[en] [en] PREMISE: Southern Africa is a biodiversity hotspot rich in endemic plants and lichen-forming fungi. However, species-level data about lichen photobionts in this region are minimal. We focused on Trebouxia (Chlorophyta), the most common lichen photobiont, to understand how southern African species fit into the global biodiversity of this genus and are distributed across biomes and mycobiont partners.
METHODS: We sequenced Trebouxia nuclear ribosomal ITS and rbcL of 139 lichen thalli from diverse biomes in South Africa and Namibia. Global Trebouxia phylogenies incorporating these new data were inferred with a maximum likelihood approach. Trebouxia biodiversity, biogeography, and mycobiont-photobiont associations were assessed in phylogenetic and ecological network frameworks.
RESULTS: An estimated 43 putative Trebouxia species were found across the region, including seven potentially endemic species. Only five clades represent formally described species: T. arboricola s.l. (A13), T. cf. cretacea (A01), T. incrustata (A06), T. lynniae (A39), and T. maresiae (A46). Potential endemic species were not significantly associated with the Greater Cape Floristic Region or desert. Trebouxia species occurred frequently across multiple biomes. Annual precipitation, but not precipitation seasonality, was significant in explaining variation in Trebouxia communities. Consistent with other studies of lichen photobionts, the Trebouxia-mycobiont network had an anti-nested structure.
CONCLUSIONS: Depending on the metric used, ca. 20-30% of global Trebouxia biodiversity occurs in southern Africa, including many species yet to be described. With a classification scheme for Trebouxia now well established, tree-based approaches are preferable over "barcode gap" methods for delimiting new species.
Medeiros, Ian D ; Department of Biology, Duke University, Durham, NC, USA
Ibáñez, Alicia ; Independent Researcher, Gamboa, Panama
Arnold, A Elizabeth ; School of Plant Sciences, Department of Ecology and Evolutionary Biology, and Bio5 Institute, University of Arizona, Tucson, AZ, USA
Hedderson, Terry A ; Bolus Herbarium, Department of Biological Sciences, University of Cape Town, Cape Town, South Africa
Miadlikowska, Jolanta ; Department of Biology, Duke University, Durham, NC, USA
Flakus, Adam ; W. Szafer Institute of Botany, Kraków, Poland
Carbone, Ignazio ; Center for Integrated Fungal Research, Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, USA
LaGreca, Scott ; Department of Biology, Duke University, Durham, NC, USA
Magain, Nicolas ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
Mazur, Edyta ; W. Szafer Institute of Botany, Kraków, Poland
Castillo, Reinaldo Vargas ; Universidad Metropolitana de Ciencias de la Educación, Santiago, Chile
Geml, József ; Eötvös Loránd Research Network, Eszterházy Károly Catholic University, Eger, Hungary
Kaup, Maya; Department of Biology, University of Mississippi, University, MS, USA
Maggs-Kölling, Gillian ; Gobabeb Namib Research Institute, Gobabeb, Namibia
Oita, Shuzo ; School of Plant Sciences, Department of Ecology and Evolutionary Biology, and Bio5 Institute, University of Arizona, Tucson, AZ, USA
Sathiya Seelan, Jaya Seelan ; Institute for Tropical Biology and Conservation (ITBC), Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia
Terlova, Elizaveta ; Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA
Hom, Erik F Y ; Department of Biology, University of Mississippi, University, MS, USA
Lewis, Louise A ; Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA
Lutzoni, François ; Department of Biology, Duke University, Durham, NC, USA
Eco-phylogenetic study of Trebouxia in southern Africa reveals interbiome connectivity and potential endemism in a green algal lichen photobiont.
