ORIGINAL ARTICLE
Emmanuelia, a new genus of lobarioid lichen-forming fungi (Ascomycota: Peltigerales): phylogeny and synopsis of accepted species
| 1 | Evolution and Conservation Biology, InBIOS Research Center, University
of Liège, Quartier Vallée 1, Chemin de la Vallée 4, B-4000
Liège, Belgium |
| 2 | Botanischer Garten Und Botanisches Museum, Freie Universität Berlin, Germany |
| 3 | Universidad Distrital Francisco José de Caldas, Torre de Laboratorios,
Herbario, Bogotá, 11021, Colombia |
| 4 | Field Museum, Science and Education, Chicago, IL 60605, USA |
| 5 | Committee on Evolutionary Biology, University of Chicago, 1025 E.
57th Street, Chicago, IL 60637, USA |
| 6 | Biodiversity Integration Knowledge Center, Arizona State University,
PO Box 874108, Arizona State University, Tempe, AZ 85287-4108, USA |
| 7 | Instituto Nacional de Biodiversidad (INABIO), Quito, Ecuador |
| 8 | Charles Darwin Foundation for the Galapagos Islands (CDF), Galápagos,
Ecuador |
| 9 | Departamento de Biociências, Universidade Federal de Sergipe, CEP:
49500-000, Itabaiana, Sergipe, Brazil |
| 10 | Universidade da Região de Joinville, Departamento de Ciências
Biológicas, Laboratório de Liquenologia, Rua: Paulo Malschitzki,
n° 10 – Zona Industrial, CEP: 89219-710 – Joinville, SC, Brazil |
| 11 | Fundação Zoobotânica do Rio Grande do Sul, Museu de Ciências
Naturais, Porto Alegre, RS, Brasil |
| 12 | Laboratório de Botânica / Liquenologia, Instituto de Biociências, Universidade
Federal de Mato Grosso do Sul, CEP 79070-900, Campo
Grande – MS, Brazil |
| 13 | Department of Ecology and Evolutionary Biology, University of
Connecticut, Storrs, CT 06269-3043, USA |
| 14 | Department of Plant and Environmental Sciences, University of
Copenhagen,
Thorvaldsensvej 40, 1871 Frederiksberg, Denmark |
Publication date: 2020-06-02
Plant and Fungal Systematics 2020; 65(1): 76–94
KEYWORDS
ABSTRACT
The former family Lobariaceae, now included in Peltigeraceae as subfamily
Lobarioideae, has undergone substantial changes in its generic classification in recent
years, based on phylogenetic inferences highlighting the polyphyly of the speciose genera
Lobaria, Pseudocyphellaria and Sticta. Here we introduce the new genus Emmanuelia,
named in honor of Prof. Emmanuël Sérusiaux for his extensive work on the Peltigerales.
Emmanuelia currently comprises twelve species. It is superficially similar to the lobarioid
genus Ricasolia, but differs by its apothecia, rimmed by overarching and often crenulate to
lobulate margins, with the parathecium (proper excipulum) and the amphithecium (thalline
excipulum formed by the thallus cortex) apically separated and of a different structure.
Also, ascospore dimensions and shape differ between the two genera, with the ascospores
of Emmanuelia being longer and narrower. Molecular phylogenetic analyses using DNA
nucleotide sequences of the internal transcribed spacer region (ITS) and the small subunit
of mitochondrial ribosomal DNA (mtSSU) confirm that Emmanuelia belongs to the
Lobaria s.lat. clade and forms a monophyletic group sister to the lineage consisting of
Dendriscosticta, Lobariella and Yoshimuriella. None of the available generic names of
lobarioid lichens can be applied to this group, and consequently a new name is proposed
for this new genus, which is typified with E. ravenelii comb. nov. Eleven other species are
transferred to Emmanuelia: E. americana comb. nov., E. conformis comb. nov., E. cuprea
comb. nov., E. elaeodes comb. nov., E. erosa comb. nov., E. excisa comb. nov., E. lobulifera
comb. nov., E. ornata comb. nov., E. patinifera comb. nov., E. pseudolivacea
comb. nov. and E. tenuis comb. nov. The genus is represented in North America by three
species, including E. lobulifera, which is resurrected from synonymy with E. (Lobaria)
tenuis, a South American species, and E. ornata, whose populations were previously treated
under E. (Lobaria) ravenelii.
