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Species delimitations in the Cladonia cariosa group (Cladoniaceae, Ascomycota)

Published online by Cambridge University Press:  12 December 2011

Raquel PINO-BODAS ,
Ana Rosa BURGAZ ,
María P. MARTÍN  and
H. Thorsten LUMBSCH
Raquel PINO-BODAS
Affiliation:
Departamento Biología Vegetal 1, Facultad de Biología, Universidad Complutense de Madrid, E-28040 Madrid, Spain. Email: rpino@bio.ucm.es
Ana Rosa BURGAZ
Affiliation:
Departamento Biología Vegetal 1, Facultad de Biología, Universidad Complutense de Madrid, E-28040 Madrid, Spain. Email: rpino@bio.ucm.es
María P. MARTÍN
Affiliation:
Departamento de Micología, Real Jardín Botánico, CSIC, E-28014 Madrid, Spain.
H. Thorsten LUMBSCH
Affiliation:
Department of Botany, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA.
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Abstract

Phenotypic characters, either morphological or chemical, have shown to be insufficient to delimit species boundaries in the genus Cladonia. The present study addresses the circumscription of species within the Cladonia cariosa group, examining a number of specimens of the currently accepted taxa Cladonia cariosa, C. symphycarpa, C. acuminata, C. subcariosa and C. latiloba. We employed maximum likelihood and Bayesian methods of phylogenetic reconstructions based on DNA sequences of ITS, rpb2 and ef1α regions. Our results show that the C. cariosa group consists of at least four phylogenetic lineages. It is also shown that each of these lineages is chemically variable, which restricts the taxonomic value of the chemical differences within the group. However, anatomical differences, such as squamule surface and cortex structure, were found to correlate with the distinct lineages found in the phylogenetic analysis. This result confirms the taxonomic value of the cortical surface under SEM, as was found in other lichen groups.

Keywords

chemistryLecanoraleslichenstaxonomy
Type
Research Article
Information
The Lichenologist , Volume 44 , Issue 1 , January 2012 , pp. 121 - 135
Copyright
Copyright © British Lichen Society 2011

