylogenetic analysis. Journal of the Hattori Botanical Laboratory 78 : 243–253.Google Scholar
Kärenlampi, L. (1964) Preliminary notes on the variability of Cladonia uncialis (L.) Wigg. in Eastern Fennoscandia. Annales Botanici Fennici 1 : 220–223.Google Scholar
Kärenlampi, L. & Pelkonen, M. (1971) Studies on the morphological variation of the lichen Cladonia uncialis. Reports from the Kevo Subarctic Research Station 7 : 47–56.Google Scholar
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. Molecular Phylogenetics and Evolution 25 : 138–156.CrossRefGoogle ScholarPubMed
Kauff, F. & Lutzoni, F. (2003) Compat.py – a program to detect topological conflict between supported clades in phylogenetic trees. Available at http://www.lutzonilab.net/downloads/index.shtml.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16 : 111–120.CrossRefGoogle ScholarPubMed
Kurokawa, S. & Kashiwadani, H. (2006) Checklist of Japanese lichens and allied fungi. National Science Museum Monographs 33 : 1–157.Google Scholar
Leuckert, C., Bärmann, U. & Schug, G. (1971) Chemische Flechtenanalysen II. Herzogia 5 : 465–475.CrossRefGoogle Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 : 1451–1452.CrossRefGoogle ScholarPubMed
Litterski, B. & Ahti, T. (2004) World distribution of selected European Cladonia species. Symbolae Botanicae Upsalienses 34 : 205–236.Google Scholar
Lohtander, K., Myllys, L., Sundin, R., Källersjö, M. & Tehler, A. (1998) The species pair concept in the lichen Dendrographa leucophaea (Arthoniales): analyses based on ITS sequences. Bryologist 101 : 404–411.CrossRefGoogle Scholar
Mattick, F. (1938) Systembildung und Phylogenie der Gattung Cladonia. Botanisches Zentralblatt 58B : 215–234.Google Scholar
Mattick, F. (1940) Übersicht der Flechtengattung Cladonia in neuer systematischer Anordnung. Repertorium Specierum Novarum Regni Vegetabilis 49 : 140–168.CrossRefGoogle Scholar
Mattick, F. (1951) Alte und neue Probleme der Lichenologie. Berichte der Deutschen Botanischen Gesellschaft 64 : 94–107.Google Scholar
Merrill, G. K. (1908) Lichen notes no. 7: Yukon lichens. Bryologist 11 : 105–113.CrossRefGoogle Scholar
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. Molecular Phylogenetics and Evolution 12 : 295–309.CrossRefGoogle Scholar
Myllys, L., Lohtander, K. & Tehler, A. (2001) β-tubulin, ITS and group I intron challenge the species pair concept in Physcia aipolia and P. caesia. Mycologia 93 : 335–343.CrossRefGoogle Scholar
Nylander, J. A. A. (2004) MrModeltest v2. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden. Computer program distributed by the author, available from http://www.abc.se/~nylander/.Google Scholar
Nylander, J. A. A., Wilgenbusch, J. C., Warren, D. L. & Swofford, D. L. (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24 : 581–583.CrossRefGoogle Scholar
Nylander, W. (1866) Lichenes Lapponiae orientalis. Notiser ur Sällskapets pro Fauna et Flora Fennica Förhandlingar 5 : 101–192. (preprint).Google Scholar
Pino-Bodas, R., Martín, M. P., Burgaz, A. R. & Lumbsch, H. T. (2013) Species delimitation in Cladonia (Ascomycota): a challenge to the DNA barcoding philosophy. Molecular Ecology Resource 13 : 1058–1068.CrossRefGoogle Scholar
Robert, C. E. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Research 32 : 1792–1797.Google Scholar
Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18 : 502–504.CrossRefGoogle ScholarPubMed
Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16 : 1114–1116.CrossRefGoogle Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 : 2688–2690.CrossRefGoogle ScholarPubMed
Stenroos, S., Ahti, T. & Hyvönen, J. (1997) Phylogenetic analysis of the genera Cladonia and Cladina (Cladoniaceae, lichenized Ascomycota). Plant Systematics and Evoution 207 : 43–58.CrossRefGoogle Scholar
Stenroos, S., Hyvönen, J., Myllys, L., Thell, A. & Ahti, T. (2002) Phylogeny of the genus Cladonia s. lat. (Cladoniaceae, Ascomycetes) inferred from molecular, morphological, and chemical data. Cladistics 18 : 237–278.CrossRefGoogle ScholarPubMed
Strimmer, K. & Rambaut, A. (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the Royal Society of London, Series B 269 : 137–142.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Vainio, E. A. (1880) Tutkimus Cladoniain Phylogenetillisestä Kehityksestä. Helsinki: Frenckell & Poika.Google Scholar
Vainio, E. A. (1887) Monographia Cladoniarum universalis. 1. Acta Societatis pro Fauna et Flora Fennica 4 : 1–509.Google Scholar
Vainio, E. A. (1897) Monographia Cladoniarum universalis. 3. Acta Societatis pro Fauna et Flora Fennica 14 : 1–268.Google Scholar
Vainio, E. A. (1922) Lichenographia Fennica II. Baeomyceae et Lecideales. Acta Societatis pro Fauna et Flora Fennica 53 : 1–341.Google Scholar
White, F. J. & James, P. W. (1985) A new guide to microchemical techniques for the identification of lichen substances. Bulletin of the British Lichen Society 57 (Suppl): 1–41.Google Scholar
White, T. J., Bruns, T., Lee, S. B. & Taylor, J. W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: a Guide to Methods and Application (M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White, eds): 315–322. San Diego: Academic Press.Google Scholar
Wirth, N., Printzen, C. & Lumbsch, H. T. (2008) The delimitation of Antarctic and bipolar species of neuropogonoid Usnea (Ascomycota, Lecanorales): a cohesion approach of species recognition for the Usnea perpusilla complex. Mycological Research 112 : 472–484.CrossRefGoogle Scholar