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Phylogenetic relationships among reindeer lichens of North America

Published online by Cambridge University Press:  03 May 2016

Sarangi N. P. ATHUKORALA
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada, R3T 2N2.
Raquel PINO-BODAS
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P.O. Box 7, FI-00014 University of Helsinki, Finland
Soili STENROOS
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
Michele D. PIERCEY-NORMORE
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada, R3T 2N2.
Corresponding

Abstract

Cladonia is one of the largest lichen-forming ascomycete genera. It was formerly divided into ten sections, three of which, Crustaceae (Cladina), Tenues, and Impexae, are called the reindeer lichens. While previous studies have elucidated the relationships between species and sections, they often examined only one or a few specimens of each species in the analysis. This study examined the monophyly of selected members of sections Crustaceae, Tenues, and Impexae and their relationships in the genus Cladonia using the internal transcribed spacer region of the nuclear ribosomal DNA (ITS rDNA) and the mitochondrial small subunit gene of the mitochondrial ribosomal DNA (mtSSU). The phylogenetic tree contained four clades, two representing species in section Impexae, one representing species that belong to sections Crustaceae and Tenues, and one clade with C. arbuscula and related species. Five of 22 species, C. pycnoclada, C. stellaris, C. evansii, C. ciliata and C. subtenuis, showed monophyly in the phylogenetic tree; some of these 5 species have been shown previously to be monophyletic. The thallus branching pattern was interpreted as an important heritable character using the mtSSU network. Three duplets of paraphyletic species were further examined using ITS rDNA haplotype networks and AMOVA analysis. The results for the species duplets showed some mixing of haplotypes but the AMOVA analysis provided support for species separation within the duplets. While the evidence supports distinct species, further study is needed to conclusively show separate species in these duplets.

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Articles
Copyright
© British Lichen Society, 2016 