Publication date :
December 2024
Journal title :
American Journal of Botany
ISSN :
0002-9122
eISSN :
1537-2197
Publisher :
John Wiley and Sons Inc, United States
Volume :
111
Issue :
12
Pages :
e16441
Peer reviewed :
Peer Reviewed verified by ORBi
Funding text :
Specimens were collected and exported under permits from South African National Parks (CRC/2019-2020/020-\u22122018/V1), Ezemvelo KZN Wildlife (OP 1404/2019), Mpumalanga Parks and Tourism Agency, CapeNature (CN35-31-9213 and export permit CN17-31-9607), and the Namibian Ministry of Environment and Tourism. We thank the Namibian National Botanical Research Institute (NBRI) and National Commission on Research, Science and Technology. We acknowledge the Sabah Biodiversity Center (SABC) and Sabah Parks for issuing collecting and export permits in Borneo [Access License JKM/MBS.1000-2/2 JLD.6 (101) and Transfer License JKM/MB.1000-2/3 JLD.3 (70)] and the Corporaci\u00F3n Nacional Forestal for issuing collecting and export permits in Chile (034/2016). Funding for this research was provided by the United States National Science Foundation (NSF) through the collaborative grant \u201CGoLife: Filling the largest void of the fungal genealogy of life (the Pezizomycotina) and integrating symbiotic, environmental and physiological data layers\u201D (DEB 1541548 to F.L. and J.M.; DEB 1541496 to A.E.A.; DEB 1541538 to E.F.Y.H.). I.D.M. was supported by an NSF Graduate Research Fellowship under grant DGE 1644868. The authors thank Carlos Pardo-De la Hoz, Shannon Skarha, Diego Garfias Gallegos, and Pierre-Luc Chagnon for feedback on an initial draft and thank Silke Werth and three anonymous reviewers for comments that improved the manuscript.Specimens were collected and exported under permits from South African National Parks (CRC/2019\u20102020/020\u2010\u22122018/V1), Ezemvelo KZN Wildlife (OP 1404/2019), Mpumalanga Parks and Tourism Agency, CapeNature (CN35\u201031\u20109213 and export permit CN17\u201031\u20109607), and the Namibian Ministry of Environment and Tourism. We thank the Namibian National Botanical Research Institute (NBRI) and National Commission on Research, Science and Technology. We acknowledge the Sabah Biodiversity Center (SABC) and Sabah Parks for issuing collecting and export permits in Borneo [Access License JKM/MBS.1000\u20102/2 JLD.6 (101) and Transfer License JKM/MB.1000\u20102/3 JLD.3 (70)] and the Corporaci\u00F3n Nacional Forestal for issuing collecting and export permits in Chile (034/2016). Funding for this research was provided by the United States National Science Foundation (NSF) through the collaborative grant \u201CGoLife: Filling the largest void of the fungal genealogy of life (the Pezizomycotina) and integrating symbiotic, environmental and physiological data layers\u201D (DEB 1541548 to F.L. and J.M.; DEB 1541496 to A.E.A.; DEB 1541538 to E.F.Y.H.). I.D.M. was supported by an NSF Graduate Research Fellowship under grant DGE 1644868. The authors thank Carlos Pardo\u2010De la Hoz, Shannon Skarha, Diego Garfias Gallegos, and Pierre\u2010Luc Chagnon for feedback on an initial draft and thank Silke Werth and three anonymous reviewers for comments that improved the manuscript.
Allaire, J., C. Gandrud, K. Russell, and C. Yetman. 2017. networkD3: D3 JavaScript Network Graphs from R. R package version 0.4. Website: https://CRAN.R-project.org/package=networkD3
Almborn, O. 1988. Some distribution patterns in the lichen flora of South Africa. Monographs in Systematic Botany from the Missouri Botanical Garden 25: 429–432.
Almborn, O. 1989. Revision of the lichen genus Teloschistes in central and southern Africa. Nordic Journal of Botany 8: 521–538.
Almeida-Neto, M., and W. Ulrich. 2011. A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling & Software 26: 173–178.
Baas Becking, L. G. M. 1934. Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, The Hague, Netherlands.
Barreno, E., L. Muggia, S. Chiva, A. Molins, C. Bordenave, F. García-Breijo, and P. Moya. 2022. Trebouxia lynnae sp. nov. (Former Trebouxia sp. TR9): Biology and biogeography of an epitome lichen symbiotic microalga. Biology 11: 1196.
Beck, A. 2002. Selektivität der symbionten schwermetalltoleranter flechten. Ph.D. thesis, Ludwig Maximilian University of Munich, Munich, Germany.
Beckett, S. J. 2016. Improved community detection in weighted bipartite networks. Royal Society Open Science 3: 140536.
Bengtsson-Palme, J., M. Ryberg, M. Hartmann, S. Branco, Z. Wang, A. Godhe, P. De Wit, et al. 2013. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods in Ecology and Evolution 4: 914–919.
Berger, S. A., D. Krompass, and A. Stamatakis. 2011. Performance, accuracy, and web server for evolutionary placement of short sequence reads under maximum likelihood. Systematic Biology 60: 291–302.
Botnen, S. S., M. L. Davey, R. Halvorsen, and H. Kauserud. 2018. Sequence clustering threshold has little effect on the recovery of microbial community structure. Molecular Ecology Resources 18: 1064–1076.
Bordenave, C. D., L. Muggia, S. Chiva, S. D. Leavitt, P. Carrasco, and E. Barreno. 2022. Chloroplast morphology and pyrenoid ultrastructural analyses reappraise the diversity of the lichen phycobiont genus Trebouxia (Chlorophyta). Algal Research 61: 102561.
Born, J., H. P. Linder, and P. Desmet. 2007. The Greater Cape Floristic Region. Journal of Biogeography 34: 147–162.
Buckley, H. L., A. Rafat, J. D. Ridden, R. H. Cruickshank, H. J. Ridgway, and A. M. Paterson. 2014. Phylogenetic congruence of lichenised fungi and algae is affected by spatial scale and taxonomic diversity. PeerJ 2: e573.
