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Phylogenetic evidence for an expanded circumscription of Gabura (Arctomiaceae)

Published online by Cambridge University Press:  04 March 2020

Nicolas Magain Open the ORCID record for Nicolas Magain [Opens in a new window] ,
Toby Spribille Open the ORCID record for Toby Spribille [Opens in a new window] ,
Joseph DiMeglio ,
Peter R. Nelson ,
Jolanta Miadlikowska  and
Emmanuël Sérusiaux
Nicolas Magain*
Affiliation:
Evolution and Conservation Biology, InBios Research Center, University of Liège, Sart Tilman B22, Quartier Vallée 1, Chemin de la vallée 4, B-4000 Liège, Belgium
Toby Spribille
Affiliation:
Department of Biological Sciences, University of Alberta, CW405, Edmonton, AlbertaT6G 2R3, Canada
Joseph DiMeglio
Affiliation:
Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR97331-2902, USA
Peter R. Nelson
Affiliation:
University of Maine at Fort Kent, 23 University Drive, Fort Kent, ME04743, USA
Jolanta Miadlikowska
Affiliation:
Department of Biology, Duke University, Durham, NC27708-0338, USA
Emmanuël Sérusiaux
Affiliation:
Evolution and Conservation Biology, InBios Research Center, University of Liège, Sart Tilman B22, Quartier Vallée 1, Chemin de la vallée 4, B-4000 Liège, Belgium
*
Author for correspondence: Nicolas Magain. E-mail: Nicolas.Magain@uliege.be
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Abstract

Since the advent of molecular taxonomy, numerous lichen-forming fungi with homoiomerous thalli initially classified in the family Collemataceae Zenker have been transferred to other families, highlighting the extent of morphological convergence within Lecanoromycetes O. E. Erikss. & Winka. While the higher level classification of these fungi might be clarified by such transfers, numerous specific and generic classifications remain to be addressed. We examined the relationships within the broadly circumscribed genus Arctomia Th. Fr., which has been the recipient of several transfers from Collemataceae. We demonstrated that Arctomia insignis (P. M. Jørg. & Tønsberg) Ertz does not belong to Arctomia s. str. but forms a strong monophyletic group with Gabura fascicularis (L.) P. M. Jørg. We also confirmed that Arctomia borbonica Magain & Sérus. and the closely related Arctomia insignis represent two species. We formally transferred A. insignis and A. borbonica to the genus Gabura Adans. and introduced two new combinations: Gabura insignis and Gabura borbonica. We reported Gabura insignis from Europe (Scotland and Ireland) for the first time. While material from Europe and North America is genetically almost identical, specimens from Madagascar, South Africa and Reunion Island belong to three distinct phylogenetic lineages, all of which are present in the latter area and may represent distinct species. In its current circumscription, the genus Gabura may contain up to six species, whereas Arctomia s. str. includes only two species (A. delicatula Th. Fr. and A. teretiuscula P. M. Jørg.). The Gabura insignis group is shown to have an unexpectedly large, subcosmopolitan distribution. With the extended sampling from Arctomiaceae Th. Fr., the placement of Steinera sorediata P. James & Henssen in the genus Steinera Zahlbr. is confirmed and the presence of a new Steinera species from Chile is highlighted.

Keywords

biogeographyIrelandlichenized fungiScotlandspecies delimitation
Type
Standard Papers
Information
The Lichenologist , Volume 52 , Issue 1 , January 2020 , pp. 3 - 15
Copyright
Copyright © British Lichen Society 2020

