Skip to main content
×
×
Home

Historical biogeography of the lichenized fungal genus Hypotrachyna (Parmeliaceae, Ascomycota): insights into the evolutionary history of a pantropical clade

  • Paloma CUBAS (a1), H. Thorsten LUMBSCH (a2), Ruth DEL PRADO (a1), Zuzana FERENCOVA (a1), Nestor L. HLADUN (a3), Victor J. RICO (a1) and Pradeep K. DIVAKAR (a1)...
Abstract

Hypotrachyna is a speciose genus of primarily tropical and oceanic lichen-forming fungi. It includes species with distinct distribution patterns, such as pantropical, restricted and disjunct species. We used a dataset of mitochondrial SSU, nuclear ITS and LSU ribosomal DNA from 89 specimens to study the historical biogeography of the genus. We employed Bayesian and maximum likelihood approaches for phylogenetic analyses, a likelihood-based approach to ancestral area estimation, and a Bayesian approach to estimate divergence times of major lineages within the genus based on molecular evolutionary rates for ITS and a secondary calibration point at the Hypotrachyna clade – Parmeliopsis split. Our analyses suggest that the genus might have originated in the Neotropics during the Eocene and that the split of major lineages happened primarily during the Eocene and Oligocene. The major diversification within those clades is estimated to have occurred during the Miocene. Pantropical species distributions are explained by long-distance dispersal. A number of currently accepted species were found to be non-monophyletic, illustrating that the delimitation of species in the genus needs attention.

