Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-28T11:23:22.428Z Has data issue: false hasContentIssue false

Multi-locus phylogeny of Bryoria reveals recent diversification and unexpected diversity in section Divaricatae

Published online by Cambridge University Press:  28 November 2023

Leena Myllys*
Affiliation:
Botanical Museum, Finnish Museum of Natural History, FI-00014 University of Helsinki, Finland
Raquel Pino-Bodas
Affiliation:
Area of Biodiversity and Conservation, Rey Juan Carlos University, 28933 Móstoles, Madrid, Spain
Saara Velmala
Affiliation:
Botanical Museum, Finnish Museum of Natural History, FI-00014 University of Helsinki, Finland
Li-Song Wang
Affiliation:
Kunming Institute of Botany, Chinese Academy of Science, Heilongtan, Kunming, Yunnan, 650204, China
Trevor Goward
Affiliation:
UBC Herbarium, Beaty Museum, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
*
Corresponding author: Leena Myllys; Email: leena.myllys@helsinki.fi

Abstract

In recent years, the genus Bryoria (Parmeliaceae, Lecanoromycetes) has been the subject of considerable phylogenetic scrutiny. Here we used information on six gene regions, three nuclear protein-coding markers (Mcm7, GAPDH and Tsr1), two nuclear ribosomal markers (ITS and IGS) and a partial mitochondrial small subunit (mtSSU), to examine infrageneric relationships in the genus and to assess species delimitation in the Bryoria bicolor/B. tenuis group in section Divaricatae. For this purpose, phylogenetic analyses and several of the available algorithms for species delimitation (ASAP, GMYC single, GMYC multiple and bPTP) were employed. We also estimated divergence times for the genus using *BEAST. Our phylogenetic analyses based on the combined data set of six gene loci support the monophyly of sections Americanae, Divaricatae and Implexae, while section Bryoria is polyphyletic and groups in two clades. Species from Bryoria clade 1 are placed in an emended section Americanae. Our study reveals that section Divaricatae is young (c. 5 My) and is undergoing diversification, especially in South-East Asia and western North America. Separate phylogenetic analyses of section Divaricatae using ITS produced a topology congruent with the current species concepts. However, the remaining gene regions produced poorly resolved phylogenetic trees and the different species delimitation methods also generated highly inconsistent results, congruent with other studies that highlight the difficulty of species delimitation in groups with recent and rapid radiation. Based on our results, we describe the new species B. ahtiana sp. nov., characterized by its bicolorous, caespitose, widely divergent thallus, conspicuously thickening main stems, well-developed secondary branches, and rather sparse third-order branchlets. Another new lineage, referred to here as B. tenuis s. lat., is restricted to western North America and may represent a new species recently diverged from B. tenuis s. str., though further work is needed.

Type
Standard Paper
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of the British Lichen Society