REFERENCES (73)
1.
Avise, J. C. & Johns, G. C. 1999. Proposal for a standardized temporal scheme of biological classification for extant species. Proceedings of the National Academy of Sciences of the United States of America 96: 7358–7363.
2.
Batalha-Filho, H., Fjeldså, J., Fabre, P. H. & Miyaki, C. Y. 2013. Connections between the Atlantic and the Amazonian forest avifaunas represent distinct historical events. Journal of Ornithology 154: 41–50.
3.
Brako, L., Dibben, M. J. & Amaral, I. D. 1985. Preliminary notes on the macrolichens of Serra do Cachimbo, northcentral Brazil. Acta Amazonica 15: 123–136.
4.
Brotzu, P., Melluso, L., Bennio, L., Gomes, C. B., Lustrino, M., Morbidelli, L., Morra, V., Ruberti, E., Tassinari, C. & d’Antonio, M. 2007. Petrogenesis of the Early Cenozoic potassic alkaline complex of Morro de São João, southeastern Brazil. Journal of South American Earth Sciences 24: 93–115.
5.
Büdel, B., Meyer, A., Salazar, N., Zellner, H., Zotz, G. & Lange, O. L. 2000. Macrolichens of montane rain forests in Panama, Province Chiriquí. The Lichenologist 32: 539–551.
6.
Clement, M., Posada, D. & Crandall, K. A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.
7.
Colombo, A. F. & Joly, C. A. 2010. Brazilian Atlantic Forest lato sensu: the most ancient Brazilian forest, and a biodiversity hotspot, is highly threatened by climate change. Brazilian Journal of Biology 70: 697–708.
8.
Cornejo, C., Derr, C. & Dillman, K. 2017. Ricasolia amplissima (Lobariaceae): One species, three genotypes and a new taxon from south-eastern Alaska. The Lichenologist 49: 579–596.
9.
Cubero, O. F., Crespo, A., Fatehi, J. & Bridge, P. D. 1999. DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Systematics and Evolution 216: 243–249.
10.
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.
11.
Drummond, A. J. & Rambaut, A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC evolutionary biology 7: 214.
12.
Etayo, J., Flakus, A. & Kukwa, M. 2018. Three new lichenicolous species of the genus Plectocarpon (Ascomycota: Lecanographaceae) discovered in the Bolivian Andes. Phytotaxa 357: 275–283.
13.
Fouquet, A., Loebmann, D., Castroviejo-Fisher, S., Padial, J. M., Orrico, V. G., Lyra, M. L., Roberto, I. J., Kok, P. J., Haddad, C. F. & Rodrigues, M. T. 2012. From Amazonia to the Atlantic forest: Molecular phylogeny of Phyzelaphryninae frogs reveals unexpected diversity and a striking biogeographic pattern emphasizing conservation challenges. Molecular Phylogenetics and Evolution 65: 547–561.
14.
Galloway, D. J. 2015. Contributions to a history of New Zealand lichenology 5*. James Murray (1923–1961). Phytotaxa 198: 1–67.
15.
Galloway, D. J. & Elix, J. A. 2013. Reinstatement of Crocodia Link (Lobariaceae: Ascomycota) for five species formerly included in Pseudocyphellaria Vain. Australasian Lichenology 72: 32–42.
16.
Gardes, M. & Bruns, T. D. 1993. ITS primers with enhanced specificity for basidiomycetes–application to the identification of mycorrhizae and rusts. Molecular ecology 2: 113–118.
17.
Gernhard, T. 2008. The conditioned reconstructed process. Journal of Theoretical Biology 253: 769–778.
18.
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321.
19.
Högnabba, F., Stenroos, S. & Thell, A. 2009. Phylogenetic relationship and evolution of photobiont associations in the Lobariaceae (Peltigerales, Lecanoromycetes, Ascomycota). Bibliotheca Lichenologica 100: 157–187.
20.
Hoorn, C., Wesselingh, F. P., Ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A., Anderson, C. L., Figueiredo, J. P. & Jaramillo, C., 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927–931.
21.
Jordan, W. P. 1972. Erumpent cephalodia, an apparent case of phycobial influence on lichen morphology. Journal of Phycology 8: 112–117.
