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Assessing phylogeny and historical biogeography of the largest genus of lichen-forming fungi, Xanthoparmelia (Parmeliaceae, Ascomycota)

  • Steven D. LEAVITT (a1), Paul M. KIRIKA (a2), Guillermo AMO DE PAZ (a3), Jen-Pan HUANG (a4), Jae-Seoun HUR (a5), John A. ELIX (a6), Felix GREWE (a4), Pradeep K. DIVAKAR (a7) and H. Thorsten LUMBSCH (a4)...


Species richness is not evenly distributed across the tree of life and a limited number of lineages comprise an extraordinarily large number of species. In lichen-forming fungi, only two genera are known to be ‘ultradiverse’ (>500 species), with the most diverse genus, Xanthoparmelia, consisting of c. 820 species. While Australia and South Africa are known as current centres of diversity for Xanthoparmelia, it is not well known when and where this massive diversity arose. To better understand the geographical and temporal context of diversification in this diverse genus, we sampled 191 Xanthoparmelia specimens representing c. 124 species/species-level lineages from populations worldwide. From these specimens, we generated a multi-locus sequence data set using Sanger and high-throughput sequencing to reconstruct evolutionary relationships in Xanthoparmelia, estimate divergence times and reconstruct biogeographical histories in a maximum likelihood and Bayesian framework. This study corroborated the phylogenetic placement of several morphologically or chemically diverse taxa within Xanthoparmelia, such as Almbornia, Chondropsis, Karoowia, Namakwa, Neofuscelia, Omphalodiella, Paraparmelia, Placoparmelia and Xanthomaculina, in addition to improved phylogenetic resolution and reconstruction of previously unsampled lineages within Xanthoparmelia. Our data indicate that Xanthoparmelia most likely originated in Africa during the early Miocene, coinciding with global aridification and development of open habitats. Reconstructed biogeographical histories of Xanthoparmelia reveal diversification restricted to continents with infrequent intercontinental exchange by long-distance dispersal. While likely mechanisms by which Xanthoparmelia obtained strikingly high levels of species richness in Australia and South Africa remain uncertain, this study provides a framework for ongoing research into diverse lineages of lichen-forming fungi. Finally, our study highlights a novel approach for generating locus-specific molecular sequence data sets from high throughput metagenomic reads.



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Amo de Paz, G., Lumbsch, H. T., Cubas, P., Elix, J. A. & Crespo, A. (2010 a) The genus Karoowia (Parmeliaceae, Ascomycota) includes unrelated clades nested within Xanthoparmelia . Australian Systematic Botany 23: 173184.
Amo de Paz, G., Lumbsch, H. T., Cubas, P., Elix, J. A. & Crespo, A. (2010 b) The morphologically deviating genera Omphalodiella and Placoparmelia belong to Xanthoparmelia (Parmeliaceae). Bryologist 113: 376386.
Amo de Paz, G., Cubas, P., Divakar, P. K., Lumbsch, H. T. & 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.
Amo de Paz, G., Cubas, P., Crespo, A., Elix, J. A. & Lumbsch, H. T. (2012) Transoceanic dispersal and subsequent diversification on separate continents shaped diversity of the Xanthoparmelia pulla group (Ascomycota). PLoS ONE 7: e39683.
Benton, M. J. & Emerson, B. C. (2007) How did life become so diverse? The dynamics of diversification according to the fossil record and molecular phylogenetics. Palaeontology 50: 2340.
Blanco, O., Crespo, A., Elix, J. A., Hawksworth, D. L. & Lumbsch, H. T. (2004) A molecular phylogeny and a new classification of parmelioid lichens containing Xanthoparmelia-type lichenan (Ascomycota: Lecanorales). Taxon 53: 959975.
Bowker, M. A., Miller, M. E., Belnap, J., Sisk, T. D. & Johnson, N. C. (2008) Prioritizing conservation effort through the use of biological soil crusts as ecosystem function indicators in an arid region. Conservation Biology 22: 15331543.
Büdel, B., Colesie, C., Green, T. G. A., Grube, M., Lázaro Suau, R., Loewen-Schneider, K., Maier, S., Peer, T., Pintado, A., Raggio, J., et al. (2014) Improved appreciation of the functioning and importance of biological soil crusts in Europe: the Soil Crust International Project (SCIN). Biodiversity and Conservation 23: 16391658.
