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The phenotypic features used for distinguishing species within the Cladonia furcata complex are highly homoplasious

Published online by Cambridge University Press:  09 September 2015

Raquel Pino-Bodas
Affiliation:
Botany Unit, Finnish Museum of Natural History, P.O. Box 7, FI-00014 University of Helsinki, Finland. Email: [email protected]
Ana R. Burgaz
Affiliation:
Departamento Biología Vegetal 1, Facultad de Biología, Universidad Complutense de Madrid, E-28040 Madrid, Spain
María P. Martín
Affiliation:
Departamento de Micología, Real Jardín Botánico, RJB-CSIC, E-28014 Madrid, Spain
Teuvo Ahti
Affiliation:
Botany Unit, Finnish Museum of Natural History, P.O. Box 7, FI-00014 University of Helsinki, Finland. Email: [email protected]
Soili Stenroos
Affiliation:
Botany Unit, Finnish Museum of Natural History, P.O. Box 7, FI-00014 University of Helsinki, Finland. Email: [email protected]
Mats Wedin
Affiliation:
Department of Botany, Swedish Museum of Natural History, SE-10405 Stockholm, Sweden
H. Thorsten Lumbsch
Affiliation:
Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA

Abstract

The Cladonia furcata complex treated here comprises C. farinacea, C. furcata, C. multiformis, C. scabriuscula, C. stereoclada, and C. subrangiformis. The well-known taxonomic complexity of this group is caused by wide phenotypic variation and high morphological similarity among the species, for which reason we investigated the distribution in the phylogeny of the phenotypic characters traditionally used to distinguish the species in this complex. A phylogenetic analysis of the C. furcata complex is presented here, based on three loci (ITS rDNA, IGS rDNA and RPB2), representing specimens from a broad geographical range (Europe, North America and New Zealand). The phylogenetic reconstructions were performed using Maximum Likelihood and Bayesian analyses. In addition, 14 features traditionally used for species delimitation within this complex were mapped onto the Bayesian phylogeny. All the species currently accepted, with the exception of C. stereoclada, turned out to be polyphyletic. Most of the phenotypic characters studied are highly homoplasious with the exception of the podetium type. The solid podetia represent a diagnostic character of C. stereoclada.

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Articles
Copyright
© British Lichen Society, 2015 

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References

Abbayes, H. des (1937) Contributions nouvelles à la connaissance des Lichens armoricains II. Cladonia subrangiformis Sandst. emend. H. des Abb. Bulletin de la Societe Scientifique de Bretagne 13: 122144.Google Scholar
Abbayes, H. des (1946) Les Cladonia (Lichens) des Îles Açores. Portugaliae Acta Biologica 1: 243254.Google Scholar
Ahti, T. (1962) Notes on the lichen Cladonia pseudorangiformis Asah. Archivum Societatis Zoologicae Botanicae Fennicae “Vanamo” 17: 3841.Google Scholar
Ahti, T. (1977) Cladonia gorgonina group and C. gigantea in East Africa. Lichenologist 9: 115.Google Scholar
Ahti, T. (1980) Taxonomic revision of Cladonia gracilis and its allies. Annales Botanici Fennici 17: 195243.Google Scholar
Ahti, T. (2000) Cladoniaceae . Flora Neotropica Monograph 78: 1363.Google Scholar
Ahti, T. & Stenroos, S. (2013) Cladoniaceae . In Nordic Lichen Flora Vol. 5 (T. Ahti, S. Stenroos & R. Moberg, eds): 1117. Uppsala: Museum of Evolution, Uppsala University.Google Scholar
Ahti, T., Pino-Bodas, R. & Stenroos, S. (2015) Cladonia corymbescens consists of two species. Mycotaxon 130: 91103.Google Scholar