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

Ahrens, D, Fujisawa, T, Krammer, HJ, Eberle, J, Fabrizi, S and Vogler, AP (2016) Rarity and incomplete sampling in DNA-based species delimitation. Systematic Biology 65, 478494.Google Scholar
Ahti, T (2007) Further studies on the Cladonia verticillata group (Lecanorales) in East Asia and western North America. Bibliotheca Lichenologica 96, 519.Google Scholar
Ahti, T and Henssen, A (1965) New localities for Cavernularia hultenii in eastern and western North America. Bryologist 68, 8589.CrossRefGoogle Scholar
Amo de Paz, G, Cubas, P, Divakar, PK, Lumbsch, HT and Crespo, A (2011) Origin and diversification of major clades in parmelioid lichens (Parmeliaceae, Ascomycota) during the Paleogene inferred by Bayesian analysis. PLoS ONE 6, e28161.Google Scholar
Asher, OA, Howieson, J and Lendemer, JC (2023) A new perspective on the macrolichen genus Platismatia (Parmeliaceae, Ascomycota) based on molecular and phenotypic data. Bryologist 126, 118.Google Scholar
Boluda, CG, Divakar, PK, Hawksworth, DL, Villagra, J and Rico, VJ (2015) Molecular studies reveal a new species of Bryoria in Chile. Lichenologist 47, 387394.CrossRefGoogle Scholar
Boluda, CG, Rico, VJ, Divakar, PK, Nadyeina, O, Myllys, L, McMullin, RT, Zamora, JC, Scheidegger, C and Hawksworth, DL (2019) Evaluating methodologies for species delimitation: the mismatch between phenotypes and genotypes in lichenized fungi (Bryoria sect. Implexae, Parmeliaceae). Persoonia 42, 75100.CrossRefGoogle ScholarPubMed
Brodo, IM and Ahti, T (1996) Lichens and lichenicolous fungi of the Queen Charlotte Islands, British Columbia, Canada. 2. The Cladoniaceae. Canadian Journal of Botany 74, 11471180.CrossRefGoogle Scholar
Brodo, IM and Hawksworth, DL (1977) Alectoria and allied genera in North America. Opera Botanica 42, 1164.Google Scholar
Bystrek, J (1969) Die Gattung Alectoria. Lichenes, Usneaceae (Flechten des Himalaya 5). Khumbu Himal 6, 1724.Google Scholar
Carstens, BC, Pelletier, TA, Reid, NM and Satler, JD (2013) How to fail at species delimitation. Molecular Ecology 22, 43694383.Google Scholar
Dayrat, B (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407417.Google Scholar
Divakar, PK, Crespo, A, Wedin, M, Leavitt, S, Hawksworth, D, Myllys, L, McCune, B, Randlane, T, Bjerke, JW, Ohmura, Y, et al. (2015) Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi. New Phytologist 208, 12171226.Google Scholar
Divakar, PK, Crespo, A, Kraichak, E, Leavitt, SD, Singh, G, Schmitt, I and Lumbsch, HT (2017) Using a temporal phylogenetic method to harmonize family- and genus-level classification in the largest clade of lichen-forming fungi. Fungal Diversity 84, 101117.Google Scholar
Drummond, AJ, Suchard, MA, Xie, D and Rambaut, A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 19691973.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.Google Scholar
Fontaine, KM, Ahti, T and Piercey-Normore, MD (2010) Convergent evolution in Cladonia gracilis and allies. Lichenologist 42, 116.Google Scholar
Fujisawa, T and Barraclough, TG (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62, 707724.Google Scholar
Gardes, M and Bruns, TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2, 113118.Google Scholar
Gargas, A and Taylor, JW (1992) Polymerase chain reaction (PCR) primers for amplifying and sequencing nuclear 18S rDNA from lichenized fungi. Mycologia 84, 589592.Google Scholar
Goloboff, PA, Farris, JS and Nixon, KC (2008) TNT, a free program for phylogenetic analysis. Cladistics 24, 774786.Google Scholar
Goward, T and Ahti, T (1983) Parmelia hygrophila, a new lichen species from the Pacific Northwest of North America. Bryologist 20, 913.Google Scholar