Câmara, P. E. A. S., F. A. C. Lopes, F. L. V. Bones, L. A. C. Rodrigues, M. Carvalho-Silva, M. Stech, P. Convey, and L. H. Rosa. 2023. Investigating aerial diversity of non-fungal eukaryotes across a 40° latitudinal transect using DNA metabarcoding. Austral Ecology 48: 1178–1194.
Candotto Carniel, F., D. Zanelli, S. Bertuzzi, and M. Tretiach. 2015. Desiccation tolerance and lichenization: a case study with the aeroterrestrial microalga Trebouxia sp. (Chlorophyta). Planta 242: 493–505.
Carbone, I., J. B. White, J. Miadlikowska, A. E. Arnold, M. A. Miller, F. Kauff, J. M. U'Ren, et al. 2017. T-BAS: Tree-Based Alignment Selector toolkit for phylogenetic-based placement, alignment downloads, and metadata visualization: an example with the Pezizomycotina tree of life. Bioinformatics 33: 1160–1168.
Carbone, I., J. B. White, J. Miadlikowska, A. E. Arnold, M. A. Miller, N. Magain, J. M. U'Ren, and F. Lutzoni. 2019. T-BAS version 2.1: Tree-Based Alignment Selector toolkit for evolutionary placement and viewing of alignments and metadata on curated and custom trees. Microbiology Resource Announcements 8: e00328-19.
Chagnon, P. L., N. Magain, J. Miadlikowska, and F. Lutzoni. 2018. Strong specificity and network modularity at a very fine phylogenetic scale in the lichen genus Peltigera. Oecologia 187: 767–782.
Chernomor, O., A. Von Haeseler, and B. Q. Minh. 2016. Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65: 997–1008.
Clark, V. R., J. E. Burrows, B. C. Turpin, K. Balkwill, M. Lötter, and S. J. Siebert. 2022. The Limpopo–Mpumalanga–Eswatini Escarpment—Extra-ordinary endemic plant richness and extinction risk in a summer rainfall montane region of Southern Africa. Frontiers in Ecology and Evolution 10: 765854.
Cowling, R. M., P. L. Bradshaw, J. F. Colville, and F. Forest. 2017. Levyns' Law: explaining the evolution of a remarkable longitudinal gradient in Cape plant diversity. Transactions of the Royal Society of South Africa 72: 184–201.
Cox, F., K. K. Newsham, and C. H. Robinson. 2019. Endemic and cosmopolitan fungal taxa exhibit differential abundances in total and active communities of Antarctic soils. Environmental Microbiology 21: 1586–1596.
Crous, P. W., I. H. Rong, A. Wood, S. Lee, H. Glen, W. Botha, B. Slippers, et al. 2006. How many species of fungi are there at the tip of Africa? Studies in Mycology 55: 13–33.
Csardi, G., and T. Nepusz. 2006. The igraph software package for complex network research. InterJournal, Complex Systems, 1695. Website: https://igraph.org
Culberson, C. F. 1972. Improved conditions and new data for the identification of lichen products by a standardized thin-layer chromatographic method. Journal of Chromatography 72: 113–125.
Culberson, C. F., and A. Johnson. 1982. Substitution of methyl tert-butyl ether for diethyl ether in the standardized thin-layer chromatographic method for lichen products. Journal of Chromatography 128: 253–259.
Culberson, C. F., and H. Kristinsson. 1970. A standardized method for the identification of lichen products. Journal of Chromatography 46: 85–93.
Dal Grande, F., G. Rolshausen, P. K. Divakar, A. Crespo, J. Otte, M. Schleuning, and I. Schmitt. 2018. Environment and host identity structure communities of green algal symbionts in lichens. New Phytologist 217: 277–289.
De Carolis, R., A. Cometto, P. Moya, E. Barreno, M. Grube, M. Tretiach, S. D. Leavitt, and L. Muggia. 2022. Photobiont diversity in lichen symbioses from extreme environments. Frontiers in Microbiology 13: 809804.
De Wever, A., F. Leliaert, E. Verleyen, P. Vanormelingen, K. Van der Gucht, D. A. Hodgson, K. Sabbe, and W. Vyverman. 2009. Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proceedings of the Royal Society, B, Biological Sciences 276: 3591–3599.
Díaz-Escandón, D., G. Tagirdzhanova, D. Vanderpool, C. C. Allen, A. Aptroot, O. Češka, D. L. Hawksworth, et al. 2022. Genome-level analyses resolve an ancient lineage of symbiotic ascomycetes. Current Biology 32: 5209–5218.
Dormann, C. F., J. Fruend, N. Bluethgen, and B. Gruber. 2009. Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecology Journal 2: 7–24.