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References

Baloch, E, Lücking, R, Lumbsch, HT and Wedin, M (2010) Major clades and phylogenetic relationships between lichenized and non-lichenized lineages in Ostropales (Ascomycota: Lecanoromycetes). Taxon 59, 1483–1494.CrossRefGoogle Scholar
Carlberg, T (2012) Leptogium insigne P. M. Jørg. & Tønsberg, new to California. Bulletin of the California Lichen Society 19, 1–3.Google Scholar
Degelius, G (1974) The lichen genus Collema with special reference to the extra-European species. Symbolae Botanicae Upsalienses 20, 1–215.Google Scholar
Drummond, AJ and Rambaut, A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Ekman, S, Andersen, HL and Wedin, M (2008) The limitations of ancestral state reconstruction and the evolution of the ascus in the Lecanorales (lichenized Ascomycota). Systematic Biology 57, 141–156.CrossRefGoogle Scholar
Ertz, D, Poulsen, RS, Charrier, M and Søchting, U (2017) Taxonomy and phylogeny of the genus Steinera (Arctomiales, Arctomiaceae) in the subantarctic islands of Crozet and Kerguelen. Phytotaxa 324, 201–238.CrossRefGoogle Scholar
Ezard, T, Fujisawa, T and Barraclough, T (2009) splits: SPecies’ LImits by Threshold Statistics. R package version 1.0-11/r29. [WWW resource] URL https://rdrr.io/rforge/splits/Google Scholar
Fernández-Brime, S, Llimona, X, Molnar, K, Stenroos, S, Hognabba, F, Bjork, C, Lutzoni, F and Gaya, E (2011) Expansion of the Stictidaceae by the addition of the saxicolous lichen-forming genus Ingvariella. Mycologia 103, 755–763.CrossRefGoogle ScholarPubMed
Henssen, AM (1969) Eine Studie über die Gattung Arctomia. Svensk Botanisk Tidskrift 63, 126–138.Google Scholar
Jørgensen, PM (2003) A new species of Arctomia from Sichuan Province, China. Lichenologist 35, 287–289.CrossRefGoogle Scholar
Jørgensen, PM (2007) Arctomiaceae. In Jørgensen, PM, Tønsberg, T and Vitikainen, O (eds), Nordic Lichen Flora Vol. 3. Uddevalla: Nordic Lichen Society, pp. 9–11.Google Scholar
Jørgensen, PM (2014) Taxonomy and nomenclature of Collema fasciculare (L.) G. H. Weber. Lichenologist 46, 594.CrossRefGoogle Scholar
Jørgensen, PM and Palice, Z (2016) Leptogium insigne new to Ecuador, with notes on its generic position. Evansia 33, 14–17.CrossRefGoogle Scholar
Jørgensen, PM and Tønsberg, T (2010) Leptogium insigne, a new species from the Pacific Northwest of North America. Bibliotheca Lichenologica 104, 241–245.Google Scholar
Katoh, K, Misawa, K, Kuma, K and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.CrossRefGoogle ScholarPubMed
Kraichak, E, Huang, J-P, Nelsen, M, Leavitt, SD and Lumbsch, HT (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.Google Scholar
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.Google Scholar
Lücking, R, Dal-Forno, M, Sikaroodi, M, Gillevet, PM, Bungartz, F, Moncada, B, Yánez-Ayabaca, A, Chaves, JL, Coca, LF and Lawrey, JD (2014) A single macrolichen constitutes hundreds of unrecognized species. Proceedings of the National Academy of Sciences of the United States of America 111, 11091–11096.CrossRefGoogle ScholarPubMed
Lücking, R, Moncada, B, McCune, B, Farkas, E, Goffinet, B, Parker, D, Chaves, JL, Lőkös, L, Nelson, PR, Spribille, T, et al. (2017) Pseudocyphellaria crocata (Ascomycota: Lobariaceae) in the Americas is revealed to be thirteen species, and none of them is P. crocata. Bryologist 120, 441–500.CrossRefGoogle Scholar