Byrne, M., Yeates, D. K., Joseph, L., Kearney, M., Bowler, J., Williams, M. A. J., Cooper, S., Donnellan, S. C., Keogh, J. S., Leys, R., et al. (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17: 43984417.
Claramunt, S., Derryberry, E. P., Remsen, J. & Brumfield, R. T. (2012) High dispersal ability inhibits speciation in a continental radiation of passerine birds. Proceedings of the Royal Society of London B: Biological Sciences 279: 15671574.
Crespo, A. & Lumbsch, H. T. (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1: 167170.
Crespo, A. & Pérez-Ortega, S. (2009) Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenies and morphological characters. Anales del Jardin Botanico de Madrid 66: 7181.
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: 17351753.
Crisp, M., Cook, L. & Steane, D. (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philosophical Transactions of the Royal Society of London B: Biological Sciences 359: 15511571.
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.
Del-Prado, R., Blanco, O., Lumbsch, H. T., Divakar, P. K., Elix, J. A., Molina, M. C. & Crespo, A. (2013) Molecular phylogeny and historical biogeography of the lichen-forming fungal genus Flavoparmelia (Ascomycota: Parmeliaceae). Taxon 62: 928939.
Divakar, P. K., Del-Prado, R., Lumbsch, H. T., Wedin, M., Esslinger, T. L., Leavitt, S. D. & Crespo, A. (2012) Diversification of the newly recognized lichen-forming fungal lineage Montanelia (Parmeliaceae, Ascomycota) and its relation to key geological and climatic events. American Journal of Botany 99: 20142026.
Divakar, P. K., Kauff, F., Crespo, A., Leavitt, S. D. & Lumbsch, H. T. (2013) Understanding phenotypical character evolution in parmelioid lichenized fungi (Parmeliaceae, Ascomycota). PLoS ONE 8: e83115.
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: 12171226.
Drummond, A. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
Drummond, A., Ho, S., Phillips, M. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4: e88.
Elix, J. A. (1994) Xanthoparmelia . In Flora of Australia. Volume 55 Lichens-Lecanorales 2, Parmeliaceae (C. Grgurinovic, ed.): 201308. Canberra: Australian Biological Resources Study.
Elix, J. A. (2001) A revision of the lichen genus Paraparmelia Elix & J. Johnst. Bibliotheca Lichenologica 80: 1224.
Elix, J. A. (2003) The lichen genus Paraparmelia, a synonym of Xanthoparmelia (Ascomycota, Parmeliaceae). Mycotaxon 97: 395403.
Esslinger, T. L. (1977) A chemosystematic revision of the brown Parmeliae . Journal of the Hattori Botanical Laboratory 42: 1211.
Flowers, B. P. & Kennett, J. P. (1994) The middle Miocene transition: East Antarctic ice sheet development, deep ocean circulation and global carbon cycling. Palaeogeography, Palaeoclimatology, Palaeoecology 108: 537555.
Grewe, F., Huang, J. P., Leavitt, S. D. & Lumbsch, H. T. (2017) Reference-based RADseq resolves robust relationships among closely related species of lichen-forming fungi using metagenomic DNA. Scientific Reports 7: 9884.
Griffin, P. C. & Hoffmann, A. A. (2014) Limited genetic divergence among Australian alpine Poa tussock grasses coupled with regional structuring points to ongoing gene flow and taxonomic challenges. Annals of Botany 113: 953965.
Gyelnik, V. (1931) Additamenta ad cognitionem Parmeliarum - II. Feddes Repertorium Specierum Novarum Regni Vegetabilis 29: 273291.
Hale, M. E. (1990) A synopsis of the lichen genus Xanthoparmelia (Vainio) Hale (Ascomycotina, Parmeliaceae). Smithsonian Contributions to Botany 74: 1250.
Heled, J. & Drummond, A. J. (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27: 570580.
Hodkinson, B. P. & Lendemer, J. C. (2011) Molecular analyses reveal semi-cryptic species in Xanthoparmelia tasmanica . Bibliotheca Lichenologica 106: 108119.