22.
Jordan, W. P. 1973. The genus Lobaria in North America North of Mexico. The Bryologist 76: 225–251.
23.
Käffer, M. I., Ganade, G. & Marcelli, M. P. 2009. Lichen diversity and composition in Araucaria forests and tree monocultures in southern Brazil. Biodiversity and Conservation 18: 3543–3561.
24.
Käffer, M. I., Dantas, R. V. & Martins, S. M. d. A., 2016. Characterization of the epiphytic lichen vegetation in a riparian forest in southern Brazil. Plant Ecology and Evolution 149: 92–100.
25.
Kalb, K. 1983. Lichenes Neotropici, Fascikel VI (No. 201–250). Published by the author, Neumarkt/OPf., Germany.
26.
Katoh, K. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–3066.
27.
Katoh, K., Asimenos, G. & Toh, H. 2009. Multiple alignment of DNA sequences with MAFFT. Methods in molecular biology 537: 39–64.
28.
Kraichak, E., Crespo, A., Divakar, P. K., Leavitt, S. D. & Lumbsch, H. T. 2017. A temporal banding approach for consistent taxonomic ranking above the species level. Scientific Reports 7: 1–7.
29.
Kraichak, E., Huang, J.-P., Nelsen, M., Leavitt, S. D. & Lumbsch, H. T. 2018. A revised classification of orders and families in the two major subclasses of Lecanoromycetes (Ascomycota) based on a temporal approach. Botanical Journal of the Linnean Society 188: 233–249.
30.
Lanfear, R., Calcott, B., Ho, S. Y. W. & Guindon, S. 2012. PartitionFinder: Combined Selection of Partitioning Schemes and Substitution Models for Phylogenetic Analyses. Molecular Biology and Evolution 29: 1695–1701.
31.
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. 2016. Partition- Finder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34: 772–773.
32.
Lehnen, P. G., Käffer, M. I., Lucheta, F. & Schmitt, J. L. 2017. Estrutura da comunidade de liquens corticícolas em área urbana e rural no município de Novo Hamburgo, Rio Grande do Sul, Brasil. Iheringia. Série Botânica 72: 66–74.
33.
Leigh, J. W. & Bryant, D. 2015. POPART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution 6: 1110–1116.
34.
Lohtander, K., Oksanen, I. & Rikkinen, J. 2002. A phylogenetic study of Nephroma (lichen-forming Ascomycota). Mycological Research 106: 777–787.
35.
Lücking, R. 2019. Stop the Abuse of Time! Strict Temporal Banding is not the Future of Rank-Based Classifications in Fungi (Including Lichens) and Other Organisms. Critical Reviews in Plant Sciences 38: 199–253.
36.
Lücking, R., Dal Forno, M., Moncada, B., Coca, L. F., Vargas-Mendoza, L. Y., Aptroot, A., Arias, L. J., Besal, B., Bungartz, F., Cabrera-Amaya, D. M., Cáceres, M. E. S., Chaves, J. L., Eliasaro, S., Gutiérrez, M. C., Hernández-M., J. E., Herrera-Campos, M. A., Holgado-Rojas, M. E., Jonitz, H., Kukwa, M., Lucheta, F., Madriñán, S., Marcelli, M. P., Martins, S. M. A., Mercado-Díaz, J. A., Molina, J. A., Morales, E. A., Nelson, P. R., Nugra, F., Ortega, F., Paredes, T., Patiño, A. L., Peláez-Pulido, R. N., Pérez-Pérez, R. E., Perlmutter, G. B., Rivas-Plata, M. E., Robayo, J., Rodríguez, C., Simijaca, D. F., Soto-Medina, E., Spielmann, A. A., Suárez-Corredor, A., Torres, J. M., Vargas, C. A., Yánez-Ayabaca, A., Weerakoon, G., Wilk. K., Celis-Pacheco, M., Diazgranados, M., Brokamp, G., Borsch, T., Gillevet, P. M., Sikaroodi, M. & Lawrey, J. D. 2017a. Turbo-taxonomy to assemble a megadiverse lichen genus: seventy new species of Cora (Basidiomycota: Agaricales: Hygrophoraceae), honouring David Leslie Hawksworth’s seventieth birthday. Fungal Diversity 84: 139–207.
