Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-19T20:46:07.390Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  08 May 2018

Paloma CUBAS ,
H. Thorsten LUMBSCH ,
Ruth DEL PRADO ,
Zuzana FERENCOVA ,
Nestor L. HLADUN ,
Victor J. RICO  and
Pradeep K. DIVAKAR
Paloma CUBAS
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid 28040, Spain.
H. Thorsten LUMBSCH
Affiliation:
Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA
Ruth DEL PRADO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid 28040, Spain.
Zuzana FERENCOVA
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid 28040, Spain.
Nestor L. HLADUN
Affiliation:
Departament de Biologia Vegetal (Botànica), Facultat de Biologia, Universitat de Barcelona, Diagonal 645, 08028 Barcelona, Spain
Victor J. RICO
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid 28040, Spain.
Pradeep K. DIVAKAR*
Affiliation:
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid 28040, Spain.
*
(corresponding author): Email: pdivakar@farm.ucm.es
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

ancestral areasdistributionNeotropicsparmelioid lichensphylogeny
Type
Articles
Information
The Lichenologist , Volume 50 , Issue 3 , May 2018 , pp. 283 - 298
Copyright
© British Lichen Society, 2018 

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

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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Crespo, A. & Lumbsch, H. T. (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1: 167–170.CrossRefGoogle ScholarPubMed
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: 71–81.Google Scholar
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: 1735–1753.Google Scholar
Crisci, J. V. (2001) The voice of historical biogeography. Journal of Biogeography 28: 157–168.CrossRefGoogle Scholar
Culberson, W. L. & Culberson, C. F. (1981) The genera Cetrariastrum and Concamerella (Parmeliaceae): a chemosynthetic synopsis. Bryologist 84: 273–314.CrossRefGoogle Scholar
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: 569–583.CrossRefGoogle Scholar
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: 928–939.CrossRefGoogle Scholar
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): 45–60. New Delhi: Springer.Google Scholar
Divakar, P. K. & Upreti, D. K. (2005) Parmelioid Lichens in India (A Revisionary Study). Dehra Dun: Bishen Singh Mahendra Pal Singh.Google Scholar
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: 579–590.Google Scholar
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: 47–55.CrossRefGoogle Scholar
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: 2014–2026.CrossRefGoogle ScholarPubMed
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: 21–38.Google Scholar
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: 1217–1226.Google Scholar
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: 101–117.Google Scholar
Donoghue, M. J. & Moore, B. R. (2003) Toward an integrative historical biogeography. Integrative and Comparative Biology 43: 261–270.Google Scholar
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: 1969–1973.Google Scholar
Elix, J. A. (1994) Hypotrachyna . Flora of Australia 55: 49–59.Google Scholar
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.Google Scholar
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: 1529–1542.Google Scholar
Hale, M. E. (1975) A revision of lichen genus Hypotrachyna (Parmeliaceae) in tropical America. Smithsonian Contributions to Botany 25: 1–73.CrossRefGoogle Scholar
Hawksworth, D. L. (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological Research 105: 1422–1432.Google Scholar
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: 2425–2433.Google Scholar
Hodkinson, B. P. & Lendemer, J. C. (2011) Molecular analyses reveal semi-cryptic species in Xanthoparmelia tasmanica . Bibliotheca Lichenologica 106: 108–119.Google Scholar
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: 927–931.Google Scholar
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.): 1–150. Stuttgart: Gebrüder Borntraeger Verlagsbuchhandlung.Google Scholar
Jaramillo, C., Rueda, M. J. & Mora, G. (2006) Cenozoic plant diversity in the Neotropics. Science 311: 1893–1896.Google Scholar
Kaasalainen, U., Schmidt, A. R. & Rikkinen, J. (2017) Diversity and ecological adaptations in Palaeogene lichens. Nature Plants 3: 17049.CrossRefGoogle ScholarPubMed
Katoh, K. & Toh, H. (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinformatics 9: 286–298.Google Scholar
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.Google Scholar
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: 1695–1701.Google Scholar
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.Google Scholar
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: 920–937.Google Scholar
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: 1764–1777.Google Scholar
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: 138–152.Google Scholar
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: 85–96.CrossRefGoogle ScholarPubMed
Lücking, R. (2003) Takhtajan’s floristic regions and foliicolous lichen biogeography: a compatibility analysis. Lichenologist 35: 33–54.Google Scholar
Lücking, R., Papong, K., Thammathaworn, A. & Boonpragob, K. (2008) Historical biogeography and phenotype-phylogeny of Chroodiscus (lichenized Ascomycota: Ostropales: Graphidaceae). Journal of Biogeography 35: 2311–2327.Google Scholar
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: 361–416.Google Scholar
Lumbsch, H. T. (2016) Diversification of lichen-forming fungi. In Encyclopedia of Evolutionary Biology (R. M. Kliman, ed.): 305–311. Oxford: Academic Press.Google Scholar
Lumbsch, H. T. & Leavitt, S. D. (2011) Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity 50: 59–72.Google Scholar
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): 53–62. Boca Raton, Florida: CRC Press.Google Scholar
Matzke, N. J. (2014) BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis in R scripts. http://cran.rproject. org/package=BioGeoBEARS.Google Scholar
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: 315–331.Google Scholar
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: 331–342.Google Scholar
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: 585–601.CrossRefGoogle Scholar
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: 603–616.Google Scholar
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: 238–253.Google Scholar
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: 257–268.Google Scholar
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: 216–223.Google Scholar
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: 515–537.Google Scholar
Rambaut, A. (2009) FigTree 1.2.2. Institute of Evolutionary Biology, University of Edinburgh. Available at: http://tree.bio.ed.ac.uk/software/figtree Google Scholar
Rambaut, A., Suchard, M., Xie, D. & Drummond, A. (2014) Tracer v1.6. Available at: http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Ree, R. H. & Sanmartin, I. (2009) Prospects and challenges for parametric models in historical biogeographical inference. Journal of Biogeography 36: 1211–1220.Google Scholar
Ree, R. H. & Smith, S. A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57: 4–14.CrossRefGoogle ScholarPubMed
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: 2299–2311.Google Scholar
Ronquist, F. & Sanmartin, I. (2011) Phylogenetic methods in biogeography. Annual Review of Ecology, Evolution, and Systematics 42: 441–464.Google Scholar
Sanmartin, I. & Ronquist, F. (2004) Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology 53: 216–243.Google Scholar
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: 428–449.Google Scholar
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: 1138–1151.Google Scholar
Sipman, H. J. M., Elix, J. A. & Nash, T. H. III (2009) Hypotrachyna (Parmeliaceae, lichenized fungi). Flora Neotropica 104: 1–176.Google Scholar
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.Google Scholar
Takhtajan, A. L., Crovello, T. J. & Cronquist, A. (1986) Floristic Regions of the World. Berkeley: University of California Press.Google Scholar
Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564–577.Google Scholar
Taylor, T. N., Krings, M. & Taylor, E. L. (2015) Fossil Fungi. London: Academic Press.Google Scholar
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: 641–664.CrossRefGoogle Scholar
van der Hammen, T. & Hooghiemstra, H. (2000) Neogene and Quaternary history of vegetation, climate, and plant diversity in Amazonia. Quaternary Science Reviews 19: 725–742.Google Scholar
Werth, S. (2011) Biogeography and phylogeography of lichen fungi and their photobionts. In Biogeography of Microscopic Organisms: Is Everything Small Everywhere? (D. Fontaneto, ed.): 191–208. Cambridge: Cambridge University Press.Google Scholar
Wiens, J. J. & Donoghue, M. J. (2004) Historical biogeography, ecology and species richness. Trends in Ecology and Evolution 19: 639–644.Google Scholar
Supplementary material: PDF

Cubas et al. supplementary material

Cubas et al. supplementary material 1

Download Cubas et al. supplementary material(PDF)
PDF 213.7 KB
Supplementary material: File

Cubas et al. supplementary material

Cubas et al. supplementary material 2

Download Cubas et al. supplementary material(File)
File 17.9 KB