Goward, T and Ahti, T (1997) Notes on the distributional ecology of the Cladoniaceae (lichenized Ascomycetes) in temperate and boreal western North America. Journal of the Hattori Botanical Laboratory 82, 143155.Google Scholar
Goward, T, Gauslaa, Y, Björk, CR, Woods, D and Wright, KG (2022) Stand openness predicts hair lichen (Bryoria) abundance in the lower canopy, with implications for the conservation of Canada's critically imperiled Deep-Snow Mountain Caribou (Rangifer tarandus caribou). Forest Ecology and Management 520, 120416.Google Scholar
Graur, D and Martin, W (2004) Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends in Genetics 20, 8086.Google Scholar
Grewe, F, Huang, JP, Leavitt, SD and Lumbsch, HT (2017) Reference-based RADseq resolves robust relationships among closely related species of lichen-forming fungi using metagenomic DNA. Scientific Reports 7, 111.Google Scholar
Grewe, F, Lagostina, E, Wu, H, Printzen, C and Lumbsch, HT (2018) Population genomic analyses of RAD sequences resolves the phylogenetic relationship of the lichen-forming fungal species Usnea antarctica and Usnea aurantiacoatra. MycoKeys 43, 61113.Google Scholar
Hawksworth, DL and Coppins, BJ (2003) Bryoria tenuis (Parmeliaceae) new to the British Isles, and either awaiting rediscovery or extinct. Lichenologist 35, 361364.Google Scholar
Heled, J and Drummond, AJ (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570580.Google Scholar
Hofmann, EP, Nicholson, KE, Luque-Montes, IR, Köhler, G, Cerrato-Mendoza, CA, Medina-Flores, M, Wilson, LD and Townsend, JH (2019) Cryptic diversity, but to what extent? Discordance between single-locus species delimitation methods within mainland anoles (Squamata: Dactyloidae) of northern Central America. Frontiers in Genetics 10, 11.Google Scholar
Jørgensen, PM (1972) Further studies in Alectoria sect. Divaricatae DR. Svensk Botanisk Tidskrift 66, 191201.Google Scholar
Jørgensen, PM (1975) Further notes on Asian Alectoria. Bryologist 78, 7780.Google Scholar
Jørgensen, PM and Ryvarden, L (1970) Contribution to the lichen flora of Norway. Årbok for Universitetet I Bergen, Matematisk-Naturvidenskapelig Serie 1969 10, 124.Google Scholar
Jørgensen, PM and Tønsberg, T (2010) The lichen Bryoria bicolor found fertile in western Norway. Graphis Scripta 22, 5253.Google Scholar
Jørgensen, PM, Myllys, L, Velmala, S and Wang, LS (2012) Bryoria rigida, a new Asian lichen species from the Himalayan region. Lichenologist 44, 777781.Google Scholar
Jorna, J, Linde, JB, Searle, PC, Jackson, AC, Nielsen, M-E, Nate, MS, Saxton, NA, Grewe, F, Herrera-Campos, MA, Spjut, RW, et al. (2021) Species boundaries in the messy middle – a genome-scale validation of species delimitation in a recently diverged lineage of coastal fog desert lichen fungi. Ecology and Evolution 11, 1861518632.Google Scholar
Keuler, R, Jensen, J, Barcena-Peña, A, Grewe, F, Lumbsch, HT, Huang, JP and Leavitt, SD (2022) Interpreting phylogenetic conflict: hybridization in the most speciose genus of lichen-forming fungi. Molecular Phylogenetics and Evolution 174, 107543.Google Scholar
Kotelko, R and Piercey-Normore, MD (2010) Cladonia pyxidata and C. pocillum; genetic evidence to regard them as conspecific. Mycologia 102, 534545.CrossRefGoogle Scholar
Kraichak, E, Divakar, PK, Crespo, A, Leavitt, SD, Nelsen, MP, Lücking, R and Lumbsch, HT (2015) A tale of two hyper-diversities: diversification dynamics of the two largest families of lichenized fungi. Scientific Reports 5, 10028.Google Scholar
Kurokawa, S and Kashiwadani, H (2006) Checklist of Japanese Lichens and Allied Fungi. Tokyo: National Science Museum.Google Scholar
Leavitt, SD, Johnson, L and St Clair, LL (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, 175188.Google Scholar
Leavitt, SD, Esslinger, TL, Divakar, PK and Lumbsch, HT (2012) Miocene and Pliocene dominated diversification of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota) and Pleistocene population expansions. BMC Evolutionary Biology 12, 118.Google Scholar
Leavitt, SD, Esslinger, TL, Divakar, PK, Crespo, A and Lumbsch, HT (2016) Hidden diversity before our eyes: delimiting and describing cryptic lichen-forming fungal species in camouflage lichens (Parmeliaeceae, Ascomycota). Fungal Biology 120, 13741391.Google Scholar
Lohse, K (2009) Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology 58, 439442.Google Scholar
Lohtander, K, Myllys, L, Sundin, R, Källersjö, M and Tehler, A (1998) The species pair concept in the lichen Dendrographa leucophaea (Arthoniales): analyses based on ITS sequences. Bryologist 101, 404411.Google Scholar
Lohtander, K, Oksanen, I and Rikkinen, J (2002) A phylogenetic study of Nephroma (lichen-forming Ascomycota). Mycological Research 106, 777787.Google Scholar
Lücking, R, Nadel, MRA, Araujo, E and Gerlach, A (2020) Two decades of DNA barcoding in the genus Usnea (Parmeliaceae): how useful and reliable is the ITS? Plant and Fungal Systematics 65, 303357.Google Scholar
Lücking, R, Leavitt, SD and Hawksworth, DL (2021) Species in lichen-forming fungi: balancing between conceptual and practical considerations, and between phenotype and phylogenomics. Fungal Diversity 109, 99154.Google Scholar
Lumbsch, HT and Leavitt, SD (2011) Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity 50, 5972.Google Scholar
Lutsak, T, Fernández-Mendoza, F, Kirika, P, Wondafrash, M and Printzen, C (2020) Coalescence-based species delimitation using genome-wide data reveals hidden diversity in a cosmopolitan group of lichens. Organisms Diversity and Evolution 20, 189218.Google Scholar
Magoga, G, Fontaneto, D and Montagna, M (2021) Factors affecting the efficiency of molecular species delimitation in a species-rich insect family. Molecular Ecology Resources 21, 14751489.Google Scholar
Maharachchikumbura, SS, Chen, Y, Ariyawansa, HA, Hyde, KD, Haelewaters, D, Perera, RH, Samarakoon, MC, Wanasinghe, DN, Bustamante, DE, Liu, J-J, et al. (2021) Integrative approaches for species delimitation in Ascomycota. Fungal Diversity 109, 155179.Google Scholar
Mark, K, Saag, L, Leavitt, SD, Will-Wolf, S, Nelsen, MP, Tõrra, T, Saag, A, Randlane, T and Lumbsch, HT (2016) Evaluation of traditionally circumscribed species in the lichen-forming genus Usnea, section Usnea (Parmeliaceae, Ascomycota) using a six-locus dataset. Organisms Diversity and Evolution 16, 497524.Google Scholar
McCune, B, Arup, U, Breuss, O, Di Meglio, E, Di Meglio, J, Esslinger, TL, Miadlikowska, J, Miller, AE, Rosentreter, R, Schultz, M, et al. (2020) Biodiversity and ecology of lichens of Kenai Fjords National Park, Alaska. Plant and Fungal Systematics 65, 586619.Google Scholar
McMullin, RT, Lendemer, JC, Braid, HE and Newmaster, SG (2016) Molecular insights into the lichen genus Alectoria (Parmeliaceae) in North America. Botany 94, 165175.CrossRefGoogle Scholar
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. 18.Google Scholar
Myllys, L, Lohtander, K, Källersjö, M and 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.Google Scholar
Myllys, L, Stenroos, S and Thell, A (2002) New genes for phylogenetic studies of lichenized fungi: glyceraldehyde-3-phosphate dehydrogenase and beta-tubulin genes. Lichenologist 34, 237246.Google Scholar
Myllys, L, Velmala, S, Holien, H, Halonen, P, Wang, LS and Goward, T (2011) Phylogeny of the genus Bryoria. Lichenologist 45, 617638.CrossRefGoogle Scholar
Myllys, L, Velmala, S, Lindgren, H, Glavich, D, Carlberg, T, Wang, LS and Goward, T (2014) Taxonomic delimitation of the genera Bryoria and Sulcaria, with a new combination Sulcaria spiralifera introduced. Lichenologist 46, 737752.Google Scholar
Myllys, L, Velmala, S, Pino-Bodas, R and Goward, T (2016) New species in Bryoria (Parmeliaceae, Lecanoromycetes) from north-west North America. Lichenologist 48, 355365.Google Scholar
Orange, A, James, PW and White, FJ (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Padial, JM, Castroviejo-Fisher, S, Koehler, J, Vila, C, Chaparro, JC and De la Riva, I (2009) Deciphering the products of evolution at the species level: the need for an integrative taxonomy. Zoologica Scripta 38, 431447.Google Scholar
Paradis, E, Claude, J and Strimmer, K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289290.Google Scholar
Piercey-Normore, MD, Ahti, T and Goward, T (2010) Phylogenetic and haplotype analyses of four segregates within Cladonia arbuscula s.l. Botany 88, 397408.Google Scholar
Pino-Bodas, R, Burgaz, AR, Martín, MP and Lumbsch, HT (2011) Phenotypical plasticity and homoplasy complicate species delimitation in the Cladonia gracilis group (Cladoniaceae, Ascomycota). Organisms Diversity and Evolution 11, 343355.Google Scholar
Pino-Bodas, R, Burgaz, AR, Martín, MP, Ahti, T, Stenroos, S, Wedin, M and Lumbsch, HT (2015) The phenotypic features used for distinguishing species within the Cladonia furcata complex are highly homoplasious. Lichenologist 47, 287303.Google Scholar
Pino-Bodas, R, Burgaz, AR, Ahti, T and Stenroos, S (2018) Taxonomy of Cladonia angustiloba and related species. Lichenologist 50, 267282.Google 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, 595609.Google Scholar
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.Google Scholar
Printzen, C and Ekman, S (2002) Genetic variability and its geographical distribution in the widely disjunct Cavernularia hultenii. Lichenologist 34, 101111.Google Scholar
Puillandre, N, Brouillet, S and Achaz, G (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609620.Google Scholar
Rambaut, A and Drummond, AJ (2013) TreeAnnotator v. 1.7.0. Available as part of the BEAST package [WWW resource] URL http://beast.bio.ed.ac.uk.Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901904.Google Scholar
Randlane, T and Mark, K (2021) Response to Clerc & Naciri (2021) Usnea dasopoga (Ach.) Nyl. and U. barbata (L.) F. H. Wigg. (Ascomycetes, Parmeliaceae) are two different species: a plea for reliable identifications in molecular studies. Lichenologist 53, 231232.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.Google Scholar
Sanmartín, I, Enghoff, H and Ronquist, F (2001) Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biological Journal of the Linnean Society 73, 345390.Google Scholar
Schmitt, I, Crespo, A, Divakar, PK, Fankhauser, JD, Herman-Sackett, E, Kalb, K, Nelsen, MP, Nelson, NA, Rivas-Plata, E, Shimp, AD, et al. (2009) New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia 23, 3540.Google Scholar
Schoch, CL, Seifert, KA, Huhndorf, S, Robert, V, Spouge, JL, Levesque, CA, Chen, W and 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, 62416246.Google Scholar
Singh, KP, Singh, P and Sinha, GP (2018) Lichen diversity in the Eastern Himalaya biodiversity hotspot region, India. Cryptogam Biodiversity and Assessment Special Volume 2018, 71114.Google Scholar
Spribille, T, Tuovinen, V, Resl, P, Vanderpool, D, Wolinski, H, Aime, MC, Schneider, K, Tabentheiner, E, Toome-Heller, M, Thor, G, et al. (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353, 488492.Google Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 13121313.CrossRefGoogle ScholarPubMed
