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Phylogenetic insight into the Lecidea atrobrunnea complex – evidence of narrow geographic endemics and the pressing need for integrative taxonomic revisions

Published online by Cambridge University Press:  22 September 2023

Nopparat Anantaprayoon
Affiliation:
Department of Botany, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
Jason Hollinger
Affiliation:
Herbarium, Western Carolina University, Cullowhee, North Carolina, USA
Abigail Robison
Affiliation:
Department of Biology, Brigham Young University, Provo, UT 84602, USA
Ekaphan Kraichak
Affiliation:
Department of Botany, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
Heather Root
Affiliation:
Botany and Plant Ecology Department, Weber State University, Ogden, UT 84408, USA
Steven D. Leavitt*
Affiliation:
M. L. Bean Life Science Museum and Department of Biology, Brigham Young University, Provo, UT 84602, USA
*
Corresponding author: Steven D. Leavitt; Email: steve_leavitt@byu.edu

Abstract

Species of lichen-forming fungi (LFF) display an array of geographical distribution patterns. Among the broadly distributed lichen-forming fungal species, the degree of reproductive isolation and genetic substructure among populations varies widely, in some cases masking unrecognized diversity or meaningful biogeographical patterns. Lecidea atrobrunnea (Raymond ex Lam. & DC.) Schaer. s. lat. (Lecideaceae) is a widespread species complex that has been studied for over two centuries since its initial description. The diversity of the L. atrobrunnea group is highest in western North America, where a dizzying array of morphologies and chemistry can occur at local scales. Here we investigate whether the assumed cosmopolitan distribution of L. atrobrunnea s. lat. is an artifact of taxonomic limitations and masks biogeographical patterns in this species complex. To address these questions, we compiled sequence data from the standard fungal barcoding marker (ITS) for over 100 specimens within this complex, in addition to genome-scale data from a subset of these representing over 1600 single-copy nuclear genes spanning over 3 Mb of the genome. Our study corroborates the perspective that the morphologically and chemically variable Lecidea atrobrunnea group reflects a complex of distinct species-level lineages, with 42–83 candidate species inferred from the ITS region and high levels of diversity inferred from a subset of specimens using genome-scale data. However, both phenotype- and molecular-based species boundaries remained unsettled, with the most common nominal taxa recovered as highly polyphyletic and with conflict among different molecular species delimitation approaches. Our study also highlights the potential for geographically restricted species, with fascinating biogeographical patterns, challenging, in part, the assumed cosmopolitan distribution of L. atrobrunnea s. lat. This study provides valuable direction for future research that will be crucial in understanding diversification and establishing a robust taxonomy for this well-known species complex.

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

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References

Allen, JL, McKenzie, SK, Sleith, RS and Alter, SE (2018) First genome-wide analysis of the endangered, endemic lichen Cetradonia linearis reveals isolation by distance and strong population structure. American Journal of Botany 105, 15561567.Google Scholar
Allen, JL, McMullin, RT, Wiersma, YF and Scheidegger, C (2021) Population genetics and biogeography of the lungwort lichen in North America support distinct Eastern and Western gene pools. American Journal of Botany 108, 24162424.Google Scholar
Bailey, RH and James, PW (1979) Birds and the dispersal of lichen propagules. Lichenologist 11, 105106.Google Scholar
