Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T04:01:01.921Z Has data issue: false hasContentIssue false
  • English
  • Français

Taxonomy of Cladonia angustiloba and related species

Published online by Cambridge University Press:  08 May 2018

Raquel PINO-BODAS ,
Ana Rosa BURGAZ ,
Teuvo AHTI  and
Soili STENROOS
Raquel PINO-BODAS
Affiliation:
Real Jardín Botánico de Madrid, CSIC, Plaza de Murillo 2, E-28014 Madrid, Spain. Email: [email protected]
Ana Rosa BURGAZ
Affiliation:
Departamento de Biología Vegetal 1, Universidad Complutense de Madrid, E-28040 Madrid, Spain
Teuvo AHTI
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P.O. Box 7, FI-00014University of Helsinki, Finland
Soili STENROOS
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P.O. Box 7, FI-00014University of Helsinki, Finland
Get access Rights & Permissions [Opens in a new window]

Abstract

The lichen species Cladonia angustiloba is characterized by a well-developed primary thallus and narrow squamules which show deep incisions, and the presence of usnic and fumarprotocetraric acids. Morphologically it is similar to C. foliacea and C. convoluta, from which it can be distiguished by the squamule size and morphology. Since similar characters were used to distinguish C. foliacea from C. convoluta which do not represent different lineages, it is necessary to examine the taxonomic status of C. angustiloba by means of DNA sequences. In this study, the species delimitation within the C. foliacea complex was studied by sequencing three loci, ITS rDNA, cox1 and RPB2. The data were analyzed by means of phylogenetic and species delimitation methods (GMYC, PTP, ABGD and BPP). Our results show that none of the three species is monophyletic. Most of the species delimitation methods did not support the current species as evolutionary lineages. Only some of the BPP analyses supported C. angustiloba as a species distinct from C. foliacea and C. convoluta. However, the hypothesis that considers the C. foliacea complex as constituted by a unique species obtained the best Bayes Factor value. Therefore, C. angustiloba and C. convoluta are synonymized with C. foliacea. A new, thoroughly checked synonymy with typifications of the whole C. foliacea complex is presented. An updated survey of the world distribution data is compiled.

Keywords

CladonialichensMacaronesiamolecular systematicsspecies delimitation
Type
Articles
Information
The Lichenologist , Volume 50 , Issue 3 , May 2018 , pp. 267 - 282
Copyright
© British Lichen Society, 2018 