Eichenberger, C., A. Aptroot, and R. Honegger. 2007. Three new Xanthoria species from South Africa: X. hirsuta, X. inflata and X. doidgeae. Lichenologist 39: 451–458.
Fick, S. E., and R. J. Hijmans. 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302–4315.
Flechtner, V. R., N. Pietrasiak, and L. A. Lewis. 2013. Newly revealed diversity of green microalgae from wilderness areas of Joshua Tree National Park (JTNP). Monographs of the Western North American Naturalist 6: 43–63.
Flessa, F., A. Kehl, M. Imtiaz, and M. Kohl. 2022. RFLPtools: Tools to analyse RFLP data. R package version 2.0. Website: https://r-forge.r-project.org/projects/rflptools/
Friedl, T. 1989. Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (lichenisierte Ascomyceten). Ph.D. dissertation, Universitat Bayreuth, Bayreuth, Germany.
Fryday, A. M. 2015. A new checklist of lichenised, lichenicolous and allied fungi reported from South Africa. Bothalia 45: 148.
Fryday, A. M., I. D. Medeiros, S. J. Siebert, N. Pope, and N. Rajakaruna. 2020. Burrowsia, a new genus of lichenized fungi (Caliciaceae), plus the new species B. cataractae and Scoliciosporum fabisporum, from Mpumalanga, South Africa. South African Journal of Botany 132: 471–481.
Fučíková, K., P. O. Lewis, and L. A. Lewis. 2014. Widespread desert affiliation of trebouxiophycean algae (Trebouxiophyceae, Chlorophyta) including discovery of three new desert genera. Phycological Research 62: 294–305.
Gardes, M., and T. D. Bruns. 1993. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118.
Garrido-Benavent, I., S. Chiva, C. D. Bordenave, A. Molins, and E. Barreno. 2022. Trebouxia maresiae sp. nov. (Trebouxiophyceae, Chlorophyta), a new lichenized species of microalga found in coastal environments. Cryptogamie, Algologie 43: 135–145.
Garrido-Benavent, I., M. R. Mora-Rodríguez, S. Chiva, S. Fos, and E. Barreno. 2023. Punctelia borreri and P. subrudecta (Parmeliaceae) associate with a partially overlapping pool of Trebouxia gelatinosa lineages. Lichenologist 55: 389–399.
Garrido-Benavent, I., S. Pérez-Ortega, A. de los Ríos, and F. Fernández-Mendoza. 2020. Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi). Symbiosis 82: 35–48.
Gasulla, F., A. Guéra, and E. Barreno. 2010. A simple and rapid method for isolating lichen photobionts. Symbiosis 51: 175–179.
Gibbs Russell, G. E. 1987. Preliminary floristic analysis of the major biomes in southern Africa. Bothalia 17: 213–227.
Goldblatt, P. 1978. An analysis of the flora of southern Africa: its characteristics, relationships, and origins. Annals of the Missouri Botanical Garden 65: 369–436.
González, A. M. M., B. Dalsgaard, and J. M. Olesen. 2010. Centrality measures and the importance of generalist species in pollination networks. Ecological Complexity 7: 36–43.
Hale, M. E. 1989. A monograph of the lichen genus Karoowia Hale (Ascomycotina: Parmeliaceae). Mycotaxon 35: 177–198.
Hale, M. E. 1990. A synopsis of the lichen genus Xanthoparmelia (Vainio) Hale (Ascomycotina, Parmeliaceae). Smithsonian Contributions to Botany 74: 1–250.
Helms, G. 2003. Taxonomy and symbiosis in associations of Physciaceae and Trebouxia. Ph.D. dissertation, Georg-August Universität Göttingen, Göttingen, Germany.
Hestmark, G., F. Lutzoni, and J. Miadlikowska. 2016. Photobiont associations in co-occurring umbilicate lichens with contrasting modes of reproduction in coastal Norway. Lichenologist 48: 545–557.
Hijmans, R. 2024. Terra: Spatial data analysis. R package version 1.7-78. Website: https://rspatial.github.io/terra/, https://rspatial.org/
Hilton-Taylor, C. 1996. Patterns and characteristics of the flora of the Succulent Karoo Biome, southern Africa. In The biodiversity of African plants: Proceedings XIVth AETFAT Congress, 1994, Wageningen, Netherlands, 58–72. Springer, Dordrecht, Netherlands.
Hoang, D. T., O. Chernomor, A. Von Haeseler, B. Q. Minh, and L. S. Vinh. 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522.
Hoveka, L. N., M. van Der Bank, B. S. Bezeng, and T. J. Davies. 2020. Identifying biodiversity knowledge gaps for conserving South Africa's endemic flora. Biodiversity and Conservation 29: 2803–2819.
Hughes, K.W., A. Case, P. B. Matheny, S. Kivlin, R. H. Petersen, A. N. Miller, and T. Iturriaga. 2020. Secret lifestyles of pyrophilous fungi in the genus Sphaerosporella. American Journal of Botany 107: 876–885.