Jaklitsch, W., Baral, H-O, Lücking, R., Lumbsch, H. T. & Frey, W (2016) Syllabus of Plant Families-Adolf Engler’s Syllabus der Pflanzenfamilien, Part 1/2. Stuttgart: Borntraeger Verlagsbuchhandlung.
Jetz, W., Thomas, G., Joy, J., Hartmann, K. & Mooers, A. (2012) The global diversity of birds in space and time. Nature 491: 444448.
Kaasalainen, U., Heinrichs, J., Krings, M., Myllys, L., Grabenhorst, H., Rikkinen, J. & Schmidt, A. R. (2015) Alectorioid morphologies in Paleogene lichens: new evidence and re-evaluation of the fossil Alectoria succini Mägdefrau. PLoS ONE 10: e0129526.
Kaasalainen, U., Schmidt, A. R. & Rikkinen, J. (2017) Diversity and ecological adaptations in Palaeogene lichens. Nature Plants 3: 17049.
Katoh, K. & Toh, H. (2008) Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9: 286298.
Katoh, K., Kuma, K-i., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33: 511518.
Kraichak, E., Divakar, P. K., Crespo, A., Leavitt, S. D., Nelsen, M. P., Lücking, R. & Lumbsch, H. T. (2015) A tale of two hyper-diversities: diversification dynamics of the two largest families of lichenized fungi. Scientific Reports 5: 10028.
Leavitt, S. D., Johnson, L. A. & St. Clair, L. L. (2011 a) 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.
Leavitt, S. D., Johnson, L. A., Goward, T. & St. Clair, L. L. (2011 b) 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.
Leavitt, S. D., Lumbsch, H. T., Stenroos, S. & St. Clair, L. L. (2013) Pleistocene speciation in North American lichenized fungi and the impact of alternative species circumscriptions and rates of molecular evolution on divergence estimates. PLoS ONE 8: e85240.
Leavitt, S. D., Kraichak, E., Nelsen, M. P., Altermann, S., Divakar, P. K., Alors, D., Esslinger, T. L., Crespo, A. & Lumbsch, H. T. (2015) Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). Molecular Ecology 24: 37793797.
Leavitt, S. D., Divakar, P. K., Crespo, A. & Lumbsch, H. T. (2016 a) A matter of time – understanding the limits of the power of molecular data for delimiting species boundaries. Herzogia 29: 479492.
Leavitt, S. D., Grewe, F., Widhelm, T., Muggia, L., Wray, B. & Lumbsch, H. T. (2016 b) Resolving evolutionary relationships in lichen-forming fungi using diverse phylogenomic datasets and analytical approaches. Scientific Reports 6: 22262.
Lindblom, L. & Ekman, S. (2006) Genetic variation and population differentiation in the lichen-forming ascomycete Xanthoria parietina on the island Storfosna, central Norway. Molecular Ecology 15: 5451559.
Lücking, R., Hodkinson, B. P. & Leavitt, S. D. (2016) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – approaching one thousand genera. Bryologist 119: 361416.
Lumbsch, H. T. & Leavitt, S. D. (2011) Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity 50: 5972.
Lumbsch, H. T., Hipp, A., Divakar, P. K., Blanco, O. & Crespo, A. (2008) Accelerated evolutionary rates in tropical and oceanic parmelioid lichens (Ascomycota). BMC Evolutionary Biology 8: e257.
Magallón, S. & Castillo, A. (2009) Angiosperm diversification through time. American Journal of Botany 96: 349365.
Matzke, N. J. (2014) Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Systematic Biology 63: 951970.
McPeek, M. A. & Brown, J. M. (2007) Clade age and not diversification rate explains species richness among animal taxa. American Naturalist 169: E97E106.
Molina, M. C., Divakar, P. K., Goward, T., Millanes, A. M., Lumbsch, H. T. & Crespo, A. (2017) Neogene diversification in the temperate lichen-forming fungal genus Parmelia (Parmeliaceae, Ascomycota). Systematics and Biodiversity 15: 166181.
Nash, T. H. III (2016) Xanthoparmelia in Mexico. Bibliotheca Lichenologica 110: 621692.
Nash, T. H. III, Gries, C. & Elix, J. A. (1995) A revision of the lichen genus Xanthoparmelia in South America. Bibliotheca Lichenologica 56: 1157.