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References

Ahti, T. (1976) The lichen genus Cladonia in Mongolia. Journal of Japanese Botany 51: 365–373.Google Scholar
Ahti, T. (2000) Cladoniaceae. Flora Neotropica Monograph 78: 1–362.Google Scholar
Ahti, T. & Hammer, S. (2002) Cladonia. In Lichen Flora of the Greater Sonoran Desert Region. Vol. 1 (Nash, T. H. III, Ryan, B. D., Gries, C., & Bungartz, F., eds): 131–158. Tempe: Lichens Unlimited, Arizona State University.Google Scholar
Ahti, T. & Sohrabi, M. (2006) Synopsis of Iranian Cladonia (lichens). Flora Mediterranea 16: 139–144.Google Scholar
Azuaga, T., Barbero, M. & Gomez-Bolea, A. (2001) Additions to the knowledge of the Cladonia (Cladoniaceae, lichenized Ascomycotina) in the alpine belt of the Pyrenees in Andorra. Mycotaxon 79: 433–446.Google Scholar
Bültmann, H. M. & Lünterbusch, C. H. (2008) Cladonia cariosa group in Greenland. Abhandlungen aus dem Westfälischen Museum für Naturkunde 70: 305–312.Google Scholar
Burgaz, A. R. & Ahti, T. (2009) Cladoniaceae. Vol 4. Madrid: Sociedad Española de Liquenologia.Google Scholar
Carlin, G. & Owe-Larson, B. (1994) Cladonia polycarpoides in Sweden, with a note on C. cervicornis ssp. pulvinata. Graphis Scripta 6: 1–6.Google Scholar
Crespo, A. & Lumbsch, H. T. (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1: 167–170.Google Scholar
Culberson, W. L. (1969) The chemistry and systematics of some species of the Cladonia cariosa group in North America. Bryologist 72: 377–386.Google Scholar
Culberson, W. L., Culberson, C. F., Johnson, A. & Park, Y. S. (1993) New chemistries in the Cladonia cariosa complex and homoheveadride in natural thalli and single-spore culture of C. polycarpoides and C. polycarpia. Bibliotheca Lichenologica 53: 43–52.Google Scholar
DePriest, P. T. (1993) Molecular innovations in lichen systematics: the use of ribosomal and intron nucleotide sequences in the Cladonia chlorophaea complex. Bryologist 96: 314–325.Google Scholar
DePriest, P. T. (1994) Variation in the Cladonia chlorophaea complex II: ribosomal DNA variation in a Southern Appalachian population. Bryologist 97: 117–126.Google Scholar
Dolnik, C., Beck, A. & Zarabska, D. (2010) Distinction of Cladonia rei and C. subulata based on molecular, chemical and morphological characteristics. Lichenologist 42: 373–386.CrossRefGoogle Scholar
Evans, A. W. (1944) On Cladonia polycarpia Merrill. Bryologist 47: 49–56.Google Scholar
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for Basidiomycetes – application to the identification of mycorrhiza and rust. Molecular Ecology 2: 113–118.CrossRefGoogle Scholar
Hale, M. E. (1973) Fine structure of the cortex in the lichen family Parmeliaceae viewed with the scanning-electron microscope. Smithsonian Contributions to Botany 10: 1–92.Google Scholar
Harris, R. C. (1975) Lichens of the Mackinac Straits region. I. The Cladonia cariosa group. The Michigan Botanist 14: 44–48.Google Scholar
Harris, R. C. (2009) Four novel lichen taxa in the lichen biota of eastern North America. Opuscula Philolichenum 6: 149–156.Google Scholar
Hawksworth, D. L. (1969) The scanning electron microscope. An aid to the study of cortical hyphal orientation in the lichen genera Alectoria and Cornicularia. Journal de Microscopie 8: 753–760.Google Scholar
Huelsenbeck, J. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.CrossRefGoogle ScholarPubMed
Huovinen, K., Ahti, T. & Stenroos, S. (1989) The composition and contents of aromatic lichen substances in Cladonia section Helopodium and subsection Foliosae. Annales Botanici Fennici 26: 297–306.Google Scholar
James, P. W. (2009) Cladonia. In The Lichens of Great Britain and Ireland (Smith, C. W., Aptroot, A., Coppins, B. J., Flechter, A., Gilbert, O. L., James, P. W. & Wolseley, P. A., eds): 309–338. London: British Lichen Society.Google Scholar
Kärkkäinen, K. (2000) Helopodium-sektion fylogenia ja takasonominen asema torvijäkälien (Cladonia) suvussa (Ascomycetes, jäkälöityneet sienet). Pro gradu Dissertation. Helsinki University, Finland.Google Scholar