Kalyaanamoorthy, S., B. Q. Minh, T. K. Wong, A. Von Haeseler, and L. S. Jermiin. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589.
Kärnefelt, I., S. Kondratyuk, U. Søchting, and P. Frödén. 2002. Xanthoria karrooensis and X. alexanderbaai (Teloschistaceae), two new lichen species from southern Africa. Lichenologist 34: 333–346.
Katoh, K., J. Rozewicki, and K. D. Yamada. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166.
Koch, N. M., J. C. Lendemer, E. A. Manzitto-Tripp, C. McCain, and D. E. Stanton. 2023. Carbon-concentrating mechanisms are a key trait in lichen ecology and distribution. Ecology 104: e4011.
Kosecka, M., M. Kukwa, A. Jabłońska, A. Flakus, P. Rodriguez-Flakus, Ł. Ptach, and B. Guzow-Krzemińska. 2022. Phylogeny and ecology of Trebouxia photobionts from Bolivian lichens. Frontiers in Microbiology 13: 779784.
Kroken, S., and J. W. Taylor. 2000. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103: 645–660.
Lange, O.L., E. Kilian, and H. Ziegler. 1986. Water vapor uptake and photosynthesis of lichens: performance differences in species with green and blue-green algae as photobionts. Oecologia 71: 104–110.
Lange, O. L., A. Meyer, H. Zellner, and U. Heber. 1994. Photosynthesis and water relations of lichen soil crusts: field measurements in the coastal fog zone of the Namib Desert. Functional Ecology 8: 253–264.
Lawrey, J. D. 1980. Sexual and asexual reproductive patterns in Parmotrema (Parmeliaceae) that correlate with latitude. Bryologist 83: 344–350.
Leavitt, S. D., E. Kraichak, M. P. Nelsen, S. Altermann, P. K. Divakar, D. Alors, T. L. Esslinger, et al. 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: 3779–3797.
Leavitt, S. D., P. M. Kirika, G. A. De Paz, J. P. Huang, J.-S. Hur, F. Grewe, P. K. Divakar, and H. T. Lumbsch. 2018. Assessing phylogeny and historical biogeography of the largest genus of lichen-forming fungi, Xanthoparmelia (Parmeliaceae, Ascomycota). Lichenologist 50: 299–312.
Lewis, L. A., and P. O. Lewis. 2005. Unearthing the molecular phylodiversity of desert soil green algae (Chlorophyta). Systematic Biology 54: 936–947.
Lopez, L. C. S., M. P. de Aguiar Fracasso, D. O. Mesquita, A. R. T. Palma, and P. Riul. 2012. The relationship between percentage of singletons and sampling effort: a new approach to reduce the bias of richness estimates. Ecological Indicators 14: 164–169.
Lutsak, T., F. Fernández-Mendoza, P. Kirika, M. Wondafrash, and C. Printzen. 2016. Mycobiont–photobiont interactions of the lichen Cetraria aculeata in high alpine regions of East Africa and South America. Symbiosis 68: 25–37.
Maddison, W. P., and D. R. Maddison. 2021. Mesquite: a modular system for evolutionary analysis, version 3.70. Website: http://www.mesquiteproject.org
Magain, N., J. Miadlikowska, B. Goffinet, E. Sérusiaux, and F. Lutzoni. 2017. Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Systematic Biology 66: 74–99.
Magain, N., C. Truong, T. Goward, D. Niu, B. Goffinet, E. Sérusiaux, O. Vitikainen, et al. 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: 836–870.
Maggs, G. L., P. Craven, and H. H. Kolberg. 1998. Plant species richness, endemism, and genetic resources in Namibia. Biodiversity & Conservation 7: 435–446.
Malavasi, V., P. Škaloud, F. Rindi, S. Tempesta, M. Paoletti, and M. Pasqualetti. 2016. DNA-based taxonomy in ecologically versatile microalgae: a re-evaluation of the species concept within the coccoid green algal genus Coccomyxa (Trebouxiophyceae, Chlorophyta). PLoS One 11: e0151137.
Maphangwa, K. W., C. F. Musil, L. Raitt, and L. Zedda. 2012. Experimental climate warming decreases photosynthetic efficiency of lichens in an arid South African ecosystem. Oecologia 169: 257–268.
Marini, L., J. Nascimbene, and P. L. Nimis. 2011. Large-scale patterns of epiphytic lichen species richness: photobiont-dependent response to climate and forest structure. Science of the Total Environment 409: 4381–4386.
Matzer, M., H. Mayrhofer, and G. Rambold. 1997. Diploicia africana comb. nov. (lichenized Ascomycetes, Physciaceae), an endemic species from the Cape Province (South Africa). Nordic Journal of Botany 17: 433–438.