Lumbsch, HT, Schmitt, I and Messuti, MI (2001) Utility of nuclear SSU and LSU rDNA data sets to discover the ordinal placement of the Coccotremataceae (Ascomycota). Organisms Diversity and Evolution 1, 99–112.CrossRefGoogle Scholar
Lumbsch, HT, Schmitt, I, Palice, Z, Wiklund, E, Ekman, S and Wedin, M (2004) Supraordinal phylogenetic relationships of Lecanoromycetes based on a Bayesian analysis of combined nuclear and mitochondrial sequences. Molecular Phylogenetics and Evolution 31, 822–832.CrossRefGoogle ScholarPubMed
Lumbsch, HT, del Prado, R and Kantvilas, G (2005) Gregorella, a new genus to accommodate Moelleropsis humida and a molecular phylogeny of Arctomiaceae. Lichenologist 37, 291–302.CrossRefGoogle Scholar
Lumbsch, HT, Schmitt, I, Lücking, R, Wiklund, E and Wedin, M (2007 a) The phylogenetic placement of Ostropales within Lecanoromycetes (Ascomycota) revisited. Mycological Research 111, 257–267.CrossRefGoogle ScholarPubMed
Lumbsch, HT, Schmitt, I, Mangold, A and Wedin, M (2007 b) Ascus types are phylogenetically misleading in Trapeliaceae and Agyriaceae (Ostropomycetidae, Ascomycota). Mycological Research 111, 1133–1141.CrossRefGoogle Scholar
Maddison, WP and Maddison, DR (2016) Mesquite: a modular system for evolutionary analysis. Version 3.1.1. [WWW resource] URL http://mesquiteproject.org.Google Scholar
Magain, N and Sérusiaux, E (2012) A further new species in the lichen genus Arctomia: A. borbonica from Reunion (Mascarene archipelago). MycoKeys 4, 9–21.CrossRefGoogle Scholar
Magain, N and Sérusiaux, E (2014) Do photobiont switch and cephalodia emancipation act as evolutionary drivers in the lichen symbiosis? A case study in the Pannariaceae (Peltigerales). PLoS ONE 9, e89876.CrossRefGoogle Scholar
Magain, N and Sérusiaux, E (2015) Dismantling the treasured flagship lichen Sticta fuliginosa (Peltigerales) into four species in Western Europe. Mycological Progress 14, 97.CrossRefGoogle Scholar
Magain, N, Miadlikowska, J, Goffinet, B, Sérusiaux, E and Lutzoni, F (2017) Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Systematic Biology 66, 74–99.Google Scholar
Miadlikowska, J, Kauff, F, Hofstetter, V, Fraker, E, Grube, M, Hafellner, J, Reeb, V, Hodkinson, BP, Kukwa, M, Lücking, R, et al. (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.CrossRefGoogle ScholarPubMed
Miadlikowska, J, Kauff, F, Högnabba, F, Oliver, JC, Molnár, K, Fraker, E, Gaya, E, Hafellner, J, Hofstetter, V, Gueidan, C, et al. (2014) A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Molecular Phylogenetics and Evolution 79, 132–168.CrossRefGoogle ScholarPubMed
Miller, MA, Pfeiffer, W and 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
Moncada, B, Lücking, R and Suárez, A (2014) Molecular phylogeny of the genus Sticta (lichenized Ascomycota: Lobariaceae) in Colombia. Fungal Diversity 64, 205–231.CrossRefGoogle Scholar
Nylander, JAA (2008) MrModeltest v2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.Google Scholar
Otálora, MAG and Wedin, M (2013) Collema fasciculare belongs in Arctomiaceae. Lichenologist 45, 295–304.CrossRefGoogle Scholar
Øvstedal, DO and Gremmen, NJM (2001) The lichens of Marion and Prince Edward Islands. South African Journal of Botany 67, 552–572.CrossRefGoogle Scholar
Øvstedal, DO and Gremmen, NJM (2006) Lichens of sub-Antarctic Heard Island. South African Journal of Botany 72, 353–366.CrossRefGoogle Scholar
Pons, J, Barraclough, TG, Gomez-Zurita, J, Cardoso, A, Duran, DP, Hazell, S, Kamoun, S, Sumlin, WD and Vogler, AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.CrossRefGoogle ScholarPubMed
