Climatic factors, soil chemistry and geography are considered as major factors affecting lichen distribution and diversity. To determine how these factors limit or support the associations between the symbiotic partners, we revise the lichen symbiosis as a network of relationships here. More than one thousand thalli of terricolous Cladonia lichens were collected at sites with a wide range of soil chemical properties from seven biogeographical regions of Europe. A total of 18 OTUs of the algal genus Asterochloris and 181 OTUs of Cladonia mycobiont were identified. We displayed all realized pairwise mycobiont-photobiont relationships and performed modularity analysis. It revealed four virtually separated modules of cooperating OTUs. The modules differed in mean annual temperature, isothermality, precipitation, evapotranspiration, soil pH, nitrogen, and carbon contents. Photobiont switching was strictly limited to algae from one module, i.e., algae of similar ecological preferences, and only few mycobionts were able to cooperate with photobionts from different modules. Thus, Cladonia mycobionts generally cannot widen their ecological niches through photobiont switching. The modules also differed in the functional traits of the mycobionts, e.g., sexual reproduction rate, presence of soredia, and thallus type. These traits may represent adaptations to the environmental conditions that drive the differentiation of the modules. In conclusion, the promiscuity in Cladonia mycobionts is strictly limited by climatic factors and soil chemistry.

Botánica ICBIBE Fac CC Biológicas Universitat de València Valencia Spain

Department of Botany Faculty of Science Charles University Prague Czechia

Museum of West Bohemia in Pilsen Pilsen Czechia

Zobrazit více v PubMed

Ahti T. (2000). Cladoniaceae. Flora Neotrop. 78 1–362.

Ahti T., Stenroos S., Moberg R. (2013). Nordic Lichen Flora, Vol 5, Cladoniaceae. Uppsala: Museum of Evolution, Uppsala University. 10.1017/S0024282914000322 DOI

Ammerman J. (2001). Determination of Nitrate/Nitrite in 0,5 M K2SO4 soil extracts by Flow Injection analysis. QuikChem Method 12-107-04-1-H. Milwaukee, WI: LACHAT INSTRUMENTS.

Armstrong R. A. (1991). The influence of climate on the dispersal of lichen soredia. Environ. Exp. Bot. 31 239–245. 10.1016/0098-8472(91)90076-Z DOI

Arnold A. E., Miadlikowska J., Higgins K. L., Sarvate S. D., Gugger P., Way A., et al. (2009). A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst. Biol. 58 283–297. 10.1093/sysbio/syp001 PubMed DOI

Bačkor M., Hudák J., Repčák M., Ziegler W., Bačkorová M. (1992). The influence of pH and lichen metabolites (vulpinic acid and (+) usnic acid) on the growth of the lichen photobiont Trebouxia irregularis. Lichenologist 30 577–582. 10.1006/lich.1998.0166 DOI

Baker A. C. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34 661–689. 10.1146/annurev.ecolsys.34.011802.132417 DOI

Bastian M., Heymann S., Jacomy M. (2009). “Gephi: an open source software for exploring and manipulating networks,” in Proceedings of the 3rd international AAAI conference on weblogs and social media, San Jose, CA.

Bates S. T., Cropsey G. W., Caporaso J. G., Knight R., Fierer N. (2011). Bacterial communities associated with the lichen symbiosis. Appl. Environ. Microbiol. 77 1309–1314. 10.1128/AEM.02257-10 PubMed DOI PMC

Beck A. (2002). Selektivität der Symbionten Schwermetalltoleranter Flechten. München: Ludwig-Maximilians-Universität.