Argüello, A., Del Prado, R., Cubas, P. & Crespo, A. (2007) Parmelina quercina (Parmeliaceae, Lecanorales) includes four phylogenetically supported morphospecies. Biological Journal of the Linnean Society 91: 455467.Google Scholar
Asahina, Y. (1942) Chemismus der Cladonien unter besonderer Berücksichtigung der japanischen Arten (Fortsetzung). Journal of Japanese Botany 18: 663683.Google Scholar
Ascaso, C., Galván, J. & Rodríguez-Pascual, C. (1982) The weathering of calcareous rocks by lichens. Pedobiologia 24: 219229.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: 11471180.Google Scholar
Burgaz, A. R. & Ahti, T. (1992) Contribution to the study of the genera Cladina and Cladonia in Spain. I. Nova Hedwigia 55: 3753.Google Scholar
Burgaz, A. R. & Ahti, T. (2009) Cladoniaceae. Flora Liquenológica Ibérica, Vol. 4. Madrid: Sociedad Española de Liquenología.Google Scholar
Buschbom, J. & Mueller, G. M. (2006) Testing “species pair” hypotheses: evolutionary processes in the lichen-forming species complex Porpidia flavocoerulescens and Porpidia melinodes . Molecular Biology and Evolution 23: 574586.Google Scholar
Clauzade, G. & Roux, C. (‘1985’) Likenoj de Ockidenta Europo. Bulletin de la Société Botanique du Centre-Ouest, Nouvelle série, Numéro spécial 7: 1891.Google Scholar
Crespo, A. & Lumbsch, H. T. (2010) Cryptic species in lichen forming fungi. IMA Fungus 1: 167170.Google Scholar
Davis, P. H. & Heywood, V. H. (1963) Principles of Angiosperm Taxonomy. Edinburgh: Oliver & Boyd.Google Scholar
Divakar, P. K., Lumbsch, H. T., Ferencova, Z., Del Prado, R. & Crespo, A. (2010) Remototrachyna, a newly recognized tropical lineage of lichens in the Hypotrachyna clade (Parmeliaceae, Ascomycota), originated in the Indian subcontinent. American Journal of Botany 97: 579590.Google Scholar
Edwards, H. G. M., Farwell, D. W., Seaward, M. R. D. & Giacobini, C. (1991) Preliminary Raman microscopic analyses of a lichen encrustation involved in the biodeterioration of Renaissance frescoes in central Italy. International Biodeterioration 27: 19.Google Scholar
Egan, R. S. (1972) Catalog of the lichens of New Mexico. Bryologist 75: 735.Google Scholar
Etayo, J. & Burgaz, A. R. (1997) Contribution to the lichen-forming fungi from the Canary Islands III. The genus Cladonia. Annalen des Naturhistorischen Museums in Wien, Serie B für Botanik und Zoologie 99: 721725.Google Scholar
Evans, A. (1950) Notes on the Cladoniae of Connecticut IV. Rhodora 52: 77123.Google Scholar
Evans, A. (1954) Cladonia subrangiformis in North America. Rhodora 56: 266272.Google Scholar
Ferencova, Z., Del Prado, R., Pérez-Vargas, I., Hernández-Padrón, C. & Crespo, A. (2010) A discussion about reproductive modes of Pseudevernia furfuracea based on phylogenetic data. Lichenologist 42: 449460.Google Scholar
Fink, B. (1904) Further notes on Cladonias. III. Cladonia furcata and Cladonia crispata . Bryologist 7: 5358.Google Scholar
Fontaine, K. M., Ahti, T. & Piercey-Normore, M. D. (2010) Convergent evolution in Cladonia gracilis and allies. Lichenologist 42: 323338.CrossRefGoogle 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: 113118.Google Scholar
Günzl, B. (2004) Erdflechten und ihre Gesellschaften in Nordhessen mit besonderer Berücksichtigung der morphologischen und genetischen Variabilität bei Cladonia furcata (Hudson) Schrader. Dissertation, Georg-August-Universität zu Göttingen.Google Scholar
Hale, M. E. & Culberson, W. L. (1960) A second checklist of the lichens of the continental United States and Canada. Bryologist 63: 137172.Google Scholar
Hammer, S. (1995) A synopsis of the genus Cladonia in the northwestern United States. Bryologist 98: 128.Google Scholar
Hariot, P. (1887) Les Cladoniées magellaniques. Journal de Botanique (Morot) 1: 282286.Google Scholar