Bankevich, A, Nurk, S, Antipov, D, Gurevich, AA, Dvorkin, M, Kulikov, AS, Lesin, VM, Nikolenko, SI, Pham, S, Prjibelski, AD, et al. (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19, 455477.Google 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.Google Scholar
Carstens, BC, Pelletier, TA, Reid, NM and Satler, JD (2013) How to fail at species delimitation. Molecular Ecology 22, 43694383.Google Scholar
Culberson, WL (1972) Disjunctive distributions in the lichen-forming fungi. Annals of the Missouri Botanical Garden 59, 165173.Google Scholar
de Lamarck, JB and de Candolle, AP (1805) Flore Française, 3rd Edn, Vol. 2. Paris: H. Agasse.Google Scholar
Divakar, PK, Wei, X-L, McCune, B, Cubas, P, Boluda, CG, Leavitt, SD, Crespo, A, Tchabanenko, S and Lumbsch, HT (2019) Parallel Miocene dispersal events explain the cosmopolitan distribution of the Hypogymnioid lichens. Journal of Biogeography 46, 945955.Google Scholar
Dupuis, JR, Roe, AD and Sperling, FAH (2012) Multi-locus species delimitation in closely related animals and fungi: one marker is not enough. Molecular Ecology 21, 44224436.Google Scholar
Fehrer, J, Slavíková-Bayerová, Š and Orange, A (2008) Large genetic divergence of new, morphologically similar species of sterile lichens from Europe (Lepraria, Stereocaulaceae, Ascomycota): concordance of DNA sequence data with secondary metabolites. Cladistics 24, 443458.Google Scholar
Fernández-Mendoza, F and Printzen, C (2013) Pleistocene expansion of the bipolar lichen Cetraria aculeata into the Southern Hemisphere. Molecular Ecology 22, 19611983.Google Scholar
Fernández-Mendoza, F, Domaschke, S, García, MA, Jordan, P, Martin, MP and Printzen, C (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Molecular Ecology 20, 12081232.Google Scholar
Fujita, MK, Leaché, AD, Burbrink, FT, McGuire, JA and Moritz, C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology and Evolution 9, 480488.Google Scholar
Garrido-Benavent, I, de los Ríos, A, Fernández-Mendoza, F and Pérez-Ortega, S (2018) No need for stepping stones: direct, joint dispersal of the lichen-forming fungus Mastodia tessellata (Ascomycota) and its photobiont explains their bipolar distribution. Journal of Biogeography 45, 213224.Google Scholar
Geml, J, Kauff, F, Brochmann, C and Taylor, DL (2010) Surviving climate changes: high genetic diversity and transoceanic gene flow in two arctic-alpine lichens, Flavocetraria cucullata and F. nivalis (Parmeliaceae, Ascomycota). Journal of Biogeography 37, 15291542.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, 91113.Google Scholar
Grube, M, Baloch, E and Arup, U (2004) A phylogenetic study of the Lecanora rupicola group (Lecanoraceae, Ascomycota). Mycological Research 108, 506514.Google Scholar
Guttová, A, Fačkovcová, Z, Martellos, S, Paoli, L, Munzi, S, Pittao, E and Ongaro, S (2019) Ecological specialization of lichen congeners with a strong link to Mediterranean-type climate: a case study of the genus Solenopsora in the Apennine Peninsula. Lichenologist 51, 7588.Google Scholar
Hale, E, Fisher, ML, Keuler, R, Smith, B and Leavitt, SD (2019) A biogeographic connection between Antarctica and montane regions of western North America highlights the need for further study of lecideoid lichens. Bryologist 122, 315324.Google Scholar
Herre, AW (1911) The desert lichens of Reno, Nevada. Botanical Gazette 51, 286297.Google Scholar
Hertel, H and Printzen, C (2004) Lecidea. In Nash, TH, III, Ryan, BD, Diederich, P, Gries, C and Bungartz, F (eds), Lichen Flora of the Greater Sonoran Desert Region, Vol. 2. Tempe, Arizona: Lichens Unlimited, Arizona State University, pp. 287309.Google Scholar