Blaha J., Baloch E., Grube M. (2006). High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biol. J. Linn. Soc. 88 283–293. 10.1111/j.1095-8312.2006.00640.x DOI

Borcard D., Legendre P., Avois-Jacquet C., Tuomisto H. (2004). Dissecting the spatial structure of ecological data at multiple scales. Ecology 85 1826–1832. 10.1890/03-3111 DOI

Borcard D., Legendre P., Drapeau P. (1992). Partialling out the spatial component of ecological variation. Ecology 73 1045–1055. 10.2307/1940179 DOI

Brodo I. M. (1973). “Substrate ecology,” in The lichens, eds Ahmadjian V., Hale M. E. (New York, NY: Academic Press; ), 401–441. 10.1016/B978-0-12-044950-7.50017-9 DOI

Chambers J. M. (2013). SoDA: Functions and Examples for “Software for Data Analysis”. R Package Version, 1-0. Available online at: https://CRAN.R-project.org/package=SoDA

Cocchietto M., Skert N., Nimis P., Sava G. (2002). A review on usnic acid, an interesting natural compound. Naturwissenschaften 89 137–146. 10.1007/s00114-002-0305-3 PubMed DOI

Cubero O. F., Crespo A. N. A., Fatehi J., Bridge P. D. (1999). DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Syst. Evol. 216 243–249. 10.1007/BF01084401 DOI

Dal Grande F., Beck A., Cornejo C., Singh G., Cheenacharoen S., Nelsen M. P., et al. (2014). Molecular phylogeny and symbiotic selectivity of the green algal genus Dictyochloropsis s.l. (Trebouxiophyceae): a polyphyletic and widespread group forming photobiont-mediated guilds in the lichen family Lobariaceae. New Phytol. 202 455–470. 10.1111/nph.12678 PubMed DOI

Dal Grande F., Widmer I., Wagner H. H., Scheidegger C. (2012). Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol. Ecol. 21 3159–3172. 10.1111/j.1365-294X.2012.05482.x PubMed DOI

Del M., Molina C., Bajon C., Sauvanet A., Robert D., Vicente C. (1998). Detection of polysaccharides and ultrastructural modification of the photobiont cell wall produced by two arginase isolectins from Xanthoria parietina. J. Plant Res. 111:191. 10.1007/BF02512169 DOI

DePriest P. T. (2004). Early molecular investigations of lichen-forming symbionts: 1986–2001. Annu. Rev. Microbiol. 58 273–301. 10.1146/annurev.micro.58.030603.123730 PubMed DOI

Dixon P. (2003). VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14 927–930. 10.1111/j.1654-1103.2003.tb02228.x DOI

Dray S., Dufour A. B. (2007). The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22 1–20.

Drummond A. J., Suchard M. A., Xie D., Rambaut A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29 1969–1973. 10.1093/molbev/mss075 PubMed DOI PMC

Easton R. (1994). Lichens and rocks: a review. Geosci. Can. 21 59–76.

Egan L. (2001). Determination of Amonia by Flow Injection Analysis Colorimetr. QuikChem Metod, 10-107-06-5-E. Loveland, CO: Lachat Instruments.

Egerton-Warburton L., Allen M. F. (2001). Endo-and ectomycorrhizas in Quercus agrifolia Nee.(Fagaceae): patterns of root colonization and effects on seedling growth. Mycorrhiza 11 283–290. 10.1007/s005720100134 PubMed DOI

Etges S., Ott S. (2001). Lichen mycobionts transplanted into the natural habitat. Symbiosis 30 191–206.

Ezard T., Fujisawa T., Barraclough T. G. (2009). Splits: species’ limits by threshold statistics. R Package Version 1:r29. Available online at: https://rdrr.io/rforge/splits/

Fernández-Mendoza F., Domaschke S., García M. A., Jordan P., Martín M. P., Printzen C. (2011). Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol. Ecol. 20 1208–1232. 10.1111/j.1365-294X.2010.04993.x PubMed DOI

Fontaine K. M., Teuvo A. H. T. I., Piercey-Normore M. D. (2010). Convergent evolution in Cladonia gracilis and allies. Lichenologist 42 323–338. 10.1017/S0024282909990569 DOI

Friedl T. (1987). Thallus development and phycobionts of the parasitic lichen Diploschistes muscorum. Lichenologist 19 183–191. 10.1017/S002428298700015X DOI