Hawksworth, D. L. (1969) The lichen flora of Derbyshire. Lichenologist 4: 105193.Google Scholar
Hennipman, E. (1967) Notes on some Dutch Cladoniae (Lichenes). Persoonia 4: 427428.Google Scholar
Hennipman, E. & Sipman, H. J. M. (1978) De Nederlandse Cladonia’s (Lichenes). Wetenschappelijke Mededelingen de Koninklijke Nederlandse Natuurhistorische Vereniging 124: 180.Google Scholar
Hillmann, J. & Grummann, V. (1957) Flechten. Kryptogamenflora der Mark Brandenburg und angrenzender Gebiete VIII. Berlin: Borntraeger.Google Scholar
Huovinen, K., Ahti, T. & Stenroos, S. (1990) The composition and contents of aromatic lichen substances in Cladonia section Cladonia and group Furcatae . Bibliotheca Lichenologica 38: 209241.Google Scholar
Huneck, S., Feige, G. B. & Schmidt, J. (2004) Chemie von Cladonia furcata und Cladonia rangiformis . Herzogia 17: 5158.Google Scholar
Jahns, H. M. & Beltman, H. A. (1973) Variations in the ontogeny of fruiting bodies in the genus Cladonia and their taxonomic and phylogenetic significance. Lichenologist 5: 349367.Google Scholar
Jahns, H. M., Herold, K. & Beltman, H. A. (1978) Chronological sequence, synchronization and induction of development of fruit bodies in Cladonia furcata var. furcata (Huds.) Schrad. Nova Hedwigia 30: 469526.Google Scholar
James, P. W. (2009) Cladonia . In The Lichens of Great Britain and Ireland (C. W. Smith, A. Aptroot, B. J. Coppins, A. Fletcher, O. L. Gilbert, P. W. James & P. A. Wolseley, eds): 309338. London: British Lichen Society.Google Scholar
Kotelko, R. & Piercey-Normore, M. D. (2010) Cladonia pyxidata and C. pocillum; genetic evidence to regard them as conspecific. Mycologia 102: 534545.Google Scholar
Krog, H. (1968) The macrolichens of Alaska. Norsk Polarinstitut Skrifter 144: 1180.Google Scholar
Leavitt, S. D., Johnson, L. & St. Clair, L. L. (2011 a) Species delimitation and evolution in morph-ologically and chemically diverse communities of the lichen-forming genus Xanthoparmelia (Parmeliaceae, Ascomycota) in western North America. American Journal of Botany 98: 175188.Google Scholar
Leavitt, S. D., Fankhauser, J. D., Leavitt, D. H., Porter, L. D., Johnson, L. A. & St. Clair, L. L. (2011 b) Complex patterns of speciation in cosmopolitan “rock posy” lichens – discovering and delimiting cryptic fungal species in the lichen-forming Rhizoplaca melanophthalma species-complex (Lecanoraceae, Ascomycota). Molecular Phylogenetics and Evolution 59: 587602.Google Scholar
Liu, Y. J., Whelen, S. & Hall, B. D. (1999) Phylogenetic relationships among Ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution 16: 17991808.Google Scholar
Lohtander, K., Myllys, L., Sundin, R., Källersjo, M. & Tehler, A. (1998) The species pair concept in the lichen Dendrographa leucophaea (Arthoniales): analyses based on ITS sequences. Bryologist 101: 404411.Google Scholar
Lumbsch, H. T. & Leavitt, S. D. (2011) Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity 50: 5972.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: 14461480.Google Scholar
Maddison, W. P. & Maddison, D. R. (2011) Mesquite 2.75: a modular system for evolutionary analysis. http://mesquiteproject.org Google Scholar
Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M. & Hornik, K. (2014) Cluster: cluster analysis basics and extensions. R package, Version 1.15.2.Google Scholar
Merrill, G. K. (1909) Lichen notes, no. 8: Cladonia multiformis (nom. nov.). Bryologist 12: 15.Google Scholar
Nelsen, M. P. & Gargas, A. (2009) Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 112: 404417.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 2.3. 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: 581583.Google Scholar