Johnson, MG, Gardner, EM, Liu, Y, Medina, R, Goffinet, B, Shaw, AJ, Zerega, NJC and Wickett, NJ (2016) HybPiper: extracting coding sequence and introns for phylogenetics from high-throughput sequencing reads using target enrichment. Applications in Plant Sciences 4, 1600016.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
Katoh, K and Toh, H (2008) Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9, 286298.Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, et al. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.Google Scholar
Keuler, R, Jensen, J, Barcena-Peña, A, Grewe, F, Lumbsch, HT, Huang, J-P 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
Kück, P and Longo, GC (2014) FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies. Frontiers in Zoology 11, 81.Google Scholar
LaGreca, S, Lumbsch, HT, Kukwa, M, Wei, X, Han, JE, Moon, KH, Kashiwadani, H, Aptroot, A and Leavitt, SD (2020) A molecular phylogenetic evaluation of the Ramalina siliquosa complex, with notes on species circumscription and relationships within Ramalina. Lichenologist 52, 197211.Google Scholar
Leavitt, SD, Johnson, LA, Goward, T and St. Clair, LL (2011) Species delimitation in taxonomically difficult lichen-forming fungi: an example from morphologically and chemically diverse Xanthoparmelia (Parmeliaceae) in North America. Molecular Phylogenetics and Evolution 60, 317332.Google Scholar
Leavitt, SD, Fernández-Mendoza, F, Pérez-Ortega, S, Sohrabi, M, Divakar, PK, Vondrák, J, Lumbsch, HT and St. Clair, LL (2013) Local representation of global diversity in a cosmopolitan lichen-forming fungal species complex (Rhizoplaca, Ascomycota). Journal of Biogeography 40, 17921806.Google Scholar
Leavitt, SD, Divakar, PK, Ohmura, Y, Wang, L-S, Esslinger, TL and Lumbsch, HT (2015) Who's getting around? Assessing species diversity and phylogeography in the widely distributed lichen-forming fungal genus Montanelia (Parmeliaceae, Ascomycota). Molecular Phylogenetics and Evolution 90, 8596.Google Scholar
Leavitt, SD, Westberg, M, Nelsen, MP, Elix, JA, Timdal, E, Sohrabi, M, St. Clair, LL, Williams, L, Wedin, M and Lumbsch, HT (2018) Multiple, distinct intercontinental lineages but isolation of Australian populations in a cosmopolitan lichen-forming fungal taxon, Psora decipiens (Psoraceae, Ascomycota). Frontiers in Microbiology 9, 283.Google Scholar
Leuckert, C and Hertel, H (2003) On the Lecidea atrobrunnea complex (Lecanorales, Lecideaceae) in the Americas I. Introduction and chemistry. Bibliotheca Lichenologica 86, 1331.Google Scholar
Lindblom, L and Søchting, U (2008) Taxonomic revision of Xanthomendoza borealis and Xanthoria mawsonii (Lecanoromycetes, Ascomycota). Lichenologist 40, 399409.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, 1109111096.Google Scholar
Lücking, R, Aime, MC, Robbertse, B, Miller, AN, Ariyawansa, HA, Aoki, T, Cardinali, G, Crous, PW, Druzhinina, IS, Geiser, DM, et al. (2020) Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus 11, 14.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
Magain, N, Tniong, C, Goward, T, Niu, D, Goffinet, B, Sérusiaux, E, Vitikainen, O, Lutzoni, F and Miadlikowska, J (2018) Species delimitation at a global scale reveals high species richness with complex biogeography and patterns of symbiont association in Peltigera section Peltigera (lichenized Ascomycota: Lecanoromycetes). Taxon 67, 836870.Google Scholar
Mamut, R, Jiamahat, A and Abbas, A (2022) Lecidea glacierensis (Lecideaceae), a new lichen species from China revealed by morphology and molecular phylogenetics. Lichenologist 54, 363369.Google Scholar
Manni, M, Berkeley, MR, Seppey, M, Simão, FA and Zdobnov, EM (2021) BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Molecular Biology and Evolution 38, 46474654.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, 128.Google Scholar
McCune, B (2017) Microlichens of the Pacific Northwest. Corvallis, Oregon: Wild Blueberry Media.Google Scholar