37.
Lücking, R., Moncada B. & Smith C. W. 2017b. The genus Lobariella (Ascomycota: Lobariaceae) in Hawaii: late colonization, high inferred endemism and three new species resulting from ‘micro-radiation’. The Lichenologist 49: 673–691.
38.
Lumbsch, T. H. & Leavitt, S. D. 2019. Introduction of subfamily names for four clades in Cladoniaceae and Peltigeraceae (Lecanoromycetes). Mycotaxon 134: 271–273.
39.
Machado, L. F., Loss, A. C., Paz, A., Vieira, E. M., Rodrigues, F. P. & Marinho-Filho, J. 2018. Phylogeny and biogeography of Phyllomys (Rodentia: Echimyidae) reveal a new species from the Cerrado and suggest Miocene connections of the Amazon and Atlantic Forest. Journal of Mammalogy 99: 377–396.
40.
Magain, N., Goffinet, B. & Sérusiaux, E. 2012. Further photomorphs in the lichen family Lobariaceae from Reunion (Mascarene archipelago) with notes on the phylogeny of Dendriscocaulon cyanomorphs. The Bryologist 115: 243–254.
41.
Magain, N. & Sérusiaux, E. 2015. Dismantling the treasured flagship lichen Sticta fuliginosa (Peltigerales) into four species in Western Europe. Mycological Progress 14: 1–33.
42.
McCune, B., Rosentreter, R., Spribille, T., Breuss, O. & Wheeler, T. B. 2014. Montana Lichens: An Annotated List. Vol. 2. Northwest Lichenologists, Corvallis, Oregon.
43.
Miadlikowska, J., Kauff, F., Hofstetter, V., Fraker, E., Grube, M., Hafellner, J., Reeb, V., Hodkinson, B. P., Kukwa, M., Lücking, R., Hestmark, G., Garcia Otalora, M., Rauhut, A., Büdel, B., Scheidegger, C., Timdal, E., Stenroos, S., Brodo, I., Perlmutter, G., Ertz, D., Diederich, P., Lendemer, J. C., May, P., Schoch, C. L., Arnold, A. E., Gueidan, C., Tripp, E., Yahr, R., Robertson, C. & Lutzoni, F. 2006. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98: 1088–1103.
44.
Miller, M. A., Pfeiffer, W. & Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE) IEEE: 1–8.
45.
Moncada, B., Lücking, R. & Betancourt-Macuase, L. 2013. Phylogeny of the Lobariaceae (lichenized Ascomycota: Peltigerales), with a reappraisal of the genus Lobariella. The Lichenologist 45: 203–263.
46.
Moore, B. J. 1969. Lobaria lobulifera, a New Species from the Southeastern United States. The Bryologist 72: 404–406.
48.
Orange, A., James, P. W. & White, F. J. 2001. Microchemical methods for the identification of lichens. London: British Lichen Society.
49.
Osorio, H. S. & Fleig, M. 1987. Contribution to the lichen flora of Brazil. XIX. New or additional records from Santa Maria, Rio Grande do Sul State. Comunicaciones Botanicas del Museo de Historia Natural de Montevideo 5: 1–8.
50.
Penn, O., Privman, E., Ashkenazy, H., Landan, G., Graur, D. & Pupko, T. 2010a. GUIDANCE: A web server for assessing alignment confidence scores. Nucleic Acids Research 38: 23–28.
51.
Penn, O., Privman, E., Landan, G., Graur, D. & Pupko, T. 2010b. An alignment confidence score capturing robustness to guide tree uncertainty. Molecular Biology and Evolution 27: 1759–1767.
52.
Peucker‐Ehrenbrink, B. & Miller, M. W. 2007. Quantitative bedrock geology of Brazil. Geochemistry, Geophysics, Geosystems 8(5): 8000.
53.
Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. 2014. Tracer v1.6. Retrieved from http://tree.bio.ed.ac.uk/softw... (accessed in May 2020).
54.
Sela, I., Ashkenazy, H., Katoh, K. & Pupko, T. 2015. GUIDANCE2: Accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research 43: W7–W14.
55.
Schmull, M., Miadlikowska, J., Pelzer, M., Stocker-Wörgötter, E., Hofstetter, V., Fraker, E., Hodkinson, B. P., Reeb, V., Kukwa, M., Lumbsch, H. T., Kauff, F. & Lutzoni, F. 2011. Phylogenetic affiliations of members of the heterogeneous lichen- forming fungi of the genus Lecidea sensu Zahlbruckner (Lecanoromycetes, Ascomycota). Mycologia 103: 983–1003.
56.
Sipman, H. J. M. 1993. Lichenotheca Latinoamericana a museo botanico berolinensi edita, fasciculum secundum. Willdenowia 23: 305–314.
57.
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
58.
Stenroos, S., Stocker-Wörgötter, E., Yoshimura, I., Myllys, L., Thell, A. & Hyvönen, J. 2003. Culture experiments and DNA sequence data confirm the identity of Lobaria photomorphs. Canadian Journal of Botany 81: 232–247.
59.
Stizenberger, E. 1895. Die Grübchenflechten (Stictei) und ihre geographische Verbreitung. Flora, Jena 81: 88–150.
60.
Simon, A., Goffinet, B., Magain N. & Sérusiaux, E. 2018. High diversity, high insular endemism and recent origin in the lichen genus Sticta (lichenized Ascomycota, Peltigerales) in Madagascar and the Mascarenes. Molecular Phylogenetics and Evolution 122: 15–28.
61.
Takahashi, K., Wang, L.-S., Tsubota, H. & Deguchi, H. 2006. Photosymbiodemes Sticta wrightii and Dendriscocaulon sp. (lichenized Ascomycota) from Yunnan, China. Journal of the Hattori Botanical Laboratory 100: 783–796.
62.
Thomas, M. A., Ryan, D. J., Farnden, K. J. F. & Galloway, D. J. 2002. Observations on phylogenetic relationships within Lobariaceae Chevall. (Lecanorales, Ascomycota) in New Zealand, based on ITS-5.8S molecular sequence data. Bibliotheca Lichenologica 82: 123–138.
63.
Tønsberg, T., Blom, H., Goffinet, B., Holtan-Hartwig, J. & Lindblom, L. 2016. The cyanomorph of Ricasolia virens comb. nov. (Lobariaceae, lichenized Ascomycetes). Opuscula Philolichenum 15: 12–21.
64.
Tuckerman, E. 1882. A Synopsis of the North American Lichens. Part 1. Boston, Massachusetts, USA, p. 176.
65.
White, T. J., Bruns, S., Lee, S. & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: A guide to methods and applications. 18: 315–322.
66.
Widhelm, T. J., Grewe, F., Huang, J. P., Mercado-Díaz, J. A., Goffinet, B., Lücking, R., Moncada, B., Mason-Gamer, R. & Lumbsch, H. T. 2019. Multiple historical processes obscure phylogenetic relationships in a taxonomically difficult group (Lobariaceae, Ascomycota). Scientific Reports 9: 8968.
67.
Wiklund, E. & Wedin, M. 2003. The phylogenetic relationships of the cyanobacterial lichens in the Lecanorales suborder Peltigerineae. Cladistics 19: 419–431.
68.
Yoshimura, I. 1971. The genus Lobaria of Eastern Asia. Journal of the Hattori Botanical Laboratory 34: 231–364.
69.
Yoshimura, I. 1998. Lobaria in Latin America: taxonomic, geographic and evolutionary aspects. In: Marcelli, M. P. & Seaward, M. R. D. (eds) Lichenology in Latin America: History, Current Knowledge and Applications, pp. 129–134. CETESB – Companhia de Tecnologia de Saneamento Ambiental, São Paulo.
70.
Yoshimura, I. & Osorio, H. 1975. Notes on Lobaria cuprea with purple pigment. Journal of the Hattori Botanical Laboratory 39: 263–268.
71.
Yu, G., Smith, D. K., Zhu, H., Guan, Y. & Lam, T. T.-Y. 2017. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution 8: 28–36.
72.
Yule, G. 1924. A mathematical theory of evolution, based on the conclusions of Dr. JC Willis. FRS Philosophical Transactions of the Royal Society of London B213: 21–87.
73.
Zoller, S., Scheidegger, C. & Sperisen, C. 1999. PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. The Lichenologist 31: 511–516.
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