Medeiros, I. D., and F. Lutzoni. 2022. Contribution to a modern treatment of Graphidaceae biodiversity in South Africa: genera of tribe Graphideae with hyaline ascospores. Lichenologist 54: 253–270.
Medeiros, I. D., E. Mazur, J. Miadlikowska, A. Flakus, P. Rodriguez-Flakus, C. J. Pardo-De la Hoz, E. Cieślak, et al. 2021. Turnover of lecanoroid mycobionts and their Trebouxia photobionts along an elevation gradient in Bolivia highlights the role of environment in structuring the lichen symbiosis. Frontiers in Microbiology 12: 774839.
Meigs, P. 1953. World distribution of arid and semi-arid homoclimates. In UNESCO [ed.], Reviews of research on arid zone hydrology, 203–210. UNESCO, Paris, France.
Meyer, C. P., and G. Paulay. 2005. DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3: e422.
Miadlikowska, J., F. Kauff, V. Hofstetter, E. Fraker, M. Grube, J. Hafellner, V. Reeb, et al. 2006. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA-and two protein-coding genes. Mycologia 98: 1088–1103.
Miller, M. A., W. Pfeiffer, and T. Schwartz. 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 2010, New Orleans, LA, USA, 1–8. https://doi.org/10.1109/GCE.2010.5676129
Moberg, R. 2004. Notes on foliose species of the lichen family Physciaceae in southern Africa. Symbolae Botanicae Upsalienses 34: 257–288.
Molins, A., P. Moya, F. J. García-Breijo, J. Reig-Armiñana, and E. Barreno. 2018. Molecular and morphological diversity of Trebouxia microalgae in sphaerothallioid Circinaria spp. lichens. Journal of Phycology 54: 494–504.
Moya, P., A. Molins, P. Škaloud, P. K. Divakar, S. Chiva, C. Dumitru, M. C. Molina, et al. 2021. Biodiversity patterns and ecological preferences of the photobionts associated with the lichen-forming genus Parmelia. Frontiers in Microbiology 12: 765310.
Mucina, L., and M. C. Rutherford [eds.]. 2006. The vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19. South African National Biodiversity Institute, Pretoria, South Africa.
Muggia, L., S. D. Leavitt, and E. Barreno. 2018. The hidden diversity of lichenised Trebouxiophyceae (Chlorophyta). Phycologia 57: 503–524.
Muggia, L., M. P. Nelsen, P. M. Kirika, E. Barreno, A. Beck, H. Lindgren, H. T. Lumbsch, et al. 2020. Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus Trebouxia (Trebouxiophyceae, Chlorophyta): an impetus for developing an integrated taxonomy. Molecular Phylogenetics and Evolution 149: 106821.
Muggia, L., S. Pérez-Ortega, T. Kopun, G. Zellnig, and M. Grube. 2014. Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi. Annals of Botany 114: 463–475.
Nelsen, M. P., S. D. Leavitt, K. Heller, L. Muggia, and H. T. Lumbsch. 2021. Macroecological diversification and convergence in a clade of keystone symbionts. FEMS Microbiology Ecology 97: fiab072.
Nelsen, M. P., E. Rivas Plata, C. J. Andrew, R. Lücking, and H. T. Lumbsch. 2011. Phylogenetic diversity of Trentepohlialean algae associated with lichen-forming fungi. Journal of Phycology 47: 282–290.
Nguyen, L. T., H. A. Schmidt, A. Von Haeseler, and B. Q. Minh. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274.
Nyati, S., D. Bhattacharya, S. Werth, and R. Honegger. 2013. Phylogenetic analysis of LSU and SSU rDNA group I introns of lichen photobionts associated with the genera Xanthoria and Xanthomendoza (Teloschistaceae, lichenized Ascomycetes). Journal of Phycology 49: 1154–1166.
Nyati, S., S. Scherrer, S. Werth, and R. Honegger. 2014. Green-algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes). Lichenologist 46: 189–212.
O'Brien, H. E., J. Miadlikowska, and F. Lutzoni. 2013. Assessing population structure and host specialization in lichenized cyanobacteria. New Phytologist 198: 557–566.
Ohmura, Y., M. Kawachi, F. Kasai, M. M. Watanabe, and S. Takeshita. 2006. Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 109: 43–59.
Ohmura, Y., S. Takeshita, and M. Kawachi. 2019. Photobiont diversity within populations of a vegetatively reproducing lichen, Parmotrema tinctorum, can be generated by photobiont switching. Symbiosis 77: 59–72.
Oksanen, J., G. L. Simpson, F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. O'Hara, et al. 2022. vegan: Community ecology package, version 2.6-4. Website: https://CRAN.R-project.org/package=vegan
Paul, F., J. Otte, I. Schmitt, and F. Dal Grande. 2018. Comparing Sanger sequencing and high-throughput metabarcoding for inferring photobiont diversity in lichens. Scientific Reports 8: 8624.
