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Conundrums in species concepts: the discovery of a new cryptic species segregated from Parmelina tiliacea(Ascomycota: Parmeliaceae)

Published online by Cambridge University Press:  05 October 2011

Jano NÚÑEZ-ZAPATA
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal, 28040, Madrid, Spain. Email: acrespo@farm.ucm.es
Pradeep K. DIVAKAR
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal, 28040, Madrid, Spain. Email: acrespo@farm.ucm.es
Ruth DEL-PRADO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal, 28040, Madrid, Spain. Email: acrespo@farm.ucm.es
Paloma CUBAS
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal, 28040, Madrid, Spain. Email: acrespo@farm.ucm.es
David L. HAWKSWORTH
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal, 28040, Madrid, Spain. Email: acrespo@farm.ucm.es
Ana CRESPO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal, 28040, Madrid, Spain. Email: acrespo@farm.ucm.es

Abstract

Parmelina tiliacea is a common, widely distributed species in south-western Europe, easily identifiable by morphology and much used as an air pollution bioindicator in many regions. A molecular phylogenetic survey of samples from many geographical areas, using Maximum Parsimony and Bayesian inference of nuITS and mtLSU rDNA regions, revealed a group of samples geographically restricted to a small region of the Iberian Peninsula and genetically separated from the other P. tiliacea specimens studied. These samples are morphologically indistinguishable from P. tiliacea, apart from subtle anatomical characters in the ascomata (hyphae of the exciple and ascospore width), which are frequently absent. Although geographically different, the two taxa occupy similar habitats and are even sympatric in some areas, indicating that they do not exchange genetic material. This previously overlooked, and apparently endemic lineage, is described as P. cryptotiliacea sp. nov., and the name Lichen tiliaceus is epitypified by a sequenced specimen to fix the application of Parmelina tiliacea to the widespread genotype. A second unexpected result was the discovery that the morphologically distinct P. pastillifera was nested within P. tiliacea. These two cases stress the need to use molecular tools to elucidate species concepts even within widespread morphologically well-characterized macrolichens. Such investigations are necessary to improve our understanding and estimation of biodiversity, and to facilitate the development of sound biodiversity conservation strategies for lichens.