Sukumaran, J and Knowles, LL (2017) Multispecies coalescent delimits structure, not species. Proceedings of the National Academy of Sciences of the United States of America 114, 16071612.Google Scholar
Thell, A, Crespo, A, Divakar, PK, Kärnefelt, I, Leavitt, SD, Lumbsch, HT and Seaward, MRD (2012) A review of the family Parmeliaceae – history, phylogeny and current taxonomy. Nordic Journal of Botany 30, 641664.Google Scholar
Velmala, S, Myllys, L, Halonen, P, Goward, T and Ahti, T (2009) Molecular data show that Bryoria fremontii and B. tortuosa (Parmeliaceae) are conspecific. Lichenologist 41, 231242.Google Scholar
Velmala, S, Myllys, L, Goward, T, Holien, H and Halonen, P (2014) Taxonomy of Bryoria section Implexae (Parmeliaceae, Lecanorales) in North America and Europe, based on chemical, morphological and molecular data. Annales Botanici Fennici 51, 345371.Google Scholar
Wang, LS and Harada, H (2001) Taxonomic study of Bryoria asiatica-group (lichenized Ascomycota, Parmeliaceae) in Yunnan, southern China. Natural History Research 6, 4352.Google Scholar
Wang, LS, Wang, XY, Liu, D, Myllys, L, Shi, HX, Zhang, YY, Yang, MX and Li, LJ (2017) Four new species of Bryoria (lichenized Ascomycota: Parmeliaceae) from the Hengduan Mountains, China. Phytotaxa 297, 2941.Google Scholar
White, TJ, Bruns, TD, Lee, SB and Taylor, JW (1990) Amplification and direct sequencing of fungal ribosomal DNA genes for phylogenetics. In Innis, MA, Gelfand, DH, Sninsky, JJ and White, TJ (eds), PCR Protocols: a Guide to Methods and Applications. San Diego: Academic Press, pp. 315322.Google Scholar
Widhelm, TJ, Egan, RS, Bertoletti, FR, Asztalos, MJ, Kraichak, E, Leavitt, SD and Lumbsch, HT (2016) Picking holes in traditional species delimitations: an integrative taxonomic reassessment of the Parmotrema perforatum group (Parmeliaceae, Ascomycota). Botanical Journal of the Linnean Society 182, 868884.Google Scholar
Widhelm, TJ, Rao, A, Grewe, F and Lumbsch, HT (2023) High-throughput sequencing confirms the boundary between traditionally considered species pairs in a group of lichenized fungi (Peltigeraceae, Pseudocyphellaria). Botanical Journal of the Linnean Society 201, 471482.Google Scholar
Wiens, JJ (2006) Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics 39, 3442.Google Scholar
Will, KW, Mishler, BD and Wheeler, QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology 54, 844851.Google Scholar
Wirtz, N, Printzen, C and Lumbsch, HT (2008) The delimitation of Antarctic and bipolar species of neuropogonoid Usnea (Ascomycota, Lecanorales): a cohesion approach of species recognition for the Usnea perpusilla complex. Mycological Research 112, 472484.Google Scholar
Zachos, J, Pagani, M, Sloan, L, Thomas, E and Billups, K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686693.Google Scholar
Zhang, J, Kapli, P, Pavlidis, P and Stamatakis, A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 28692876.Google Scholar
Zhao, X, Fernández-Brime, S, Wedin, M, Locke, M, Leavitt, SD and Lumbsch, HT (2017) Using multi-locus sequence data for addressing species boundaries in commonly accepted lichen-forming fungal species. Organisms Diversity and Evolution 17, 351363.Google Scholar
Zoller, S, Scheidegger, C and Sperisen, C (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31, 511516.Google Scholar
Supplementary material: File

Myllys et al. supplementary material 1
Download undefined(File)
File 1.4 MB
Supplementary material: File

Myllys et al. supplementary material 2
Download undefined(File)
File 1.4 MB
Supplementary material: File

Myllys et al. supplementary material 3
Download undefined(File)
File 18.4 KB