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

Ahti, T. (2000) Cladoniaceae . Flora Neotropica Monograph 78: 1–363.Google Scholar
Ahti, T. & Aptroot, A. (2009) Two new lichen species of Cladonia from the Azores. Bibliotheca Lichenologica 99: 11–17.Google Scholar
Ahti, T. & Stenroos, S. (2012) New data on nomenclature, taxonomy and distribution of some species of the lichen genus Cladonia. Botanica Complutensis 36: 31–34.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
Bendaikha, Y. & Hadjadj-Aoul, S. (2016) Diversity of lichens flora in Oran area (north-western Algeria). Advances in Environmental Biology 10: 180–191.Google Scholar
Brown, R. P., Tejangkura, T., El Mouden, E. H., Ait Baamrane, M. A. & Znari, M. (2012) Species delimitation and digit number in a North African skink. Ecology and Evolution 2: 2962–2973.CrossRefGoogle Scholar
Burgaz, A. R. (2015) Asientos de flora liquenológica Ibérica. Cladoniaceae. Clementeana 16: 3–158.Google Scholar
Burgaz, A. R. & Ahti, T. (2009) Flora Liquenólogica Ibérica Vol. 4. Cladoniaceae. Madrid: Sociedad Española de Liquenología.Google Scholar
Burgaz, A. R., Escudero, A. & Ahti, T. (1993) Morphometric variation in primary squamules of Cladonia foliacea and C. convoluta . Nova Hedwigia 57: 231–238.Google Scholar
Carstens, B. C., Pelletier, T. A., Reid, N. M. & Satler, J. D. (2013) How to fail at species delimitation. Molecular Ecology 22: 4369–4383.CrossRefGoogle ScholarPubMed
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552.CrossRefGoogle ScholarPubMed
Catalano, I., Mingo, A., Migliozzi, A. & Aprile, G. G. (2016) The lichens of Roccamonfina Volcano (southern Italy). Nova Hedwigia 103: 95–116.CrossRefGoogle Scholar
Christensen, S. N. (2016) Lichenized and lichenicolous fungi from Greece collected by M. Skytte Christiansen, Svend Rungby and other Danish botanists. Herzogia 29: 176–184.CrossRefGoogle Scholar
Cody, M. L. (2006) Plants on Islands: Diversity and Dynamics on a Continental Archipelago. Berkeley and Los Angeles: University of California Press.CrossRefGoogle Scholar
Çobanoğlu, G. & Sevgi, O. (2012) A new lichen record for Turkey and contributions to lichens of İğneada (Kırklareli). Biological Diversity and Conservation 5: 85–88.Google Scholar
Crespo, A. & Lumbsch, H. T. (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1: 167–170.CrossRefGoogle ScholarPubMed
Crespo, A. & Pérez-Ortega, S. (2009) Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenies and morphological characters. Anales del Jardín Botánico de Madrid 66: 71–81.CrossRefGoogle Scholar
Dembo, M., Matzke, N. J., Mooers, A. Ø. & Collard, M. (2015) Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships. Proceedings of the Royal Society B: Biological Sciences 282: 20150943.CrossRefGoogle ScholarPubMed
Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.CrossRefGoogle ScholarPubMed
Dufour, L. (1821) Révision des genres Cladonia, Scyphophorus, Helopodium et Baeomyces de la flore française. Annales Générales des Sciences Physiques 8: 42–72.Google Scholar
Fontaine, K. M., Ahti, T. & Piercey-Normore, M. D. (2010) Convergent evolution in Cladonia gracilis and allies. Lichenologist 42: 323–338.CrossRefGoogle Scholar
Garrido-Benavent, I., Pérez-Ortega, S. & de los Ríos, A. (2017) From Alaska to Antarctica: species boundaries and genetic diversity of Prasiola (Trebouxiophyceae), a foliose chlorophyte associated with the bipolar lichen-forming fungus Mastodia tessellata . Molecular Phylogenetics and Evolution 107: 117–131.CrossRefGoogle ScholarPubMed
Geyer, M. (1985) Hochdruck-Flüssigkeits-Chromatographie (HPLC) von Flechten-Sekundärstoffen. Ph.D. thesis, University of Duisburg-Essen.Google Scholar
Giarla, T. C., Voss, R. S. & Jansa, S. A. (2014) Hidden diversity in the Andes: comparison of species delimitation methods in montane marsupials. Molecular Phylogenetics and Evolution 70: 137–151.CrossRefGoogle ScholarPubMed
Hall, T. (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98 NT. Nucleic Acids Symposium Series 41: 95–98.Google Scholar