McCune, B, Curtis, MJ and Di, Meglio J (2017) New taxa and a case of ephemeral spore production in Lecideaceae from western North America. Bryologist 120, 115124.Google Scholar
Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A and Lanfear, R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 15301534.Google Scholar
Mirarab, S and Warnow, T (2015) ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44i52.Google Scholar
Moncada, B, Mercado-Dízz, JA and Lücking, R (2018) The identity of Sticta damicornis (Ascomycota: Lobariaceae): a presumably widespread taxon is a Caribbean endemic. Lichenologist 50, 591597.Google Scholar
Moncada, B, Mercado-Díaz, JA, Magain, N, Hodkinson, BP, Smith, CW, Bungartz, F, Pérez-Pérez, R-E, Gumboski, E, Sérusiaux, E, Lumbsch, HT, et al. (2021) Phylogenetic diversity of two geographically overlapping lichens: isolation by distance, environment, or fragmentation? Journal of Biogeography 48, 676689.Google Scholar
Onuţ-Brännström, I, Tibell, L and Johannesson, H (2017) A worldwide phylogeography of the whiteworm lichens Thamnolia reveals three lineages with distinct habitats and evolutionary histories. Ecology and Evolution 7, 36023615.Google Scholar
Orange, A, James, PW and White, FJ (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Otálora, MAG, Martínez, I, Aragón, G and Molina, MC (2010) Phylogeography and divergence date estimates of a lichen species complex with a disjunct distribution pattern. American Journal of Botany 97, 216223.Google Scholar
Paradis, E, Claude, J and Strimmer, K (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20, 289290.Google Scholar
Park, CH, Jeong, G and Hong, SG (2012) Possible multiple introductions of Cladonia borealis to King George Island. Antarctic Science 24, 359366.Google Scholar
Pentinsaari, M, Ratnasingham, S, Miller, SE and Hebert, PDN (2020) BOLD and GenBank revisited – do identification errors arise in the lab or in the sequence libraries? PLoS ONE 15, e0231814.Google Scholar
Piercey-Normore, MD (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytologist 169, 331344.Google Scholar
Pino-Bodas, R, Martín, MP, Burgaz, AR and Lumbsch, HT (2013) Species delimitation in Cladonia (Ascomycota): a challenge to the DNA barcoding philosophy. Molecular Ecology Resources 13, 10581068.Google Scholar
Printzen, C (2010) Lichen systematics: the role of morphological and molecular data to reconstruct phylogenetic relationships. Progress in Botany 71, 233275.Google Scholar
Printzen, C and Ekman, S (2003) Local population subdivision in the lichen Cladonia subcervicornis as revealed by mitochondrial cytochrome oxidase subunit 1 intron sequences. Mycologia 95, 399406.Google Scholar
Printzen, C, Domaschke, S, Fernández-Mendoza, F and Pérez-Ortega, S (2013) Biogeography and ecology of Cetraria aculeata, a widely distributed lichen with a bipolar distribution. MycoKeys 6, 3353.Google Scholar
Puillandre, N, Brouillet, S and Achaz, G (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609620.Google Scholar
R Development Core Team (2012) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. [WWW resource] URL https://www.R-project.orgGoogle Scholar
Rabiee, M and Mirarab, S (2021) SODA: multi-locus species delimitation using quartet frequencies. Bioinformatics 36, 56235631.Google Scholar
Rozewicki, J, Yamada, KD and Katoh, K (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20, 11601166.Google Scholar
Ruprecht, U, Fernández-Mendoza, F, Türk, R and Fryday, AM (2020) High levels of endemism and local differentiation in the fungal and algal symbionts of saxicolous lecideoid lichens along a latitudinal gradient in southern South America. Lichenologist 52, 287303.Google Scholar
Schmitt, I and Lumbsch, HT (2004) Molecular phylogeny of the Pertusariaceae supports secondary chemistry as an important systematic character set in lichen-forming ascomycetes. Molecular Phylogenetics and Evolution 33, 4355.Google Scholar