Ott, S., Brinkmann, M., Wirtz, N. & Lumbsch, H. T. (2004) Mitochondrial and nuclear ribosomal DNA data do not support the separation of the Antarctic lichens Umbilicaria kappenii and Umbilicaria antarctica as distinct species. Lichenologist 36: 227234.Google Scholar
Osyczka, P. & Rola, K. (2013) Phenotypic plasticity of primary thallus in selected Cladonia species (lichenized Ascomycota: Cladoniaceae). Biologia 68: 365372.Google Scholar
Osyczka, P. & Skubała, K. (2011) Chemical races of Cladonia cariosa and C. symphycarpa (lichenized Ascomycota) – a Polish case study in a worldwide context. Nova Hedwigia 93: 363373.Google Scholar
Osyczka, P., Rola, K., Lenart-Boroń, A. & Boroń, P. (2014) High intraspecific genetic and morphological variation in the pioneer lichen Cladonia rei colonising slag dumps. Central European Journal of Biology 9: 579591.Google Scholar
Ozenda, P. & Clauzade, G. (1970) Les Lichens: Étude Biologique et Flore Illustrée. Paris: Masson & Cie.Google Scholar
Parnmen, S., Rangsiruji, A., Mongkolsuk, P., Boonpragob, K., Nutakki, A. & Lumbsch, H. T. (2012) Using phylogenetic and coalescent methods to understand the species diversity in the Cladia aggregata complex (Ascomycota, Lecanorales). PloS One 7: e52245.Google Scholar
Paus, S. M. (1997) Die Erdflechtenvegetation Nordwestdeutchlands und einiger Randgebiete. Bibliotheca Lichenologica 66: 1222.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: 311326.Google Scholar
Pino-Bodas, R., Burgaz, A. R., Martín, 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.Google Scholar
Pino-Bodas, R., Burgaz, A. R. & Martín, M. P. (2012 a) Cladonia subturgida and C. iberica (Cladoniaceae) form a single, morphologically and chemically polymorphic species. Mycological Progress 11: 269278.Google Scholar
Pino-Bodas, R., Ahti, T., Stenroos, S., Martín, M. P. & Burgaz, A. R. (2012 b) Cladonia conista and C. humilis (Cladoniaceae) are different species. Bibliotheca Lichenologica 108: 161176.Google Scholar
Pino-Bodas, R., Ahti, T., Stenroos, S., Martín, M. P. & Burgaz, A. R. (2013) Multilocus approach to species recognition in the Cladonia humilis complex (Cladoniaceae, Ascomycota). American Journal of Botany 100: 664678.Google Scholar
Pišút, I. & Wagner, B. (1973) Doplnek k rozsireni lisejniku Cladonia furcata (Huds.) Schrad. subsp. subrangiformis (Sandst.) des Abb. a Collema crispum (Huds.) Web. var. crispum v Cechach. Zprávy České Botanické Společnosti 8: 2729.Google Scholar
R Core Team. (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org/.Google Scholar
Rambaut, A. (2002) Se-Al v2.0a11: sequence alignment editor. Available from http://evolve.zoo.ox.ac.uk/. Google Scholar
Rambaut, A. & Drummond, A. J. (2009) Tracer version 1.5. Website: http://tree.bio.ed.ac.uk/software/tracer/.Google Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539542.Google Scholar
Ruoss, E. & Huovinen, K. (1989) Die intraspezifische Variabilität der phenolischen Inhaltsstoffe bei der Rentierflechte Cladonia arbuscula . Nova Hedwigia 48: 253279.Google Scholar
Sandstede, H. (1922) Die Cladonien der nordwestdeutschen Tieflandes und der deutschen Nordseeinseln. III. Abhandlungen des Naturwissenschaftlichen Vereins zu Bremen 25: 89273.Google Scholar
Sandstede, H. (1931) Die Gattung Cladonia . In Kryptogamen-Flora von Deutschland, Österreich und der Schweiz, Neunter Band, Die Flechten (C. L. Rabenhorst, ed.): 1531. Leipzig: Borntraeger.Google Scholar
Schade, A. (1957) Über Hapteren bei der Flechte Cladonia rangiformis Hoffm. Berichte der Deutschen Botanischen Gesellschaft 70: 283290.Google Scholar