Paradis, E., and K. Schliep. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526–528.
Pedersen, T. 2022. ggraph: An implementation of grammar of graphics for graphs and networks. Websites: https://ggraph.data-imaginist.com, https://github.com/thomasp85/ggraph
Peksa, O., and P. Škaloud. 2011. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20: 3936–3948.
Peksa, O., T. Gebouská, Z. Škvorová, L. Vančurová, and P. Škaloud. 2022. The guilds in green algal lichens—An insight into the life of terrestrial symbiotic communities. FEMS Microbiology Ecology 98: fiac008.
Pérez-Ortega, S., M. Verdú, I. Garrido-Benavent, S. Rabasa, T. A. Green, L. G. Sancho, and A. de los Ríos. 2023. Invariant properties of mycobiont-photobiont networks in Antarctic lichens. Global Ecology and Biogeography 32: 2033–2046.
Pessi, I. S., Y. Lara, B. Durieu, P. D. C. Maalouf, E. Verleyen, and A. Wilmotte. 2018. Community structure and distribution of benthic cyanobacteria in Antarctic lacustrine microbial mats. FEMS Microbiology Ecology 94: fiy042.
Puillandre, N., S. Brouillet, and G. Achaz. 2021. ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21: 609–620.
Puillandre, N., A. Lambert, S. Brouillet, and G. Achaz. 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.
de Puymaly, A. 1924. Le Chlorococcum humicola (Nag.) Rabenh. Revue Algologique 1: 107–114.
R Core Team. 2023. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website: https://www.R-project.org/
Rafat, A., H. J. Ridgway, R. H. Cruickshank, and H. L. Buckley. 2015. Isolation and co-culturing of symbionts in the genus Usnea. Symbiosis 66: 123–132.
Rolshausen, G., F. Dal Grande, A. D. Sadowska-Deś, J. Otte, and I. Schmitt. 2018. Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualist-mediated niche expansions. Ecography 41: 1380–1392.
Rolshausen, G., U. Hallman, F. Dal Grande, J. Otte, K. Knudsen, and I. Schmitt. 2020. Expanding the mutualistic niche: parallel symbiont turnover along climatic gradients. Proceedings of the Royal Society, B, Biological Sciences 287: 20192311.
Rognes, T., T. Flouri, B. Nichols, C. Quince, and F. Mahé. 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4: e2584.
Ruprecht, U., F. Fernández-Mendoza, R. Türk, and A. M. Fryday. 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: 287–303.
Ryšánek, D., K. Hrčková, and P. Škaloud. 2015. Global ubiquity and local endemism of free-living terrestrial protists: phylogeographic assessment of the streptophyte alga Klebsormidium. Environmental Microbiology 17: 689–698.
Sadowska-Deś, A. D., M. Bálint, J. Otte, and I. Schmitt. 2013. Assessing intraspecific diversity in a lichen-forming fungus and its green algal symbiont: evaluation of eight molecular markers. Fungal Ecology 6: 141–151.
Sadowska-Deś, A. D., F. Dal Grande, H. T. Lumbsch, A. Beck, J. Otte, J.-S. Hur, J. A. Kim, and I. Schmitt. 2014. Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont Trebouxia. Molecular Phylogenetics and Evolution 76: 202–210.
Sanders, W. B., and H. Masumoto. 2021. Lichen algae: the photosynthetic partners in lichen symbioses. Lichenologist 53: 347–393.
Schieferstein, B., and K. Loris. 1992. Ecological investigations on lichen fields of the Central Namib: I. Distribution patterns and habitat conditions. Vegetatio 98: 113–128.
Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R. A. Lesniewski, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75: 7537–7541.
Schnitzler, J., T. G. Barraclough, J. S. Boatwright, P. Goldblatt, J. C. Manning, M. P. Powell, T. Rebelo, and V. Savolainen. 2011. Causes of plant diversification in the Cape biodiversity hotspot of South Africa. Systematic Biology 60: 343–357.
Simmons, R. E., M. Griffin, R. E. Griffin, E. Marais, and H. Kolberg. 1998. Endemism in Namibia: patterns, processes and predictions. Biodiversity & Conservation 7: 513–530.
Sipman, H. 2017. Compiled key to Xanthoparmelia in Southern Africa. Website: https://archive.bgbm.org/BGBM/STAFF/Wiss/Sipman/keys/Afroxantkey3a.pdf [accessed 3 August 2023].
Singh, G., F. Dal Grande, P. K. Divakar, J. Otte, A. Crespo, and I. Schmitt. 2017. Fungal–algal association patterns in lichen symbiosis linked to macroclimate. New Phytologist 214: 317–329.