Schneider, K, Resl, P and Spribille, T (2016) Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event. Molecular Ecology 25, 34533468.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
Simão, FA, Waterhouse, RM, Ioannidis, P, Kriventseva, EV and Zdobnov, EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 32103212.Google Scholar
Simon, A, Goffinet, B, Magain, N and 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, 1528.Google Scholar
Singh, G, Dal Grande, F, Divakar, PK, Otte, J, Leavitt, SD, Szczepanska, K, Crespo, A, Rico, VJ, Aptroot, A, Cáceres, MES, et al. (2015) Coalescent-based species delimitation approach uncovers high cryptic diversity in the cosmopolitan lichen-forming fungal genus Protoparmelia (Lecanorales, Ascomycota). PLoS ONE 10, e0124625.Google Scholar
Spatafora, JW, Aime, MC, Grigoriev, IV, Martin, F, Stajich, JE and Blackwell, M (2017) The Fungal Tree of Life: from molecular systematics to genome-scale phylogenies. In Heitman, J, Howlett, BJ, Crous, PW, Stukenbrock, EH, James, TY and Gow, NAR (eds), The Fungal Kingdom. Hoboken, New Jersey: John Wiley and Sons, pp. 134.Google Scholar
Spjut, R, Simon, A, Guissard, M, Magain, N and Sérusiaux, E (2020) The fruticose genera in the Ramalinaceae (Ascomycota, Lecanoromycetes): their diversity and evolutionary history. MycoKeys 73, 168.Google Scholar
Talavera, G and Castresana, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564577.Google Scholar
Tonini, J, Moore, A, Stern, D, Shcheglovitova, M and Ortí, G (2015) Concatenation and species tree methods exhibit statistically indistinguishable accuracy under a range of simulated conditions. PLoS Currents 7, ecurrents.tol.34260cc27551a34527b34124ec34265f36334b34266be.Google Scholar
Walser, J-C, Holderegger, R, Gugerli, F, Hoebee, SE and Scheidegger, C (2005) Microsatellites reveal regional population differentiation and isolation in Lobaria pulmonaria, an epiphytic lichen. Molecular Ecology 14, 457467.Google Scholar
Weber, WA (2003) The Middle Asian Element in the Southern Rocky Mountain Flora of the western United States: a critical biogeographical review. Journal of Biogeography 30, 649685.Google Scholar
Werth, S (2011) Biogeography and phylogeography of lichen fungi and their photobionts. In Fontaneto, D (ed.), Biogeography of Microscopic Organisms: Is Everything Small Everywhere?, vol. London: Cambridge University Press, pp. 191208.Google Scholar
Werth, S, Meidl, P and Scheidegger, C (2021) Deep divergence between island populations in lichenized fungi. Scientific Reports 11, 7428.Google Scholar
Widhelm, TJ, Grewe, F, Huang, J-P, Mercado-Díaz, JA, Goffinet, B, Lücking, R, Moncada, B, Mason-Gamer, R and Lumbsch, HT (2019) Multiple historical processes obscure phylogenetic relationships in a taxonomically difficult group (Lobariaceae, Ascomycota). Scientific Reports 9, 8968.Google Scholar
Widhelm, TJ, Grewe, F, Huang, J-P, Ramanauskas, K, Mason-Gamer, R and Lumbsch, HT (2021) Using RADseq to understand the circum-Antarctic distribution of a lichenized fungus, Pseudocyphellaria glabra. Journal of Biogeography 48, 7890.Google Scholar
Williams, PH (2022) Guerrilla taxonomy and discriminating cryptic species – is quick also dirty? In Monro, AK and Mayo, SJ (eds), Cryptic Species: Morphological Stasis, Circumscription, and Hidden Diversity. Cambridge: Cambridge University Press, pp. 213241.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
Zhang, Y, Clancy, J, Jensen, J, McMullin, RT, Wang, L and Leavitt, SD (2022) Providing scale to a known taxonomic unknown – at least a 70-fold increase in species diversity in a cosmopolitan nominal taxon of lichen-forming fungi. Journal of Fungi 8, 490.Google Scholar
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