Kotelko, R. & Piercey-Normore, M. D. (2010) Cladonia pyxidata and C. pocillum; genetic evidence to regard them as conspecific. Mycologia 102: 534–545.Google Scholar
Korczyńska, J., Gajwska, M., Pilot, M., Czechowski, W. & Radchenko, A. (2010) Genetic polymorphism in “mixed” colonies of wood ants (Hymenoptera: Formicidae) in southern Finland and its possible origin. European Journal of Entomology 107: 157–167.CrossRefGoogle Scholar
Kristinsson, H. (1974) Two new Cladonia and one Cetraria species from Iceland. Lichenologist 6: 141–145.Google Scholar
Leavitt, S. D., Johnson, L. & St. Clair, L. L. (2011) 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: 175–188.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.Google Scholar
Liu, Y. J., Whelen, S. & Benjamin, D. H. (1999) Phylogenetic relationships among Ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution 16: 1799–1808.Google Scholar
Lumbsch, H. T., Parnmen, S., Rangsiruji, A. & Elix, J. A. (2010) Phenotypic disparity and adaptive radiation in the genus Cladia (Lecanorales, Ascomycota). Australian Systematic Botany 23: 239–247.Google Scholar
Lutzoni, F., Kauff, F., Cox, C. J., McLaughlin, D., Celio, G., Dentinger, B., Padamsee, M., Hibbett, D., James, T. Y., Baloch, E. et al. (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. American Journal of Botany 91: 1446–1480.CrossRefGoogle ScholarPubMed
Martín, M. P. & Winka, K. (2000) Alternative methods of extracting and amplifying DNA from lichens. Lichenologist 32: 189–196.Google Scholar
Masselink, A. K. & Sipman, H. J. (1985) Enkele nieuwe vondsten van Cladonia's in Nederland. Gorteria 12: 231–241.Google Scholar
Mendonça, F. F., Oliveira, C., Burgess, G., Coelho, R., Piercy, A., Gadig, O. B. F. & Foresti., F. (2011) Species delimitation in sharpnose sharks (genus Rhizoprionodon) in the western Atlantic Ocean using mitochondrial DNA. Conservation Genetics 12: 193–200.Google Scholar
Merrill, G. K. (1909) Lichen notes no. 10. Cladonia gracilis, C. verticillata f. symphycarpia Tuck, and Cladonia symphycarpa Fr., a present view of their identity. Bryologist 12: 43–46.Google Scholar
Milankov, V., Ståhls, G., Stamenković, J. & Vujić, A. (2008) Genetic diversity of populations of Merodon aureus and M. cinereus species complexes (Diptera, Syrphidae): integrative taxonomy and implications for conservation priorities on the Balkan Peninsula. Conservation Genetics 9: 1125–1137.Google Scholar
Murillo, C., Albertazzi, F. J., Carranza, J., Lumbsch, H. T. & Tamayo, G. (2009) Molecular data indicate that Rhytidhysteron rufulum (Ascomycetes, Patellariales) in Costa Rica consists of four distinct lineages corroborated by morphological and chemical characters. Mycological Research 113: 405–416.Google Scholar
Myllys, L., Velmala, S., Holien, H., Halonen, P., Wang, S. & Goward, T. (2011). Phylogeny of the genus Bryoria. Lichenologist 43: 617–638.Google Scholar
Nimis, P. L. (1993) The Lichens of Italy. An Annotated Catalogue. Torino: Museo Regionale di Scienze Naturali.Google Scholar
Nylander, J. A. A. (2004) MrModelTest 2.1. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.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.Google Scholar
O'Brien, H. E., Miądlikowska, J. & Lutzoni, F. (2009) Assessing reproductive isolation in highly diverse communities on the lichen-forming fungal genus Peltigera. Evolution 63: 2076–2086.CrossRefGoogle ScholarPubMed
Park, Y. S. (1985) Habitat selection in a pair of sibling chemospecies of the lichen genus Cladonia. American Midland Naturalist 114: 180–183.Google Scholar
Parnmen, S., Rangsiruji, A., Mongulsuk, P., Boonpragob, K., Elix, J. A. & Lumbsch, H. T. (2010) Morphological disparity in Cladoniaceae: the foliose genus Heterodea evolved from fruticose Cladia species (Lecanorales, Ascomycota). Taxon 59: 841–849.Google Scholar
Piercey-Normore, M. D. (2003) A field survey of the genus Cladonia (Ascomycotina) in Manitoba, Canada. Mycotaxon 86: 233–247.Google Scholar