Hamilton, C. A., Hendrixson, B. E., Brewer, M. S. & Bond, J. E. (2014) An evaluation of sampling effects on multiple DNA barcoding methods leads to an integrative approach for delimiting species: a case study of the North American tarantula genus Aphonopelma (Araneae, Mygalomorphae, Theraphosidae). Molecular Phylogenetics and Evolution 71: 79–93.CrossRefGoogle Scholar
Huelsenbeck, J. P. & Rannala, B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53: 904–913.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
Katoh, K. & Standley, D. M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.CrossRefGoogle ScholarPubMed
Kotelko, R. & Piercey-Normore, M. D. (2010) Cladonia pyxidata and C. pocillum; genetic evidence to regard them as conspecific. Mycologia 102: 534–545.CrossRefGoogle Scholar
Leaché, A. D. & Fujita, M. K. (2010) Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society B: Biological Sciences 277: 3071–3077.CrossRefGoogle ScholarPubMed
Leaché, A. D., Fujita, M. K., Minini, V. N. & Bouckaert, R. R. (2014) Species delimitation using genome-wide SNP data. Systematic Biology 63: 534–542.CrossRefGoogle ScholarPubMed
Leavitt, S. D., Divakar, P. K., Crespo, A. & Lumbsch, H. T. (2016) A matter of time – understanding the limits of the power of molecular data for delimiting species boundaries. Herzogia 29: 479–492.CrossRefGoogle Scholar
Lecocq, T., Vereecken, N. J., Michez, D., Dellicour, S., Lhomme, P., Valterová, I., Rasplus, J.-Y. & Rasmont, P. (2013) Patterns of genetic and reproductive traits differentiation in mainland vs. Corsican populations of bumblebees. PloS ONE 8: e65642.CrossRefGoogle ScholarPubMed
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
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
Mattick, F. (1940) Übersicht der Flechtengattung Cladonia in neuer systematischer Anordnung. Feddes Repertorium 49: 140–168.CrossRefGoogle Scholar
Mattsson, J.-E. & Lai, M. J. (1993) Vulpicida, a new genus in Parmeliaceae (lichenized Ascomycetes). Mycotaxon 46: 425–428.Google Scholar
Molina, M., Del-Prado, R., Divakar, P., Sánchez-Mata, D. & Crespo, A. (2011) Another example of cryptic diversity in lichen-forming fungi: the new species Parmelia mayi (Ascomycota: Parmeliaceae). Organisms Diversity and Evolution 11: 331–342.CrossRefGoogle Scholar
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Ortiz, D. & Francke, O. F. (2016) Two DNA barcodes and morphology for multi-method species delimitation in Bonnetina tarantulas (Araneae: Theraphosidae). Molecular Phylogenetics and Evolution 101: 176–193.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Pino-Bodas, R., Martin, M. P. & Burgaz, A. R. (2010) Insight into the Cladonia convoluta-C. foliacea (Cladoniaceae, Ascomycota) complex and related species, revealed through morphological, biochemical and phylogenetic analyses. Systematics and Biodiversity 8: 575–586.CrossRefGoogle 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 Resources 13: 1058–1068.CrossRefGoogle Scholar
Pino-Bodas, R., Burgaz, A. R., Martín, M. P., Ahti, T., Stenroos, S., Wedin, M. & Lumbsch, H. T. (2015 a) The phenotypic features used for distinguishing species within the Cladonia furcata complex are highly homoplasious. Lichenologist 47: 287–303.CrossRefGoogle Scholar
Pino-Bodas, R., Burgaz, A. R., Laguna, M., Stenroos, S., Ahti, T. & Martín, M. P. (2015 b) Revisión morfológica y filogenética de Cladonia rangiformis (Cladoniaceae, Ascomycota). In Abstracts of the 20th Cryptogamic Botany Symposium, 22–25th July 2015, Oporto, Portugal, p. 82.Google Scholar
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: 1–12.CrossRefGoogle ScholarPubMed
Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D. & Vogler, A. P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595–609.CrossRefGoogle ScholarPubMed
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.CrossRefGoogle ScholarPubMed
Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.CrossRefGoogle ScholarPubMed
Rambaut, A. & Drummond, A. J. (2009) Tracer version 1.5. Available at: http://tree.bio.ed.ac.uk/software/tracer/.Google Scholar
Rambaut, A. & Drummond, A. J. (2013) TreeAnnotator v1. 7.0. Available as part of the BEAST package at: http://beast.bio.ed.ac.uk.Google Scholar
Rannala, B. & Yang, Z. (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164: 1645–1656.CrossRefGoogle ScholarPubMed
Rannala, B. & Yang, Z. (2013) Improved reversible jump algorithms for Bayesian species delimitation. Genetics 194: 245–253.CrossRefGoogle ScholarPubMed
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: 539–542.CrossRefGoogle ScholarPubMed
Saag, L., Mark, K., Saag, A. & Randlane, T. (2014) Species delimitation in the lichenized fungal genus Vulpicida (Parmeliaceae, Ascomycota) using gene concatenation and coalescent-based species tree approaches. American Journal of Botany 101: 2169–2182.CrossRefGoogle ScholarPubMed
Satler, J. D., Carstens, B. C. & Hedin, M. (2013) Multilocus species delimitation in a complex of morphologically conserved trapdoor spiders (Mygalomorphae, Antrodiaetidae, Aliatypus). Systematic Biology 62: 805–823.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: 1–39.Google Scholar
Schade, A. (1965) Beiträge zur Kenntnis der Flechtengattung Cladonia Hill ex G. H. Web. mit dem Fundortverzeichnis der sächsischen Arten. B. Chasmariae (Ach.) Flk. (Forts.). Die Flechten Sachsens IX. Abhandlungen und Berichte des Naturkundemuseums Görlitz 40: 1–30.Google Scholar
Schade, A. (1966) Über die Artberechtigung der Cladonia subrangiformis Sandst. Nova Hedwigia 9: 285–308.Google Scholar
Schade, A. (1967 a) Über kalkanzeigende Flechten von Spitzbergen. Berichte der Deutschen Botanischen Gesellschaft 79: 463–473.Google Scholar
Schade, A. (1967 b) Über das Vorkommen von Calciumoxalat-Exkreten in Bodenflechten der Kiefern-Heidewälder um Schwarze Pumpe (NL) und seine Ursache. Abhandlungen und Berichte des Naturkundemuseums Görlitz 42: 1–19.Google 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: 6241–6246.CrossRefGoogle ScholarPubMed
Scholz, P. (2007) Lichen distribution maps. A world index and bibliography. Haussknechtia Beiheft 14: 1–379.Google Scholar
Singh, G., Dal Grande, F., Divakar, P. K., Otte, J., Leavitt, S. D., Szczepanska, K. & Lumbsch, H. T. (2015) Coalescent-based species delimitation approach uncovers high cryptic diversity in the cosmopolitan lichen-forming fungal genus Protoparmelia (Lecanorales, Ascomycota). PloS ONE 10: e0124625.CrossRefGoogle ScholarPubMed
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.CrossRefGoogle ScholarPubMed
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: 665–684.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
Sukumaran, J. & Knowles, L. L. (2017) Multispecies coalescent delimits structure, not species. Proceedings of the National Academy of Sciences of the United States of America 114: 1607–1612.CrossRefGoogle Scholar
Vainio, E. A. (1894) Monographia Cladoniarum universalis. II. Acta Societatis pro Fauna et Flora Fennica 10: 1–498.Google Scholar
Wei, X., McCune, B., Lumbsch, H. T., Li, H., Leavitt, S., Yamamoto, Y. & Wei, J. (2016) Limitations of species delimitation based on phylogenetic analyses: a case study in the Hypogymnia hypotrypa group (Parmeliaceae, Ascomycota). PloS ONE 11: e0163664.CrossRefGoogle ScholarPubMed
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): 1–41.Google Scholar
Yang, Z. (2015) The BPP program for species tree estimation and species delimitation. Current Zoology 61: 854–865.CrossRefGoogle Scholar
Yang, Z. & Rannala, B. (2014) Unguided species delimitation using DNA sequence from multiple loci. Molecular Biology and Evolution 31: 3125–3135.CrossRefGoogle ScholarPubMed
Zhang, C., Zhang, D.-X., Zhu, T. & Yang, Z. (2011) Evaluation of a Bayesian coalescent method of species delimitation. Systematic Biology 60: 747–761.CrossRefGoogle ScholarPubMed
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.CrossRefGoogle ScholarPubMed