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References

Abbayes, H. des (1958) Résultats des expéditions scientifiques genevoises au Népal en 1952 et 1954 (Partie botanique) 12. Cladonia (Lichen). Candollea 16: 201209.Google Scholar
Ahti, T. (1961) Taxonomic studies on reindeer lichens (Cladonia, subgenus Cladina). Annales Botanici Societatis Zoologicae Botanicae Fennicae ‘Vanamo’ 32(1):1160.Google Scholar
Ahti, T. (1984) The status of Cladina as a genus segregated from Cladonia . Nova Hedwigia 79: 2561.Google Scholar
Ahti, T. (2000) Cladoniaceae . Flora Neotropica Monograph 78: 1362.Google Scholar
Ahti, T. & Hyvönen, S. (1985) Cladina stygia, a common, overlooked species of reindeer lichen. Annales Botanici Fennici 22: 223229.Google Scholar
Ambrose, C. D. & Crease, T. J. (2011) Evolution of the nuclear ribosomal DNA intergenic spacer in four species of the Daphnia pulex complex. BMC Genetics 12: 13.CrossRefGoogle ScholarPubMed
Auclair, A. N. D. & Rencz, A. N. (1982) Concentration, mass, and distribution of nutrients in a subarctic Picea marianaCladonia alpestris ecosystem. Canadian Journal of Forest Research 12: 947968.CrossRefGoogle Scholar
Bacon, C. D., McKenna, C. J., Simmons, M. P. & Wagner, W. L. (2012) Evaluating multiple criteria for species delimitation: an empirical example using Hawaiian palms (Arecaceae: Pritchardia). BMC Evolutionary Biology 12: 117.CrossRefGoogle Scholar
Buckler, E. S., Ippolito, A. & Holtsford, T. P. (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145: 821832.Google ScholarPubMed
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540552.CrossRefGoogle ScholarPubMed
Choisy, M. (1928) Sur le phylétisme des Ascomycètes du genre Cladonia (Lichens). Bulletin de la Société Mycologique de France 43: 267271.Google Scholar
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 16571660.CrossRefGoogle ScholarPubMed
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772772.CrossRefGoogle ScholarPubMed
den Herder, M., Kytöviita, M. M. & Niemelä, P. (2003) Growth of reindeer lichens and effects of reindeer grazing on ground cover vegetation in a Scots pine forest and a subarctic heathland in Finnish Lapland. Ecography 26: 312.CrossRefGoogle Scholar
DePriest, P. T., Piercey-Normore, M., Sikaroodi, M., Kärkkäinen, K. & Oksanen, I. (1999) Phylogenetic analyses of Cladonia and Cladina (lichen-forming Ascomycota). In XVI International Botanical Congress, 1–7 August, 1999, St. Louis, Missouri, 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 IAL4, 3–8 September, 2000, Barcelona, Spain, p. 14.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783791.CrossRefGoogle ScholarPubMed
Fitzpatrick, B. M. (2009) Power and sample size for nested analysis of molecular variance. Molecular Ecology 18: 39613966.CrossRefGoogle ScholarPubMed
Fontaine, K., Ahti, T. & Piercey-Normore, M. D. (2010) Convergent evolution in Cladonia gracilis and allies. Lichenologist 42: 323338.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: 207225.Google Scholar
Grube, M., DePriest, P. T., Gargas, A. & Hafellner, J. (1995) Isolation of DNA from lichen ascomata. Mycological Research 99: 13211324.CrossRefGoogle Scholar
Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G. & Gibson, T. J. (1998) Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23: 403405.CrossRefGoogle ScholarPubMed
Kelly, L. J., Hollingsworth, P. M., Coppins, B. J., Ellis, C. J., Harrold, P., Tosh, J. & Yahr, R. (2011) DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context. New Phytologist 191: 288300.CrossRefGoogle Scholar
Knowles, L. L. & Carstens, B. C. (2007) Delimiting species without monophyletic gene trees. Systematic Biology 56: 887895.CrossRefGoogle ScholarPubMed
Kotelko, R. & Piercey-Normore, M. D. (2010) Cladonia pyxidata and C. pocillum: genetic evidence to regard them as conspecific. Mycologia 102: 534545.CrossRefGoogle 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: 404411.CrossRefGoogle Scholar
Lumbsch, H. T., 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. Molecular Phylogenetics and Evolution 31: 822832.CrossRefGoogle ScholarPubMed
Myllys, L., Stenroos, S., Thell, A. & Ahti, T. (2003) Phylogeny of bipolar Cladonia arbuscula and Cladonia mitis (Lecanorales, Euascomycetes). Molecular Phylogenetics and Evolution 27: 5869.CrossRefGoogle Scholar
Orange, A. (1993) Cladonia azorica in the British Isles. Lichenologist 25: 105114.CrossRefGoogle Scholar
Peakall, R. & Smouse, P. E. (2012) GenAlEx6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28: 25372539.CrossRefGoogle Scholar
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 14901498.CrossRefGoogle ScholarPubMed
Piercey-Normore, M. D., Ahti, T. & Goward, T. (2010) Phylogenetic and haplotype analyses of four segregates within Cladonia arbuscula s.l. Botany 88: 397408.CrossRefGoogle Scholar
Pino-Bodas, R., Burgaz, A. R., Martin, M. P. & Lumbsch, H. T. (2011) Phenotypical plasticity and homoplasy complicate species delimitation in the Cladonia gracilis group (Cladoniaceae, Ascomycota). Organisms, Diversity and Evolution 11: 343355.CrossRefGoogle Scholar
Pino-Bodas, R., Martin, M. P., Burgaz, A. R. & Lumbsch, T. H. (2013) Species delimitation in Cladonia (Ascomycota): a challenge to the DNA barcoding philosophy. Molecular Ecology Resources 13: 10581068.Google ScholarPubMed
Pino-Bodas, R., Pérez-Várgas, I., Stenroos, S., Ahti, T. & Burgaz, A. R. (2016) Sharpening the species boundaries in the Cladonia mediterranea complex (Cladoniaceae, Ascomycota). Persoonia 37: 112.CrossRefGoogle Scholar
Rambaut, A. & Drummond, A. (2007) Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 15721574.CrossRefGoogle ScholarPubMed
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. & Huelsenbeck, J. P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539542.CrossRefGoogle ScholarPubMed
Ruoss, E. (1987 a) Species differentiation in a group of reindeer lichens (Cladonia subg. Cladina). Bibliotheca Lichenologica 25: 197206.Google Scholar
Ruoss, E. (1987 b) Chemotaxonomische und morphologische Untersuchungen an den Rentierflechten Cladonia arbuscula und C. mitis . Botanica Helvetica 97: 239263.Google Scholar
Ruoss, E. & Ahti, T. (1989) Systematics of some reindeer lichens (Cladonia subg. Cladina) in the Southern Hemisphere. Lichenologist 21: 2944.CrossRefGoogle Scholar
Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., Chen, W. & Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America 109: 62416246.CrossRefGoogle ScholarPubMed
Shaver, G. R. & Chapin, F. S. III (1991) Production: biomass relationships and element cycling in contrasting arctic vegetation types. Ecological Monographs 61: 131.CrossRefGoogle Scholar
Smith, R. J., Alphandary, E., Arvidson, R., Bono, G., Chipman, B., Corkery, A., DiMegli, J., Hansen, K., Isch, K., McAlpine, J., et al. (2012) Rare inland reindeer lichens at Mima Mounds in southwest Washington State. North American Fungi 7(3):125.Google Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 26882690.CrossRefGoogle ScholarPubMed
Stenroos, S., Ahti, T. & Hyvönen, J. (1997) Phylogenetic analysis of the genera Cladonia and Cladina (Cladoniaceae, lichenized Ascomycota). Plant Systematics and Evolution 207: 4358.CrossRefGoogle Scholar
Stenroos, S., Hyvonen, 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: 237278.CrossRefGoogle Scholar
Stenroos, S., Pino-Bodas, R., Weckman, D. & Ahti, T. (2015) Phylogeny of Cladonia uncialis (Cladoniaceae, Lecanoromycetes) and its allies. Lichenologist 47: 215223.CrossRefGoogle Scholar
Svihus, B. & Holand, Ø. (2000) Lichen polysaccharides and their relation to reindeer/caribou nutrition. Journal of Range Management 53: 642648.CrossRefGoogle Scholar
Swofford, D. L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Taylor, J. W., Geiser, D. M., Burt, A. & Koufopanou, V. (1999) The evolutionary biology and population genetics underlying fungal strain typing. Clinical Microbiology Reviews 12: 126146.Google ScholarPubMed
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S. & Fisher, M. C. (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31: 2132.CrossRefGoogle ScholarPubMed
Templeton, A. R., Crandall, K. A. & Sing, C. F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619633.Google ScholarPubMed
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 (M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White, eds): 315322. New York: Academic Press.Google Scholar
Yahr, R., Vilgalys, R. & DePriest, P. T. (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology 13: 33673378.CrossRefGoogle ScholarPubMed
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: 847860.CrossRefGoogle ScholarPubMed
Zoller, S., Scheidegger, C. & Sperisen, C. (1999) PCR primers for the amplifcation of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31: 511516.CrossRefGoogle Scholar

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