Type
Research Article
Copyright
Copyright © British Lichen Society 2011

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References

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.CrossRefGoogle Scholar
Blanco, O., Crespo, A., Divakar, P. K., Esslinger, T., Hawksworth, D. L. & Lumbsch, H. T (2004) Melanelixia and Melanohalea, two new genera segregated from Melanelia (Parmeliaceae) based on molecular and morphological data. Mycological Research 108: 873884.CrossRefGoogle ScholarPubMed
Blanco, O., Crespo, A., Divakar, P. K., Elix, J. A. & Lumbsch, H. T. (2005) Molecular phylogeny of parmotremoid lichens (Ascomycota, Parmeliaceae). Mycologia 97: 150159.CrossRefGoogle ScholarPubMed
Blanco, O., Crespo, A., Ree, R. H. & Lumbsch, H. T. (2006) Major clades of parmelioid lichens (Parmeliaceae, Ascomycota) and the evolution of their morphological and chemicals diversity. Molecular Phylogenetics and Evolution 39: 5269.CrossRefGoogle ScholarPubMed
Buckley, T. R., Arensburger, P., Simon, C. & Chambers, G. K. (2002) Combined data, Bayesian phylogenetics, and the origin of the New Zealand cicada genera. Systematic Biology 51: 418.CrossRefGoogle ScholarPubMed
Clerc, P. & Truong, C. (2008) The non-sorediate and non-isidiate Parmelina species (lichenized ascomycetes, Parmeliaceae) in Switzerland – Parmelina atricha (Nyl.) P. Clerc reinstated in the European lichen flora. Sauteria 15: 175194.Google Scholar
Crespo, A., Blanco, O. & Hawksworth, D. L. (2001) The potential of mitochondrial DNA for establishing phylogeny and stabilising generic concepts in the parmelioid lichens. Taxon 50: 807819.CrossRefGoogle Scholar
Crespo, A., Ferencov, Z., Perez-Ortega, S., Elix, J. A. & Divakar, P. K. (2010) Austroparmelina, a new Australasian lineage in parmelioid lichens (Parmeliaceae, Ascomycota). Systematics and Biodiversity 8: 209221.CrossRefGoogle Scholar
Culberson, C. F. (1972) Improved conditions and new data for the identification of lichen products by a standardized thin-layer chromatographic method. Journal of Chromatography 72: 113125.CrossRefGoogle ScholarPubMed
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: 125133.CrossRefGoogle ScholarPubMed
Diaz-Guerra, D. & Manrique, E. (1984) Sustancias liquénicas en taxónes de la provincia de Madrid, Evernia prunastri (L.) Ach. y Parmelina tiliacea (Hoffm.) Hale. Lazaroa 6: 267268.Google Scholar
Divakar, P. K. & Upreti, D. K. (2005) Parmelioid Lichens in India (A Revisionary Study). Dehra Dun: Bishen Singh and Mahendra Pal Singh.Google Scholar
Divakar, P. K., Molina, M. C., Lumbsch, H. T. & Crespo, A. (2005) Parmelina barrenoae, a new lichen species related to Parmelia sulcata (Parmeliaceae) based on molecular and morphological data. Lichenologist 37: 3746.CrossRefGoogle Scholar
Divakar, P. K., Figueras, G., Hladun, N. L. & Crespo, A (2010a) Molecular phylogenetic studies reveal an undescribed species within the North American concept of Melanelixia glabra (Parmeliaceae). Fungal Diversity 42: 4755.CrossRefGoogle Scholar
Divakar, P. K., Lumbsch, H. T., Ferencova, Z., Del-Prado, R. & Crespo., A. (2010b) Remototrachyna, a new tropical lineage in hypotrachynoid lichens (Parmeliaceae, Ascomycota) originated in India. American Journal of Botany 97: 579590.CrossRefGoogle Scholar
Dobson, F. S. & Hawksworth, D. L. (1976) Parmelia pastillifera (Harm.) Schub. and Klem. and P. tiliacea (Hoffm.) Ach. in the British Isles. Lichenologist 8: 4759.CrossRefGoogle Scholar
Elix, J. A. (1993) Progress in the generic delimitation of Parmelia sensu lato lichens (Ascomycotina: Parmeliaceae) and a synoptic key to the Parmeliaceae. Bryologist 96: 359383.CrossRefGoogle Scholar
Elix, J. A. & Ernst-Russell, K. D. (1993) A Catalogue of Standardized Thin Layer Chromatographic Data and Biosynthetic Relationships for Lichen Substances. 2nd edn. Canberra: Australian National University.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783791.CrossRefGoogle ScholarPubMed
Feuerer, T. & Thell, A. (2002) Parmelia ernstiae – a new macrolichen from Germany. Mitteilungen aus dem Institut der Allgemeine Botanik, Hamburg 30–32: 4960.Google Scholar
Hale, M. E. (1976) A monograph of the lichen genus Parmelina Hale (Parmeliaceae). Smithsonian Contributions to Botany 33: 160.Google Scholar
Hall, T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 9598.Google Scholar
Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160174.CrossRefGoogle ScholarPubMed
Hillis, D. M. & Bull, J. J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42: 182192.CrossRefGoogle Scholar
Huelsenbeck, J. P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754755.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P., Rannala, B. & Masly, J. P. (2000) Accommodating phylogenetic uncertainty in evolutionary studies. Science 288: 23492350.CrossRefGoogle ScholarPubMed
Jørgensen, P. M. (1972) Noen interessante lavfunn, saerlig fra Vestlandet. Blyttia 30: 153162.Google Scholar
Kirk, P. M., Cannon, P. F., Minter, D. W. & Stalpers, J. A. (2008) Ainsworth & Bisby's Dictionary of the Fungi. 10th edn. Wallingford: CAB International.CrossRefGoogle Scholar
Larget, B. & Simon, D. (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution 16: 750759.CrossRefGoogle Scholar
Liška, J., Palice, Z., Dětinský, R. & Vondrák, J. (2006) Changes in distribution of rare and threatened lichens in the Czech Republic II. In Central European Lichens: Diversity and Threat (Lackovičová, A., Guttová, A., Lisická, E. & Lizoň, P., eds): 241258. Ithaca, New York: Mycotaxon Ltd.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: 404411.CrossRefGoogle Scholar
Molina, M. C., Crespo, A., Blanco, O., Lumbsch, H. T. & Hawksworth, D. L. (2004) Phylogenetic relationships and species concepts in Parmelia s. str. (Parmeliaceae) inferred from nuclear ITS rDNA and beta-tubulin sequences. Lichenologist 36: 3754.CrossRefGoogle Scholar
Molina, M. C., Divakar, P. K., Millanes, A. M., Sanchez, E., Hawksworth, D. L. & Crespo, A. (2011) Parmelia sulcata (Ascomycota: Parmeliaceae) a sympatric monophyletic species complex. Lichenologist 43: 585601.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: 295309.CrossRefGoogle Scholar
Nimis, P. L. (1993) The Lichens of Italy. An Annotated Catalogue. [Monografia no. XII.] Torino: Museo Regionale di Scienze Naturali.Google Scholar
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Page, R. D. M. (1996) TreeView: an application to display phylogenetic trees on personal computers. Computer Applied Biosciences 12: 357358.Google ScholarPubMed
Poelt, J. & Vězda, A. (1977) Bestimmunggsschussel Europaischer Flechten. Erganzungsheft I. [Bibliotheca Lichenologica no. 9.] Vaduz: J. Cramer.Google Scholar
Printzen, C. (2002) Fungal specific primers for PCR-amplification of mitochondrial LSU in lichens. Molecular Ecology Notes 2: 130132.CrossRefGoogle Scholar
Rannala, B. & Yang, Z. (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. Journal of Molecular Evolution 43: 304311.CrossRefGoogle Scholar
Rodriguez, F., Oliver, J. F., Marin, A. & Medina, J. R. (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142: 485501.CrossRefGoogle ScholarPubMed
Schauer, T. (1965) Ozeanische Flechten in Nordalenraum. Portugaliae Acta Biologica (B) 8: 17229.Google Scholar
Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. (2004) TREE-PUZZLE Version 5.2: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502504.CrossRefGoogle Scholar
Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16: 11141116.CrossRefGoogle Scholar
Strimmer, K. & Rambaut, A. (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the Royal Society of London, Biological Sciences 269: 137142.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Thell, A., Feuerer, T., Kärnefelt, I., Myllys, L. & Stenroos, S. (2004) Monophyletic groups within the Parmeliaceae identified by ITS rDNA, β-tubulin and GAPDH sequences. Mycological Progress 3: 297314.CrossRefGoogle Scholar
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weigh matrix choice. Nucleic Acids Research 22: 46734680.CrossRefGoogle Scholar
Wang, S. L., Chen, J. B. & Elix, J. A. (2000) New species of Parmeliaceae (lichenized Ascomycotina) from China. Mycotaxon 76: 293298.Google Scholar
Wiens, J. J. (1998) Combining data sets with different phylogenetic histories. Systematic Biology 47: 568581.CrossRefGoogle ScholarPubMed