Piercey-Normore, M. D., Ahti, T. & Goward, T. (2010) Phylogenetic and haplotype analyses of four segregates within Cladonia arbuscula s. l. Botany 88: 397–408.Google Scholar
Pino-Bodas, R., Burgaz, A. R. & Martín, M. P. (2010) Elucidating the taxonomic rank of Cladonia subulata versus C. rei (Cladoniaceae). Mycotaxon 113: 311–326.CrossRefGoogle Scholar
Porter, A. H. (1990) Testing nominal species boundaries using gene flow statistics: the taxonomy of two hybridizing Admiral butterflies (Limenitis, Nymphalidae). Systematic Zoology 39: 131–147.Google Scholar
Rambaut, A. (1996) Se-Al v2.0a11: Sequence Alignment Editor. Available from: http://evolve.zoo.ox.ac.uk/.Google Scholar
Randlane, T. (1986) New data on rare Cladonia species from Soviet Union. Folia Cryptogamica Estonica 20: 3–4.Google Scholar
Rivas-Plata, E., Hernandez, J. E., Lücking, R., Staiger, B., Kalb, K. & Cáceres, M. E. S. (2011) Graphis is two genera: a remarkable case of parallel evolution in lichenized Ascomycota. Taxon 60: 99–107.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.Google Scholar
Shaffer, H. B. & Thomson, R. C. (2007) Delimiting species in recent radiations. Systematic Biology 56: 896–906.Google Scholar
Spier, L. & Aptroot, A. (2007) Cladonia rei is a chemotype and synonym of Cladonia subulata. Lichenologist 39: 57–60.CrossRefGoogle Scholar
Stenroos, S. & Ahti, T. (1990) The lichen family Cladoniaceae in Tierra del Fuego: problematic or otherwise noteworthy taxa. Annales Botanici Fennici 27: 317–327.Google Scholar
Stenroos, S. & DePriest, P. T. (1998) SSU rDNA phylogeny of cladoniiform lichens. American Journal of Botany 85: 1548–1559.Google Scholar
Stenroos, S., Ferraro, L. I. & Ahti, T. (1992) Lichenes Lecanorales: Cladoniaceae. Flora Criptogámica de Tierra del Fuego 13(7): 1–111.Google Scholar
Stenroos, S., Hyvönen, J., Myllys, L., Thell, A. & Ahti, T. (2002a) Phylogeny of the genus Cladonia s. lat. (Cladoniaceae, Ascomycetes) inferred from molecular, morphology and chemical data. Cladistics 18: 237–278.Google Scholar
Stenroos, S., Myllys, L., Thell, A. & Hyvönen, J. (2002b) Phylogenetic hypotheses: Cladoniaceae, Stereocaulaceae, Baeomycetaceae, and Icmadophilaceae revisited. Mycological Progress 1: 267–282.Google Scholar
Swofford, D. L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Syrek, M. & Kukwa, M. (2008) Taxonomy of the lichen Cladonia rei and its status in Poland. Biologia 63: 493–497.Google Scholar
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S. & Fisher, M. C. (2000) Species recognition and species concepts in fungi. Fungal Genetics and Biology 29: 21–32.CrossRefGoogle Scholar
Thomson, J. W. (1968) The Lichen Genus Cladonia in North America. Toronto: University of Toronto Press.Google Scholar
Thomson, J. W. (1983) American Arctic Lichens 1. The Macrolichens. New York: Columbia University Press.Google Scholar
Vainio, E. A. (1887) Monographia Cladoniarum universalis. 1. Acta Sociatis pro Fauna et Flora Fennica 4: 1–509.Google Scholar
Wedin, M., Döring, H. & Ekman, S. (2000) Molecular phylogeny of the lichen families Cladoniaceae, Sphaerophoraceae, and Stereocaulaceae (Lecanorales, Ascomycotina). Lichenologist 32: 171–187.Google Scholar
Weir, B. S. & Cockerham, C. C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.Google Scholar
White, F. J. & James, P. W. (1985) A new guide to microchemical techniques for the identification of lichen substances. British Lichen Society Bulletin 75 (suppl): 1–41.Google Scholar
White, T. J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: a Guide to Methods and Applications (Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T.J., eds): 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 Usnea perpusilla complex. Mycological Research 112: 472–484.Google Scholar
Yahr, R, Vilgalys, R. & DePriest, P. T. (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171: 847–860.CrossRefGoogle ScholarPubMed
Zhou, Q. M., Wei, J. C., Ahti, T., Stenroos, S. & Högnabba, F. (2006) The systematic position of Gymnoderma and Cetradonia based on SSU rDNA sequences. Journal of the Hattori Botanical Laboratory 100: 871–880.Google Scholar