Copyright
Corresponding author
(corresponding author): Email: pdivakar@farm.ucm.es
References
Hide All
Alors, D., Lumbsch, H. T., Divakar, P. K., Leavitt, S. D. & Crespo, A. (2016) An integrative approach for understanding diversity in the Punctelia rudecta species complex (Parmeliaceae, Ascomycota). PLoS ONE 11: e0146537.
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: e2816.
Amo de Paz, G., Crespo, A., Cubas, P., 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.
Coad, L., Burgess, N. D., Bomhard, B. & Besancon, C. (2009) Progress on the Convention on Biological Diversity’s 2010 and 2012 Targets for Protected Area Coverage. A technical report for the IUCN international workshop “Looking to the Future of the CBD Programme of Work on Protected Areas”, Jeju Island, Republic of Korea, 14-17 September 2009.
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 Jardín Botánico 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.
Crisci, J. V. (2001) The voice of historical biogeography. Journal of Biogeography 28: 157168.
Culberson, W. L. & Culberson, C. F. (1981) The genera Cetrariastrum and Concamerella (Parmeliaceae): a chemosynthetic synopsis. Bryologist 84: 273314.
Del-Prado, R., Divakar, P. K. & Crespo, A. (2011) Using genetic distances in addition to ITS molecular phylogeny to identify potential species in the Parmotrema reticulatum complex: a case study. Lichenologist 43: 569583.
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. & Crespo, A. (2015) Molecular phylogenetic and phylogenomic approaches in studies of lichen systematics and evolution. In Recent Advances in Lichenology (D. K. Upreti, P. K. Divakar, V. Shukla & R. Bajpai, eds): 4560. New Delhi: Springer.
Divakar, P. K. & Upreti, D. K. (2005) Parmelioid Lichens in India (A Revisionary Study). Dehra Dun: Bishen Singh Mahendra Pal Singh.
Divakar, P. K., Ferencova, Z., Del Prado, R., Lumbsch, H. T. & Crespo, A. (2010 a) Remototrachyna, a new tropical lineage in hypotrachynoid lichens (Parmeliaceae, Ascomycota): a multigene and morphological approach. American Journal of Botany 97: 579590.
Divakar, P. K., Figueras, G., Hladun, N. L. & Crespo, A. (2010 b) Molecular phylogenetic studies reveal an undescribed species within the North American concept of Melanelixia glabra (Parmeliaceae). Fungal Diversity 42: 4755.
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., Crespo, A., Núñez-Zapata, J., Flakus, A., Sipman, H. J. M., Elix, J. A. & Lumbsch, H. T. (2013) A molecular perspective on generic concepts in the Hypotrachyna clade (Parmeliaceae, Ascomycota). Phytotaxa 132: 2138.
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.
Divakar, P. K., Crespo, A., Kraichak, E., Leavitt, S. D., Singh, G., Schmitt, I. & Lumbsch, H. T. (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.
Donoghue, M. J. & Moore, B. R. (2003) Toward an integrative historical biogeography. Integrative and Comparative Biology 43: 261270.
Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 19691973.
Elix, J. A. (1994) Hypotrachyna . Flora of Australia 55: 4959.
Ferencova, Z. (2012) Estudio morfológico comparado de los caracters generativos en relación con linajes monofileticos de la Familia Parmeliaceae (Lecanorales, Ascomycota). Ph.D. thesis, Universidad Complutense.
Geml, J., Kauff, F., Brochmann, C. & Taylor, D. L. (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.
Hale, M. E. (1975) A revision of lichen genus Hypotrachyna (Parmeliaceae) in tropical America. Smithsonian Contributions to Botany 25: 173.
Hawksworth, D. L. (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological Research 105: 14221432.
Hawksworth, D. L. (2012) Global species numbers of fungi: are tropical studies and molecular approaches contributing to a more robust estimate? Biodiversity and Conservation 21: 24252433.
Hodkinson, B. P. & Lendemer, J. C. (2011) Molecular analyses reveal semi-cryptic species in Xanthoparmelia tasmanica . Bibliotheca Lichenologica 106: 108119.
Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., Sanmartin, I., Sanchez-Meseguer, A., Anderson, C. L., Figueiredo, J. P., et al. (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927931.
Jaklitsch, W. M., Baral, H. O., Lücking, R. & Lumbsch, H. T. (2016) Ascomycota. In Syllabus of Plant Families - Adolf Engler’s Syllabus der Pflanzenfamilien (W. Frey, ed.): 1150. Stuttgart: Gebrüder Borntraeger Verlagsbuchhandlung.
Jaramillo, C., Rueda, M. J. & Mora, G. (2006) Cenozoic plant diversity in the Neotropics. Science 311: 18931896.
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. Brief Bioinformatics 9: 286298.
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: e10028.
Lanfear, R., Calcott, B., Ho, S. Y. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29: 16951701.
Leavitt, S. D., Esslinger, T. L., Divakar, P. K. & Lumbsch, H. T. (2012 a) Miocene and Pliocene dominated diversification of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota) and Pleistocene population expansions. BMC Evolutionary Biology 12: 176.
Leavitt, S. D., Esslinger, T. L., Divakar, P. K. & Lumbsch, H. T. (2012 b) Miocene divergence, phenotypically cryptic lineages, and contrasting distribution patterns in common lichen-forming fungi (Ascomycota: Parmeliaceae). Biological Journal of the Linnean Society 107: 920937.
Leavitt, S. D., Esslinger, T. L. & Lumbsch, H. T. (2012 c) Neogene-dominated diversification in neotropical montane lichens: dating divergence events in the lichen-forming fungal genus Oropogon (Parmeliaceae). American Journal of Botany 99: 17641777.