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.
Otálora, M. A. G., Martínez, I., Aragón, G. & Molina, M. C. (2010) Phylogeography and divergence date estimates of a lichen species complex with a disjunct distribution pattern. American Journal of Botany 97: 216223.
Papadopoulou, A. & Knowles, L. L. (2016) Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses. Proceedings of the National Academy of Sciences of the United States of America 113: 80188024.
Paradis, E., Claude, J. & Strimmer, K. (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20: 289290.
Parnmen, S., Rangsiruji, A., Mongkolsuk, P., Boonpragob, K., Nutakki, A. & Lumbsch, H. T. (2012) Using phylogenetic and coalescent methods to understand the species diversity in the Cladia aggregata complex (Ascomycota, Lecanorales). PLoS ONE 7: e52245.
Parnmen, S., Leavitt, S. D., Rangsiruji, A. & Lumbsch, H. T. (2013) Identification of species in the Cladia aggregata group using DNA barcoding (Ascomycota: Lecanorales). Phytotaxa 115: 114.
Rabosky, D. L., Donnellan, S. C., Talaba, A. L. & Lovette, I. J. (2007) Exceptional among-lineage variation in diversification rates during the radiation of Australia’s most diverse vertebrate clade. Proceedings of the Royal Society of London B: Biological Sciences 274: 29152923.
Rabosky, D. L., Donnellan, S. C., Grundler, M. & Lovette, I. J. (2014) Analysis and visualization of complex macroevolutionary dynamics: an example from Australian scincid lizards. Systematic Biology 63: 610627.
Rambaut, A. & Drummond, A. J. (2003) Tracer v.1.6.0. Available at:
Rambaut, A. & Drummond, A. J. (2009) TreeAnnotator v1.6.1. Available at: http://beastbioedacuk/TreeAnnotator.
Rambaut, A. & Drummond, A. J. (2013) LogCombiner v.1.8.0. Available at: http://beastbioedacuk/TreeAnnotator.
Ree, R. H. & Smith, S. A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57: 414.
Roelants, K., Gower, D. J., Wilkinson, M., Loader, S. P., Biju, S. D., Guillaume, K., Moriau, L. & Bossuyt, F. (2007) Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences of the United States of America 104: 887892.
Schmitt, I., Crespo, A., Divakar, P. K., Fankhauser, J. D., Herman-Sackett, E., Kalb, K., Nelsen, M. P., Rivas-Plata, E., Shimp, A. D., Widhelm, T., et al. (2009) New primers for promising single-copy genes in fungal phylogenies and systematics. Persoonia 23: 3540.
Sepulchre, P., Ramstein, G., Fluteau, F., Schuster, M., Tiercelin, J.-J. & Brunet, M. (2006) Tectonic uplift and Eastern Africa aridification. Science 313: 14191423.
Sérusiaux, E., VillarrealA., J. C. A., J. C., Wheeler, T. & Goffinet, B. (2011) Recent origin, active speciation and dispersal for the lichen genus Nephroma (Peltigerales) in Macaronesia. Journal of Biogeography 38: 11381151.
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31: 32103212.
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 26882690.
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758771.
Susoy, V. & Herrmann, M. (2014) Preferential host switching and codivergence shaped radiation of bark beetle symbionts, nematodes of Micoletzkya (Nematoda: Diplogastridae). Journal of Evolutionary Biology 27: 889898.
Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564577.
Thell, A., Feuerer, T., Elix, J. A. & Kärnefelt, I. (2006) A contribution to the phylogeny and taxonomy of Xanthoparmelia (Ascomycota, Parmeliaceae). Journal of the Hattori Botanical Laboratory 100: 797807.
Thell, A., Crespo, A., Divakar, P. K., Kärnefelt, I., Leavitt, S. D., Lumbsch, H. T. & Seaward, M. R. D. (2012) A review of the lichen family Parmeliaceae – history, phylogeny and current taxonomy. Nordic Journal of Botany 30: 641664.
Tolley, K. A., Chase, B. M. & Forest, F. (2008) Speciation and radiations track climate transitions since the Miocene Climatic Optimum: a case study of southern African chameleons. Journal of Biogeography 35: 14021414.


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