R Core Team (2016) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. [WWW resource] URL https://www.R-project.orgGoogle Scholar
Resl, P, Schneider, K, Westberg, M, Printzen, C, Palice, Z, Thor, G, Fryday, A, Mayrhofer, H and Spribille, T (2015) Diagnostics for a troubled backbone: testing topological hypotheses of trapelioid lichenized fungi in a large-scale phylogeny of Ostropomycetidae (Lecanoromycetes). Fungal Diversity 73, 239–258.CrossRefGoogle Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Schmitt, I, Messuti, MI, Feige, GB and Lumbsch, HT (2001) Molecular data support rejection of the generic concept in the Coccotremataceae (Ascomycota). Lichenologist 33, 315–321.CrossRefGoogle Scholar
Schmitt, I, Lumbsch, HT and Søchting, U (2003 a) Phylogeny of the lichen genus Placopsis and its allies based on Bayesian analyses of nuclear and mitochondrial sequences. Mycologia 95, 827–835.CrossRefGoogle ScholarPubMed
Schmitt, I, Martin, MP, Türk, R and Lumbsch, HT (2003 b) Phylogenetic position of the genera Melanaria, Varicellaria and Thamnochrolechia (Pertusariales). Bibliotheca Lichenologica 86, 147–154.Google Scholar
Schmitt, I, Mueller, G and Lumbsch, HT (2005) Ascoma morphology is homoplaseous and phylogenetically misleading in some pyrenocarpous lichens. Mycologia 97, 362–374.CrossRefGoogle ScholarPubMed
Schmitt, I, Yamamoto, Y and Lumbsch, HT (2006) Phylogeny of Pertusariales (Ascomycotina): resurrection of Ochrolechiaceae and new circumscription of Megasporaceae. Journal of the Hattori Botanical Laboratory 100, 753–764.Google Scholar
Schmitt, I, del Prado, R, Grube, M and Lumbsch, HT (2009) Repeated evolution of closed fruiting bodies is linked to ascoma development in the largest group of lichenized fungi (Lecanoromycetes, Ascomycota). Molecular Phylogenetics and Evolution 52, 34–44.CrossRefGoogle Scholar
Schmitt, I, Fankhauser, JD, Sweeney, K, Spribille, T, Kalb, K and Lumbsch, HT (2010) Gyalectoid Pertusaria species form a sister-clade to Coccotrema (Ostropomycetidae, Ascomycota) and comprise the new lichen genus Gyalectaria. Mycology 1, 75–83.CrossRefGoogle Scholar
Spribille, T and Muggia, L (2013) Expanded taxon sampling disentangles evolutionary relationships and reveals a new family in Peltigerales (Lecanoromycetidae, Ascomycota). Fungal Diversity 58, 171–184.CrossRefGoogle Scholar
Staiger, B, Kalb, K and Grube, M (2006) Phylogeny and phenotypic variation in the lichen family Graphidaceae (Ostropomycetidae, Ascomycota). Mycological Research 110, 765–772.CrossRefGoogle Scholar
Stamatakis, A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.CrossRefGoogle ScholarPubMed
Wedin, M, Wiklund, E, Crewe, A, Döring, H, Ekman, S, Nyberg, Å, Schmitt, I and Lumbsch, HT (2005) Phylogenetic relationships of Lecanoromycetes (Ascomycota) as revealed by analyses of mtSSU and nLSU rDNA sequence data. Mycological Research 109, 159–172.CrossRefGoogle ScholarPubMed
Wedin, M, Wiklund, E, Jørgensen, PM and Ekman, S (2009) Slippery when wet: phylogeny and character evolution in the gelatinous cyanobacterial lichens (Peltigerales, Ascomycetes). Molecular Phylogenetics and Evolution 53, 862–871.CrossRefGoogle Scholar
Wiklund, E and Wedin, M (2003) The phylogenetic relationships of the cyanobacterial lichens in the Lecanorales suborder Peltigerineae. Cladistics 19, 419–431.CrossRefGoogle Scholar
Zhang, J, Kapli, P, Pavlidis, P and Stamatakis, A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.CrossRefGoogle ScholarPubMed