Škaloud, P., J. Steinová, T. Řídká, L. Vančurová, and O. Peksa. 2015. Assembling the challenging puzzle of algal biodiversity: species delimitation within the genus Asterochloris (Trebouxiophyceae, Chlorophyta). Journal of Phycology 51: 507–527.
Škaloud, P., P. Moya, A. Molins, O. Peksa, A. Santos-Guerra, and E. Barreno. 2018. Untangling the hidden intrathalline microalgal diversity in Parmotrema pseudotinctorum: Trebouxia crespoana sp. nov. Lichenologist 50: 357–369.
Stevens, G. N. 1999. A revision of the lichen family Usneaceae in Australia. Bibliotheca Lichenologica 72: 1–128.
Swinscow, T. D. V., and H. Krog. 1988. Macrolichens of East Africa. British Museum (Natural History), London, UK.
Vančurová, L., J. Malíček, J. Steinová, and P. Škaloud. 2021. Choosing the right life partner: Ecological drivers of lichen symbiosis. Frontiers in Microbiology 12: 769304.
Vančurová, L., L. Muggia, O. Peksa, T. Řídká, and P. Škaloud. 2018. The complexity of symbiotic interactions influences the ecological amplitude of the host: a case study in Stereocaulon (lichenized Ascomycota). Molecular Ecology 27: 3016–3033.
van der Niet, T., and S. D. Johnson. 2009. Patterns of plant speciation in the Cape floristic region. Molecular Phylogenetics and Evolution 51: 85–93.
Vargas Castillo, R., and A. Beck. 2012. Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile. Fungal Biology 116: 665–676.
Vázquez, D. P., C. J. Melian, N. M. Williams, N. Blüthgen, B. R. Krasnov, and R. Poulin. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos 116: 1120–1127.
Verboom, G. A., J. K. Archibald, F. T. Bakker, D. U. Bellstedt, F. Conrad, L. L. Dreyer, F. Forest, et al. 2009. Origin and diversification of the Greater Cape flora: ancient species repository, hot-bed of recent radiation, or both? Molecular Phylogenetics and Evolution 51: 44–53.
Vilgalys, R., and M. Hester. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246.
Wagner, M., G. Brunauer, A. C. Bathke, S. C. Cary, R. Fuchs, L. G. Sancho, R. Türk, and U. Ruprecht. 2021. Macroclimatic conditions as main drivers for symbiotic association patterns in lecideoid lichens along the Transantarctic Mountains, Ross Sea region, Antarctica. Scientific Reports 11: 23460.
Werth, S., and V. L. Sork. 2010. Identity and genetic structure of the photobiont of the epiphytic lichen Ramalina menziesii on three oak species in southern California. American Journal of Botany 97: 821–830.
Wessels, D., and L. Kappen. 1993. Photosynthetic performance of rock-colonising lichens in the Mountain Zebra National Park, South Africa. Koedoe 36: 27–48.
White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols: a guide to methods and applications, 315–322. Academic Press, London, UK.
Whittaker, R. H. 1960. Vegetation of the Siskiyou mountains, Oregon and California. Ecological Monographs 30: 279–338.
Wiemers, M., and K. Fiedler. 2007. Does the DNA barcoding gap exist? A case study in blue butterflies (Lepidoptera: Lycaenidae). Frontiers in Zoology 4: 8.
Wirth, V. 2010. Lichens of the Namib Desert: a guide to their identification. Klaus Hess, Göttingen, Germany.
Wolseley, P. 1997. Response of epiphytic lichens to fire in tropical forests of Thailand. Bibliotheca Lichenologica 68: 165–176.
Xu, M., H. De Boer, E. S. Olafsdottir, S. Omarsdottir, and S. Heidmarsson. 2020. Phylogenetic diversity of the lichenized algal genus Trebouxia (Trebouxiophyceae, Chlorophyta): a new lineage and novel insights from fungal-algal association patterns of Icelandic cetrarioid lichens (Parmeliaceae, Ascomycota). Botanical Journal of the Linnean Society 194: 460–468.
Xu, S., Z. Dai, P. Guo, X. Fu, S. Liu, L. Zhou, W. Tang, et al. 2021. ggtreeExtra: Compact visualization of richly annotated phylogenetic data. Molecular Biology and Evolution 38: 4039–4042.
Yu, G., D. K. Smith, H. Zhu, Y. Guan, and T. T. Y. Lam. 2017. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution 8: 28–36.
Zedda, L., and G. Rambold. 2009. Diversity and ecology of soil lichens in the Knersvlakte (South Africa). Bryologist 112: 19–29.
Zhang, J., P. Kapli, P. Pavlidis, and A. Stamatakis. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.
Zhang, Z., S. Schwartz, L. Wagner, and W. Miller. 2000. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7: 203–214.
Zoller, S., C. Scheidegger, and C. Sperisen. 1999. PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31: 511–516.