Schade, A. (1964) Cladonia furcata (Huds.) Schrad. und die Ursachen ihrer schwierigen Taxonomie. Die Flechten Sachsens VIII. Abhandlungen und Berichte des Naturkundemuseums Görlitz 39: 139.Google Scholar
Schade, A. (1966) Über die Artberechtigung der Cladonia subrangiformis Sandst. sowie das Auftreten von Calciumoxalat-Exkreten bei ihr und einigen anderen Flechten. Nova Hedwigia 11: 285308.Google Scholar
Scotland, R. W., Olmstead, R. G. & Bennett, J. R. (2003) Phylogeny reconstruction: the role of morphology. Systematic Biology 52: 539548.Google Scholar
Sembdner, G. (1958) Standortseinflüsse auf die anatomische und morphologische Ausgestaltung bei einigen Cladonia-Arten. Flora 145: 589611.Google Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 26882690.Google Scholar
Steinová, J., Stenroos, S., Grube, M. & Škaloud, P. (2013) Genetic diversity and species delimitation of the zeorin-containing red-fruited Cladonia species (lichenized Ascomycota) assessed with ITS rDNA and β-tubulin data. Lichenologist 45: 665684.Google Scholar
Stenroos, S. (1988) The family Cladoniaceae in Melanesia 3. Cladonia sections Helopodium, Perviae and Cladonia . Annales Botanici Fennici 25: 117148.Google Scholar
Stenroos, S., Ferraro, L. I. & Ahti, T. (1992) Líquenes Lecanorales: Cladoniaceae . Flora Criptogámica de Tierra del Fuego 13: 1111.Google 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: 237278.Google Scholar
Tehler, A., Dahlkild, Å., Eldenäs, P. & Feige, G. B. (2004) The phylogeny and taxonomy of Macaronesian, European and Mediterranean Roccella (Roccellaceae, Arthoniales). Symbolae Botanicae Upsalienses 34: 405428.Google Scholar
Tehler, A., Irestedt, M., Bungartz, F. & Wedin, M. (2009) Evolution and reproduction modes in the Roccella galapagoensis aggregate (Roccellaceae, Arthoniales). Taxon 58: 438456.Google Scholar
Thomson, J. W. (1968, ‘1967’) The Lichen Genus Cladonia in North America. Toronto: University of Toronto Press.Google Scholar
Ullrich, J. (1956) Beobachtungen an Cladonien. 1. Partiell isolaterale Primärthalli der Cladonien. 2. Zur Artberechtigung von Cladonia subrangiformis Scriba. Berichte der Deutschen Botanischen Gesellschaft 69: 239244.Google Scholar
Vagts, I., Kinder, M. & Müller, J. (1994) The effect of agrochemicals on the growth of Cladonia furcata . Lichenologist 26: 7382.Google Scholar
Vainio, E. A. (1887) Monographia Cladoniarum universalis. 1. Acta Societatis pro Fauna et Flora Fennica 4: 1509.Google Scholar
Velmala, S., Myllys, L., Halonen, P., Goward, T. & Ahti, T. (2009) Molecular data show that Bryoria fremontii and B. tortuosa (Parmeliaceae) are conspecific. Lichenologist 41: 231242.Google Scholar
Verseghy, K. (1975) Talajlakó xerofiton zuzmófajok ökológiája es elterjedése Magyarországon (II.) s néhány taxon revisioja. Studia Botanica Hungarica 10: 4161.Google Scholar
Wadsten, T. & Moberg, R. (1985) Calcium oxalate hydrates on the surface of lichens. Lichenologist 17: 239245.Google Scholar
Wei, J. C. & Ahti, T. (2002) Cetradonia, a new genus in the new family Cetradoniaceae (Lecanorales, Ascomycota). Lichenologist 34: 1931.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 57(supplement): 141.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 Applications (M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White, eds): 315322. San Diego: Academic Press.Google Scholar
Winston, J. E. (1999) Describing Species: Practical Taxonomic Procedure for Biologists. New York: Columbia University Press.Google Scholar
Wirth, V. (1995) Flechtenflora. 2nd edn. Stuttgart: Verlag Eugen Ulmer.Google Scholar
Wirtz, 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: 472484.Google Scholar
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