Gardes M., Bruns T. D. (1993). ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2 113–118. 10.1111/j.1365-294X.1993.tb00005.x PubMed DOI

Gardner C. R., Mueller D. M. (1981). Factors affecting the toxicity of several lichen acids: effect of pH and lichen acid concentration. Am. J. Bot. 68 87–95. 10.1002/j.1537-2197.1981.tb06359.x DOI

Gasulla F., de Nova P. G., Esteban-Carrasco A., Zapata J. M., Barreno E., Guéra A. (2009). Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta 231 195–208. 10.1007/s00425-009-1019-y PubMed DOI

Gilbert O. L. (1986). Field evidence for an acid rain effect on lichens. Environ. Pollut. Ser. A Ecol. Biol. 40 227–231. 10.1016/0143-1471(86)90097-8 DOI

Goyal R., Seaward M. R. D. (1981). Metal uptake in terricolous lichens: I. Metal localization within the thallus. New Phytol. 89 631–645. 10.1111/j.1469-8137.1981.tb02342.x DOI

Grube M., Cardinale M., de Castro J. V., Müller H., Berg G. (2009). Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J. 3 1105–1115. 10.1038/ismej.2009.63 PubMed DOI

Hamlett C. A., Shirtcliffe N. J., Pyatt F. B., Newton M. I., McHale G., Koch K. (2011). Passive water control at the surface of a superhydrophobic lichen. Planta 234 1267–1274. 10.1007/s00425-011-1475-z PubMed DOI

Hauck M., Jürgens S. R. (2008). Usnic acid controls the acidity tolerance of lichens. Environ. Pollut. 156 115–122. 10.1016/j.envpol.2007.12.033 PubMed DOI

Hawksworth D. L., Grube M. (2020). Lichens redefined as complex ecosystems. New Phytol. 227 1281. 10.1111/nph.16630 PubMed DOI PMC

Hepperle D. (2004). SeqAssem. A Sequence Analysis Tool, Contig Assembler and Trace Data Visualization Tool for Molecular Sequences. Win32-Version. Available online at: http://www.sequentix.de

Higgins N. F., Connan S., Stengel D. B. (2015). Factors influencing the distribution of coastal lichens Hydropunctaria maura and Wahlenbergiella mucosa. Mar. Ecol. 36 1400–1414. 10.1111/maec.12239 DOI

Hijmans R. J. (2019). geosphere: Spherical Trigonometry. R Package Version 1.5-10. Available online at: https://CRAN.R-project.org/package=geosphere/

Hill D. J. (1994). The nature of the symbiotic relationship in lichens. Endeavour 18 96–103. 10.1016/S0160-9327(05)80083-3 DOI

Honegger R. (1991). Functional aspects of the lichen symbiosis. Annu. Rev. Plant Biol. 42 553–578. 10.1146/annurev.pp.42.060191.003005 DOI

Honegger R. (1996). Experimental studies of growth and regenerative capacity in the foliose lichen Xanthoria parietina. New Phytol. 133 573–581. 10.1111/j.1469-8137.1996.tb01926.x DOI

Honegger R. (2006). Water Relations in Lichens. Fungi and the Environment Lichen Biology. Cambridge: Cambridge University Press, 185–200.

Hume B. C., D’Angelo C., Smith E. G., Stevens J. R., Burt J., Wiedenmann J. (2015). Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci. Rep. 5 1–8. 10.1038/srep08562 PubMed DOI PMC

Jackson D. A. (1993). Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74 2204–2214. 10.2307/1939574 DOI

James P. W. (2009). “Cladonia P. Browne (1756),” in The Lichens of Great Britain and Ireland, eds Smith C. W., Aptroot A., Coppins B. J., Fletcher A., Gilbert O. L., James P. W., et al. (London: British Lichen Society; ), 309–338.

Jukes T. H., Cantor C. R. (1969). Evolution of protein molecules. Mammal. Protein Metab. 3 21–132.

Kaplan J. (2020). fastDummies: Fast Creation of Dummy (Binary) Columns and Rows from Categorical Variables. R package version 1.6. 1. Available online at: https://CRAN.R-project.org/package=fastDummies

Karger D. N., Conrad O., Böhner J., Kawohl T., Kreft H., Soria-Auza R. W., et al. (2017). Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4 1–20. 10.1038/sdata.2017.122 PubMed DOI PMC

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 772–780. 10.1093/molbev/mst010 PubMed DOI PMC

Kawaida H., Ohba K., Koutake Y., Shimizu H., Tachida H., Kobayakawa Y. (2013). Symbiosis between hydra and chlorella: molecular phylogenetic analysis and experimental study provide insight into its origin and evolution. Mol. Phylogenet. Evol. 66 906–914. 10.1016/j.ympev.2012.11.018 PubMed DOI

Kemp D. W., Hernandez-Pech X., Iglesias-Prieto R., Fitt W. K., Schmidt G. W. (2014). Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol. Oceanogr. 59 788–797. 10.4319/lo.2014.59.3.0788 DOI

Kosecka M., Guzow-Krzemińska B., Černajová I., Škaloud P., Jabłońska A., Kukwa M. (2021). New lineages of photobionts in Bolivian lichens expand our knowledge on habitat preferences and distribution of Asterochloris algae. Sci. Rep. 11 1–12. 10.1038/s41598-021-88110-0 PubMed DOI PMC

Kotelko R., Piercey-Normore M. D. (2010). Cladonia pyxidata and C. pocillum; genetic evidence to regard them as conspecific. Mycologia 102 534–545. 10.3852/09-030 PubMed DOI

Lapeyrie F. F., Chilvers G. A. (1985). An endomycorrhiza-ectomycorrhiza succession associated with enhanced growth of Eucalyptus dumosa seedlings planted in a calcareous soil. New Phytol. 100 93–104. 10.1111/j.1469-8137.1985.tb02761.x DOI

Leavitt S. D., Kraichak E., Nelsen M. P., Altermann S., Divakar P. K., Alors D., 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). Mol. Ecol. 24 3779–3797. 10.1111/mec.13271 PubMed DOI

Lechowicz M. J. (1982). The effects of simulated acid precipitation on photosynthesis in the caribou lichen Cladina stellaris (Opiz) Brodo. Water Air Soil Pollut. 18 421–430. 10.1007/BF02419429 DOI

Lücking R., Lawrey J. D., Sikaroodi M., Gillevet P. M., Chaves J. L., Sipman H. J., et al. (2009). Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. Am. J. Bot. 96 1409–1418. 10.3732/ajb.0800258 PubMed DOI

Moya P., Škaloud P., Chiva S., García-Breijo F. J., Reig-Arminana J., Vančurová L., et al. (2015). Molecular phylogeny and ultrastructure of the lichen microalga Asterochloris mediterranea sp. nov. from Mediterranean and Canary Islands ecosystems. Int. J. Syst. Evol. Microbiol. 65(Pt_6) 1838–1854. 10.1099/ijs.0.000185 PubMed DOI

Nakazawa M. (2012). fmsb: Functions for Medical Statistics Book with some Demographic Data. R package version 0.7.1. Available online at: http://cran.r-project.org/web/packages/fmsb/fmsb.pdf

Nelsen M. P., Gargas A. (2008). Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol. 177 264–275. 10.1111/j.1469-8137.2007.02241.x PubMed DOI

Nelson D. W., Sommers L. E. (1996). Total carbon, organic carbon, and organic matter. Methods Soil Anal. Part 3 Chem. Methods 5 961–1010. 10.2136/sssabookser5.3.c34 DOI

Nowack E. C., Price D. C., Bhattacharya D., Singer A., Melkonian M., Grossman A. R. (2016). Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. Proc. Natl. Acad. Sci. U.S.A. 113 12214–12219. 10.1073/pnas.1608016113 PubMed DOI PMC

Orange A., James P. W., White F. J. (2001). Microchemical Methods for the Identification of Lichens. London: British Lichen Society.

Osyczka P., Lenart-Boroń A., Boroń P., Rola K. (2021). Lichen-forming fungi in postindustrial habitats involve alternative photobionts. Mycologia 113 43–55. 10.1080/00275514.2020.1813486 PubMed DOI

Paradis E., Schliep K. (2019). ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35 526–528. 10.1093/bioinformatics/bty633 PubMed DOI

Peksa O., Škaloud P. (2011). Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol. Ecol. 20 3936–3948. 10.1111/j.1365-294X.2011.05168.x PubMed DOI

Pennell M. W., Eastman J. M., Slater G. J., Brown J. W., Uyeda J. C., FitzJohn R. G., et al. (2014). geiger v2. 0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30 2216–2218. 10.1093/bioinformatics/btu181 PubMed DOI

Perret X., Staehelin C., Broughton W. J. (2000). Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64 180–201. 10.1128/MMBR.64.1.180-201.2000 PubMed DOI PMC

Piercey-Normore M. D., DePriest P. T. (2001). Algal switching among lichen symbioses. Am. J. Bot. 88 1490–1498. 10.2307/3558457 PubMed DOI

Pino-Bodas R., Stenroos S. (2020). Global biodiversity patterns of the photobionts associated with the genus Cladonia (Lecanorales, Ascomycota). Microb. Ecol. 82 1–15. 10.1007/s00248-020-01633-3 PubMed DOI PMC

Pino-Bodas R., Martin M. P., Burgaz A. R., Lumbsch H. T. (2013). Species delimitation in Cladonia (Ascomycota): a challenge to the DNA barcoding philosophy. Mol. Ecol. Resour. 13 1058–1068. 10.1111/1755-0998.12086 PubMed DOI

Puillandre N., Lambert A., Brouillet S., Achaz G. (2012). ABGD, Automatic barcode gap discovery for primary species delimitation. Mol. Ecol. 21 1864–1877. 10.1111/j.1365-294X.2011.05239.x PubMed DOI

Purvis O. W., Halls C. (1996). A review of lichens in metal-enriched environments. Lichenologist 28 571–601. 10.1006/lich.1996.0052 DOI

Pyatt F. B. (1973). “Lichen propagules,” in The Lichens, eds Ahmadjian V., Hale M. E., Jr. (London: Academic Press; ), 117–145. 10.1016/B978-0-12-044950-7.50009-X DOI

R Core Team (2020). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Rambaut A., Drummond A. J., Xie D., Baele G., Suchard M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67:901. 10.1093/sysbio/syy032 PubMed DOI PMC

Resl P., Fernández-Mendoza F., Mayrhofer H., Spribille T. (2018). The evolution of fungal substrate specificity in a widespread group of crustose lichens. Proc. R. Soc. B 285:20180640. 10.1098/rspb.2018.0640 PubMed DOI PMC

Revell L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3 217–223. 10.1111/j.2041-210X.2011.00169.x DOI

Rikkinen J. (2003). Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34 99–110.

Rola K., Lenart-Boroń A., Boroń P., Osyczka P. (2021). Heavy-metal pollution induces changes in the genetic composition and anatomical properties of photobionts in pioneer lichens colonizing post-industrial habitats. Sci. Total Environ. 750:141439. 10.1016/j.scitotenv.2020.141439 PubMed DOI

Rolshausen G., Hallman U., Grande F. D., Otte J., Knudsen K., Schmitt I. (2020). Expanding the mutualistic niche: parallel symbiont turnover along climatic gradients. Proc. R. Soc. B 287:20192311. 10.1098/rspb.2019.2311 PubMed DOI PMC

Rosabal D., Burgaz A. R., Reyes O. J. (2013). Substrate preferences and phorophyte specificity of corticolous lichens on five tree species of the montane rainforest of Gran Piedra, Santiago de Cuba. Bryologist 116 113–121. 10.1639/0007-2745-116.2.113 PubMed DOI

Scott M. G., Hutchinson T. C. (1987). Effects of a simulated acid rain episode on photosynthesis and recovery in the caribou-forage lichens Cladina stellaris (Opiz.) Brodo and Cladina rangiferina (L.) Wigg. New Phytol. 107 567–575. 10.1111/j.1469-8137.1987.tb02927.x DOI

Singh G., Dal Grande F., Divakar P. K., Otte J., Crespo A., Schmitt I. (2017). Fungal–algal association patterns in lichen symbiosis linked to macroclimate. New Phytol. 214 317–329. 10.1111/nph.14366 PubMed DOI

Škaloud P., Peksa O. (2010). Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Mol. Phylogenet. Evol. 54 36–46. 10.1016/j.ympev.2009.09.035 PubMed DOI

Škaloud P., Steinová J., Řídká T., Vančurová L., Peksa O. (2015). Assembling the challenging puzzle of algal biodiversity: species delimitation within the genus Asterochloris (Trebouxiophyceae, Chlorophyta). J. Phycol. 51 507–527. 10.1111/jpy.12295 PubMed DOI

Slocum R. D., Ahmadjian V., Hildreth K. C. (1980). Zoosporogenesis in Trebouxia gelatinosa: ultrastructure potential for zoospore release and implications for the lichen association. Lichenologist 12 173–187. 10.1017/S0024282980000151 DOI

Spribille T., Tuovinen V., Resl P., Vanderpool D., Wolinski H., Aime M. C., et al. (2016). Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353 488–492. 10.1126/science.aaf8287 PubMed DOI PMC

Steinová J., Škaloud P., Yahr R., Bestová H., Muggia L. (2019). Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in Cladonia lichens. Mol. Phylogen. Evol. 134, 226–237. 10.1016/j.ympev.2019.02.014 PubMed DOI

Stenroos S., Hyvönen J., Myllys L., Thell A., Ahti T. (2002). Phylogeny of the genus Cladonia s. lat.(Cladoniaceae, Ascomycetes) inferred from molecular, morphological, and chemical data. Cladistics 18 237–278. 10.1006/clad.2002.0202 PubMed DOI

Stenroos S., Pino-Bodas R., Hyvönen J., Lumbsch H. T., Ahti T. (2019). Phylogeny of the family Cladoniaceae (Lecanoromycetes, Ascomycota) based on sequences of multiple loci. Cladistics 35 351–384. 10.1111/cla.12363 PubMed DOI

Suchard M. A., Lemey P., Baele G., Ayres D. L., Drummond A. J., Rambaut A. (2018). Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4:vey016. 10.1093/ve/vey016 PubMed DOI PMC

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30 2725–2729. 10.1093/molbev/mst197 PubMed DOI PMC

Ten Veldhuis M. C., Ananyev G., Dismukes G. C. (2020). Symbiosis extended: exchange of photosynthetic O2 and fungal-respired CO2 mutually power metabolism of lichen symbionts. Photosynthesis Res. 143 287–299. 10.1007/s11120-019-00702-0 PubMed DOI PMC

Thüs H., Muggia L., Pérez-Ortega S., Favero-Longo S. E., Joneson S., O’Brien H., et al. (2011). Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur. J. Phycol. 46 399–415. 10.1080/09670262.2011.629788 DOI

Thüs H., Schultz M. (2008). Freshwater Flora of Central Europe, Vol. 21/1, Fungi, Part 1: Lichens. Heidelberg: Spektrum.

Tormo R., Recio D., Silva I., Muñoz A. F. (2001). A quantitative investigation of airborne algae and lichen soredia obtained from pollen traps in south-west Spain. Eur. J. Phycol. 36, 385–390. 10.1080/09670260110001735538 DOI

Trabucco A., Zomer R. J. (2019). Global Aridity Index and Potential Evapotranspiration (ET0) Climate Database v2 Fileset. figshare. Available online at: https://figshare.com/articles/dataset/Global_Aridity_Index_and_Potential_Evapotranspiration_ET0_Climate_Database_v2/7504448/3 (accessed January 18, 2019). PubMed PMC

Uphof J. T. (1925). The occurrence of purple bacteria as symbionts of a lichen. Am. J. Bot. 12 97–103. 10.2307/243539 PubMed DOI

Vančurová L., Muggia L., Peksa O., Řídká T., Škaloud P. (2018). The complexity of symbiotic interactions influences the ecological amplitude of the host: a case study in Stereocaulon (lichenized Ascomycota). Mol. Ecol. 27 3016–3033. 10.1111/mec.14764 PubMed DOI

Vandenkoornhuyse P., Husband R., Daniell T. J., Watson I. J., Duck J. M., Fitter A. H., et al. (2002). Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol. Ecol. 11 1555–1564. 10.1046/j.1365-294X.2002.01538.x PubMed DOI

Vargas A. A., Graham P. H. (1989). Cultivar and pH effects on competition for nodule sites between isolates of Rhizobium in beans. Plant Soil 117 195–200. 10.1007/BF02220712 DOI

Vondrák J., Liška J. (2010). Changes in distribution and substrate preferences of selected threatened lichens in the Czech Republic. Biologia 65 595–602. 10.2478/s11756-010-0061-3 DOI

Weber K., Kabsch W. (1994). Intron positions in actin genes seem unrelated to the secondary structure of the protein. EMBO J. 13 1280–1286. 10.1002/j.1460-2075.1994.tb06380.x PubMed DOI PMC

Wedin M., Maier S., Fernandez-Brime S., Cronholm B., Westberg M., Grube M. (2016). Microbiome change by symbiotic invasion in lichens. Environ. l Microbiol. 18 1428–1439. 10.1111/1462-2920.13032 PubMed DOI

Wei T., Simko V., Levy M., Xie Y., Jin Y., Zemla J. (2017). Package ‘corrplot’. Statistician 56:e24.

White T. J., Bruns T., Lee S. J. W. T., Taylor J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc. Guide Methods Appl. 18 315–322.

Wilcoxon F. (1992). “Individual comparisons by ranking methods,” in Breakthroughs in statistics, eds Kotz S., Johnson N. L. (New York, NY: Springer; ), 196–202. 10.1007/978-1-4612-4380-9_16 DOI

Williams L., Colesie C., Ullmann A., Westberg M., Wedin M., Büdel B. (2017). Lichen acclimation to changing environments: photobiont switching vs. climate-specific uniqueness in Psora decipiens. Ecol. Evol. 7 2560–2574. 10.1002/ece3.2809 PubMed DOI PMC

Wirtz N., Lumbsch H. T., Green T. A., Türk R., Pintado A., Sancho L., et al. (2003). Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol. 160 177–183. 10.1046/j.1469-8137.2003.00859.x PubMed DOI

Wornik S., Grube M. (2010). Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microb. Ecol. 59 150–157. 10.1007/s00248-009-9584-y PubMed DOI

Yahr R., Vilgalys R., DePriest P. T. (2006). Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol. 171 847–860. 10.1111/j.1469-8137.2006.01792.x PubMed DOI

Zedler J. B. (2000). Progress in wetland restoration ecology. Trends Ecol. Evol. 15 402–407. 10.1016/S0169-5347(00)01959-5 PubMed DOI

Zhang J., Kapli P., Pavlidis P., Stamatakis A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29 2869–2876. 10.1093/bioinformatics/btt499 PubMed DOI PMC

Zhang Z. S., Song X. L., Lu X. G., Xue Z. S. (2013). Ecological stoichiometry of carbon, nitrogen, and phosphorus in estuarine wetland soils: influences of vegetation coverage, plant communities, geomorphology, and seawalls. J. Soils Sediments 13 1043–1051. 10.1007/s11368-013-0693-3 DOI

Zraik M., Booth T., Piercey-Normore M. D. (2018). Relationship between lichen species composition, secondary metabolites and soil pH, organic matter, and grain characteristics in Manitoba. Botany 96 267–279. 10.1139/cjb-2017-0176 DOI

An Exception to the Rule? Could Photobiont Identity Be a Better Predictor of Lichen Phenotype than Mycobiont Identity?