Leavitt, S. D., Esslinger, T. L., Spribille, T., Divakar, P. K. & Lumbsch, H. T. (2013) Multilocus phylogeny of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota): insights on diversity, distributions, and a comparison of species tree and concatenated topologies. Molecular Phylogenetics and Evolution 66: 138152.
Leavitt, S. D., Divakar, P. K., Ohmura, Y., Wang, L.-S., Esslinger, T. L. & Lumbsch, H. T. (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.
Lücking, R. (2003) Takhtajan’s floristic regions and foliicolous lichen biogeography: a compatibility analysis. Lichenologist 35: 3354.
Lücking, R., Papong, K., Thammathaworn, A. & Boonpragob, K. (2008) Historical biogeography and phenotype-phylogeny of Chroodiscus (lichenized Ascomycota: Ostropales: Graphidaceae). Journal of Biogeography 35: 23112327.
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. (2016) Diversification of lichen-forming fungi. In Encyclopedia of Evolutionary Biology (R. M. Kliman, ed.): 305311. Oxford: Academic Press.
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. & Rikkinen, J. (2017) Evolution of lichens. In The Fungal Community: its Organization and Role in the Ecosystem (J. Dighton & J. F. White, eds): 5362. Boca Raton, Florida: CRC Press.
Matzke, N. J. (2014) BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis in R scripts. http://cran.rproject. org/package=BioGeoBEARS.
Mittelbach, G. G., Schemske, D. W., Cornell, H. V., Allen, A. P., Brown, J. M., Bush, M. B., Harrison, S. P., Hurlbert, A. H., Knowlton, N., Lessios, H. A., et al. (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters 10: 315331.
Molina, M. C., Del-Prado, R., Divakar, P. K., Sánchez-Mata, D. & Crespo, A. (2011 a) Another example of cryptic diversity in lichen-forming fungi: the new species Parmelia mayi (Ascomycota: Parmeliaceae). Organisms Diversity and Evolution 11: 331342.
Molina, M. C., Divakar, P. K., Millanes, A. M., Sánchez, E., Del-Prado, R., Hawksworth, D. L. & Crespo, A. (2011 b) Parmelia sulcata (Ascomycota: Parmeliaceae), a sympatric monophyletic species complex. Lichenologist 43: 585601.
Nuñez-Zapata, J., Divakar, P. K., Del-Prado, R., Cubas, P., Hawksworth, D. L. & Crespo, A. (2011) Conundrums in species concepts: the discovery of a new cryptic species segregated from Parmelina tiliacea (Ascomycota: Parmeliaceae). Lichenologist 43: 603616.
Núñez-Zapata, J., Alors, D., Cubas, P., Divakar, P. K., Leavitt, S. D., Lumbsch, H. T. & Crespo, A. (2017) Understanding disjunct distribution patterns in lichen-forming fungi: insights from Parmelina (Parmeliaceae, Ascomycota). Botanical Journal of the Linnean Society 184: 238253.
Nylander, J. A., Olsson, U., Alstrom, P. & Sanmartin, I. (2008) Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves: Turdus). Systematic Biology 57: 257268.
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.
Pennington, R. T., Lavin, M., Prado, D. E., Pendry, C. A., Pell, S. K. & Butterworth, C. A. (2004) Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philosophical Transactions of the Royal Society B-Biological Sciences 359: 515537.
Rambaut, A. (2009) FigTree 1.2.2. Institute of Evolutionary Biology, University of Edinburgh. Available at: http://tree.bio.ed.ac.uk/software/figtree
Rambaut, A., Suchard, M., Xie, D. & Drummond, A. (2014) Tracer v1.6. Available at: http://beast.bio.ed.ac.uk/Tracer.
Ree, R. H. & Sanmartin, I. (2009) Prospects and challenges for parametric models in historical biogeographical inference. Journal of Biogeography 36: 12111220.
Ree, R. H. & Smith, S. A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57: 414.
Ree, R. H., Moore, B. R., Webb, C. O. & Donoghue, M. J. (2005) A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution 59: 22992311.
Ronquist, F. & Sanmartin, I. (2011) Phylogenetic methods in biogeography. Annual Review of Ecology, Evolution, and Systematics 42: 441464.
Sanmartin, I. & Ronquist, F. (2004) Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology 53: 216243.
Sanmartin, I., Van der Mark, P. & Ronquist, F. (2008) Inferring dispersal: a Bayesian approach to phylogeny-based island biogeography, with special reference to the Canary Islands. Journal of Biogeography 35: 428449.
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.
Sipman, H. J. M., Elix, J. A. & Nash, T. H. III (2009) Hypotrachyna (Parmeliaceae, lichenized fungi). Flora Neotropica 104: 1176.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 13121313.
Takhtajan, A. L., Crovello, T. J. & Cronquist, A. (1986) Floristic Regions of the World. Berkeley: University of California Press.
Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564577.
Taylor, T. N., Krings, M. & Taylor, E. L. (2015) Fossil Fungi. London: Academic Press.
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.
van der Hammen, T. & Hooghiemstra, H. (2000) Neogene and Quaternary history of vegetation, climate, and plant diversity in Amazonia. Quaternary Science Reviews 19: 725742.
Werth, S. (2011) Biogeography and phylogeography of lichen fungi and their photobionts. In Biogeography of Microscopic Organisms: Is Everything Small Everywhere? (D. Fontaneto, ed.): 191208. Cambridge: Cambridge University Press.
Wiens, J. J. & Donoghue, M. J. (2004) Historical biogeography, ecology and species richness. Trends in Ecology and Evolution 19: 639644.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

The Lichenologist
  • ISSN: 0024-2829
  • EISSN: 1096-1135
  • URL: /core/journals/lichenologist
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
WORD
Supplementary materials

Cubas et al. supplementary material
Cubas et al. supplementary material 2

 Word (18 KB)
18 KB
PDF
Supplementary materials

Cubas et al. supplementary material
Cubas et al. supplementary material 1

 PDF (214 KB)
214 KB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed