Hostname: page-component-745bb68f8f-5r2nc Total loading time: 0 Render date: 2025-01-12T05:34:45.896Z Has data issue: false hasContentIssue false
  • English
  • Français

Microchemical and molecular investigations reveal Pseudephebe species as cryptic with an environmentally modified morphology

Published online by Cambridge University Press:  27 September 2016

Carlos G. BOLUDA ,
David L. HAWKSWORTH ,
Pradeep K. DIVAKAR ,
Ana CRESPO  and
Víctor J. RICO
Carlos G. BOLUDA*
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense, Plaza de Ramón y Cajal s/n, Madrid 28040, Spain
David L. HAWKSWORTH
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense, Plaza de Ramón y Cajal s/n, Madrid 28040, Spain Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK; and Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, Surrey TW9 3DS, UK
Pradeep K. DIVAKAR
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense, Plaza de Ramón y Cajal s/n, Madrid 28040, Spain
Ana CRESPO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense, Plaza de Ramón y Cajal s/n, Madrid 28040, Spain
Víctor J. RICO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense, Plaza de Ramón y Cajal s/n, Madrid 28040, Spain
*
Email: carlgala@ucm.es
Get access Rights & Permissions [Opens in a new window]

Abstract

The results of the first molecular phylogenetic study of Pseudephebe are presented; a three-locus phylogeny. The genus is confirmed as monophyletic within the alectorioid clade of Parmeliaceae. Two major clades were recovered, which can be assigned to the two traditional taxa, P. minuscula and P. pubescens, with modifications of the species delimitation, especially the variable P. minuscula. These species are cryptic and cannot be confidently distinguished morphologically due to phenotypic convergence. Therefore, the use of P. pubescens aggr. is recommended for samples not molecularly analyzed. Contrary to previous studies, specimens of both species might have indistinct pseudocyphellae and also contain lichen substances; norstictic acid was detected in c. 60% of specimens tested. An SSU 1516 Group I intron is usually present in P. minuscula but always absent in P. pubescens. The species-level nomenclature is summarized and sequenced reference specimens (RefSpec) for both Pseudephebe species are selected. Sequences from Bryoria mariensis established that this name was a synonym of P. minuscula.

Keywords

Alectorioid cladebarcodingBryoriaintronlichenParmeliaceaephenotypic convergence
Type
Articles
Information
The Lichenologist , Volume 48 , Issue 5 , September 2016 , pp. 527 - 543
Copyright
© British Lichen Society, 2016 

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

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723.CrossRefGoogle Scholar
Ariyawansa, H. A., Hawksworth, D. L., Hyde, K. D., Jones, E. B. G., Maharachchikumbura, S. S. N., Manamgoda, D. S., Thambugala, K. M., Udayanga, D., Camporesi, E., Daranagama, A. et al. (2014) Epitypification and neotypification: guidelines with appropriate and inappropriate examples. Fungal Diversity 69: 57–91.CrossRefGoogle Scholar
Arnold, F. (1878) Lichenologische Ausfläge in Tirol. XVII. Windischmatrei. Verhandlungen den Kaiserlich-Königlichen Zoologisch-Botanischen Gesellschaft in Wien 28: 247–296.Google Scholar
Bhattacharya, D., Reeb, V., Simon, D. & Lutzoni, F. (2005) Phylogenetic analyses suggest reverse splicing spread of group I introns in fungal ribosomal DNA. BMC Evolutionary Biology 5: 68.CrossRefGoogle Scholar
Brodo, I. M. & Hawksworth, D. L. (1977) Alectoria and allied genera in North America. Opera Botanica 42: 1–164.Google Scholar
Campbell, V., Legendre, P. & Lapointe, F. J. (2011) The performance of the Congruence Among Distance Matrices (CADM) test in phylogenetic analysis. BMC Evolutionary Biology 11: 64.CrossRefGoogle ScholarPubMed
Clokie, H. N. (1964) An Account of the Herbaria of the Department of Botany in the University of Oxford. Oxford: Oxford University Press.Google Scholar
Common, R. S. (1991) The distribution and taxonomic significance of lichenan and isolichenan in the Parmeliaceae (lichenized Ascomycotina), as determined by iodine reactions. I. Introduction and methods. II. The genus Alectoria and associated taxa. Mycotaxon 41: 67–112.Google Scholar
Common, R. S. & Brodo, I. M. (1995) Bryoria sect. Subdivergentes recognized as the new genus Nodobryoria (lichenized Ascomycotina). Bryologist 98: 189–206.Google Scholar
Crespo, A. & Lumbsch, H. T. (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1: 167–170.CrossRefGoogle ScholarPubMed
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: 807–819.Google Scholar
Crespo, A., Kauff, F., Divakar, P. K., del Prado, R., Pérez-Ortega, S., Amo de Paz, G., Ferencova, Z., Blanco, O., Roca-Valiente, B., Núñez-Zapata, J. et al. (2010) Phylogenetic generic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence. Taxon 59: 1735–1753.Google Scholar
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.Google Scholar
Dillenius, J. J. (1742) [“1741”] Historia Muscorum. Oxford: Sheldonian Theatre.Google Scholar
Divakar, P. K., Crespo, A., Wedin, M., Leavitt, S. D., Hawksworth, D. L., Myllys, L., McCune, B., Randlane, T., Bjerke, J. W., Ohmura, Y. et al. (2015) Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi. New Phytologist 208: 1217–1226.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: 359–383.Google Scholar
Fryday, A. M. & Øvstedal, D. O. (2012) New species, combinations and records of lichenized fungi from the Falkland Islands (Islas Malvinas). Lichenologist 44: 483–500.CrossRefGoogle Scholar
Gutiérrez, G., Blanco, O., Divakar, P. K., Lumbsch, H. T. & Crespo, A. (2007) Patterns of group I intron presence in nuclear SSU rDNA of the lichen family Parmeliaceae . Journal of Molecular Evolution 64: 181–195.CrossRefGoogle Scholar
Haugen, P., Reeb, V., Lutzoni, F. & Bhattacharya, D. (2004) The evolution of homing endonuclease genes and group I introns in nuclear rDNA. Molecular Biology and Evolution 21: 105–116.CrossRefGoogle Scholar
Hawksworth, D. L. (1972) Regional studies in Alectoria (Lichenes). II. The British Species. Lichenologist 5: 181–261.Google Scholar
Hawksworth, D. L. (1973) Ecological factors and species delimitation in lichens. In Taxonomy and Ecology (V. H. Heywood, ed.): 31–69. [Systematics Association Special Vol. 5.] London: Academic Press.Google Scholar
Hawksworth, D. L. & Iturriaga, T. (2006) Lichenicolous fungi described from Antarctica and the sub-Antarctic islands by Carroll W. Dodge (1895–1988). Antarctic Science 18: 291–301.CrossRefGoogle Scholar
Hillmann, J. (1936) Parmeliaceae. In Dr. L. Rabenhorst Kryptogamen-Flora von Deutschland, Österreich und der Schweiz 9, 5(3): 1–309. Leipzig: Akademische Verlag.Google Scholar
Howe, R. H. Jr. (1912) The lichens of the Linnean herbarium with remarks on Acharian material. Bulletin of the Torrey Botanical Club 39: 199–203.Google Scholar
Huelsenbeck, J. P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.CrossRefGoogle ScholarPubMed
Imshaug, H. A. (1957) Alpine lichens of western United States and adjacent Canada. I. The macrolichens. Bryologist 60: 177–272.Google Scholar
Jørgensen, P. M., James, P. W. & Jarvis, C. E. (1994) Linnaean lichen names and their typification. Botanical Journal of the Linnean Society 115: 261–405.Google Scholar
Kantvilas, G. (1994) Pseudephebe . Flora of Australia 55: 162–163.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
Lamb, I. M. (1948) New, rare or interesting lichens from the Southern Hemisphere. Lilloa 14: 203–251.Google Scholar
Lamb, I. M. (1964) Antarctic lichens I. The genera Usnea, Ramalina, Himantormia, Alectoria, and Cornicularia . British Antarctic Survey Science Reports 38: 1–34.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
Leavitt, S. D., Esslinger, T. L., Divakar, P. K. & Lumbsch, H. T. (2012) Miocene and Pliocene dominated diversification of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota) and Pleistocene population expansions. BMC Evolutionary Biology 12: 176.CrossRefGoogle ScholarPubMed
Leavitt, S. D., Moreau, C. S. & Lumbsch, H. T. (2015) The dynamic discipline of species delimitation: progress toward effectively recognizing species boundaries in natural populations. In Recent Advances in Lichenology (D. K. Upreti, P. K. Divakar, V. Shukla & R. Bajpai, eds): 11–44. New Delhi: Springer.Google Scholar
Legendre, P. & Lapointe, F. J. (2004) Assessing congruence among distance matrices: single-malt Scotch whiskies revisited. Australian and New Zealand Journal of Statistics 46: 615–629.CrossRefGoogle Scholar
Linnaeus, C. (1753) Species Plantarum. Vol. 2. Stockholm: L. Salvius.Google Scholar
Lumbsch, H. T. & Huhndorf, S. M. (2010) Myconet Volume 14. Part Two. Notes on ascomycete systematics. Nos. 4751–5113. Fieldiana, Life and Earth Sciences 1: 42–64.Google Scholar
Lynge, B. (1915–16) Index specierum et varietum lichenum quae collectionibus “Lichenes Exsiccati” distributae sunt. [Pars I (1)]. Nyt Magazin for Naturvidensk 53–54: 1–304.Google Scholar
Matheny, P. B., Liu, Y. J., Ammirati, J. F & Hall, B. D. (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). American Journal of Botany 89: 688–698.Google Scholar
Miller, M. A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, Louisiana, pp. 1–8.Google Scholar
Molina, M. C., Del-Prado, R, Divakar, P. K. & Crespo, A. (2011 a) Another example of cryptic diversity in lichen-forming fungi: the new species Parmelia mayi (Ascomycota: Parmeliaceae). Organisms, Diversity and Evolution 11: 331–342.Google Scholar
Molina, M. C., Divakar, P. K., Millanes, A. M. & Crespo, A. (2011 b) Parmelia sulcata (Ascomycota: Parmeliaceae), a sympatric monophyletic species complex. Lichenologist 43: 585–601.Google Scholar
Myllys, L., Velmala, S. & Holien, H. (2011) Pseudephebe. In Nordic Lichen Flora. Vol. 4. Parmeliaceae (A. Thell & R. Moberg, eds): 99–101. Uppsala: Nordic Lichen Society.Google Scholar
Orange, A., James, P. W. & White, F. J. (2010) Microchemical Methods for the Identification of Lichens, 2nd edn. London: British Lichen Society.Google Scholar
Øvstedal, D. O. & Smith, R. I. L. (2001) Lichens of Antarctica and South Georgia: A Guide to Their Identification and Ecology. Cambridge: Cambridge University Press.Google Scholar
Paradis, E., Claude, J. & Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.Google Scholar
Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2011) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.Google Scholar
Rambaut, A. (2009) FigTree. v1.4. Available from: http://tree.bio.ed.uk/software/figtree/.Google Scholar
Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. (2014) Tracer version 1.6. Available from: http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Reeb, V., Haugen, P., Bhattacharya, D. & Lutzoni, F. (2007) Evolution of Pleopsidium (lichenized Ascomycota) S943 group I introns and the phylogeography of an intron-encoded putative homing endonuclease. Journal of Molecular Evolution 64: 285–298.CrossRefGoogle Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.Google Scholar
Schmitt, I., Crespo, A., Divakar, P. K., Fankhauser, J. D., Herman-Sackett, E., Kalb, K., Nelsen, M. P., Nelson, N. A., Rivas-Plata, E., Shimp, A. D. et al. (2009) New primers for promising single-copy genes in fungal phylogenies and systematics. Persoonia 23: 35–40.Google Scholar
Simon, D. M., Hummel, C. L., Sheeley, S. L. & Bhattacharya, D. (2005) Heterogeneity of intron presence or absence in rDNA genes of the lichen species Physcia aipolia and P. stellaris . Current Genetics 47: 389–399.CrossRefGoogle ScholarPubMed
Smith, C. W., Aptroot, A., Coppins, B. J., Fletcher, A., Gilbert, O. L., James, P. W. & Wolseley, P. A. (eds) (2009) The Lichens of Great Britain and Ireland. London: British Lichen Society.Google Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.Google Scholar
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML webservers. Systematic Biology 57: 758–771.Google Scholar
Sultan, S. E. (2015) Organism and Environment: Ecological Development, Niche Construction, and Adaptation. Oxford: Oxford University Press.Google Scholar
Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564–577.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.Google Scholar
Toju, H., Tanabe, A. S., Yamamoto, S. & Sato, H. (2012) High-coverage ITS for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS ONE 7: e40863.Google Scholar
Velmala, S., Myllys, L., Goward, T., Holien, H. & Halonen, P. (2014) Taxonomy of Bryoria section Implexae (Parmeliaceae, Lecanoromycetes) in North America and Europe, based on chemical, morphological and molecular data. Annales Botanici Fennici 51: 345–371.Google Scholar
Wang, L.-S. & McCune, B. (2010) Contributions to the lichen flora of the Hengduan Mountains, China 1. Genus Pseudephebe (lichenized Ascomycota, Parmeliaceae). Mycotaxon 113: 431–437.CrossRefGoogle Scholar
Yang, Z. & Rannala, B. (2010) Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of the United States of America 107: 9264–9269.CrossRefGoogle ScholarPubMed
Zamora, J. C., Calonge, F. D. & Martín, M. P. (2015) Integrative taxonomy reveals an unexpected diversity in Geastrum section Geastrum (Geastrales, Basidiomycota). Persoonia 34: 130–165.Google Scholar
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.Google Scholar
Supplementary material: File

Boluda supplementary material

Boluda supplementary material 1

Download Boluda supplementary material(File)
File 115.8 KB