The worldwide, ecologically relevant lichen-forming genus Parmelia currently includes 41 accepted species, of which the Parmelia sulcata group (PSULgp) and the Parmelia saxatilis group (PSAXgp) have received considerable attention over recent decades; however, phycobiont diversity is poorly known in Parmelia s. lat. Here, we studied the diversity of Trebouxia microalgae associated with 159 thalli collected from 30 locations, including nine Parmelia spp.: P. barrenoae, P. encryptata, P. ernstiae, P. mayi, P. omphalodes, P. saxatilis, P. serrana, P. submontana, and P. sulcata. The mycobionts were studied by carrying out phylogenetic analyses of the nrITS. Microalgae genetic diversity was examined by using both nrITS and LSU rDNA markers. To evaluate putative species boundaries, three DNA species delimitation analyses were performed on Trebouxia and Parmelia. All analyses clustered the mycobionts into two main groups: PSULgp and PSAXgp. Species delimitation identified 13 fungal and 15 algal species-level lineages. To identify patterns in specificity and selectivity, the diversity and abundance of the phycobionts were identified for each Parmelia species. High specificity of each Parmelia group for a given Trebouxia clade was observed; PSULgp associated only with clade I and PSAXgp with clade S. However, the degree of specificity is different within each group, since the PSAXgp mycobionts were less specific and associated with 12 Trebouxia spp., meanwhile those of PSULgp interacted only with three Trebouxia spp. Variation-partitioning analyses were conducted to detect the relative contributions of climate, geography, and symbiotic partner to phycobiont and mycobiont distribution patterns. Both analyses explained unexpectedly high portions of variability (99 and 98%) and revealed strong correlations between the fungal and algal diversity. Network analysis discriminated seven ecological clusters. Even though climatic conditions explained the largest proportion of the variation among these clusters, they seemed to show indifference relative to climatic parameters. However, the cluster formed by P. saxatilis A/P. saxatilis B/Trebouxia sp. 2/Trebouxia sp. S02/Trebouxia sp. 3A was identified to prefer cold-temperate as well as humid summer environments.

Botánica Instituto Cavanilles de Biodiversidad y Biología Evolutiva Fac CC Biológicas Universitat de València Valencia Spain

Departamento de Biología Geología Física y Química Inorgánica Escuela Superior de Ciencias Experimentales y Tecnología Universidad Rey Juan Carlos Madrid Spain

Departamento de Farmacología Farmacognosia y Botánica Facultad de Farmacia Universidad Complutense de Madrid Madrid Spain

Department of Botany Faculty of Science Charles University Prague Czechia

Zobrazit více v PubMed

Ahlmann-Eltze C., Patil I. (2021). Ggsignif: R package for displaying significance brackets for ‘gplot2. 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? PubMed DOI

Bačkor M., Peksa O., Škaloud P., Backorová M. (2010). Photobiont diversity in lichens from metal-rich substrata based on ITS rDNA sequences. PubMed DOI

Bastian M., Heymann S., Jacomy M. (2009). “Gephi: an open source software for exploring and manipulating networks,” in

Beck A., Kasalicky T., Rambold G. (2002). Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida.

Blaha J., Baloch E., Grube M. (2006). High photobiont diversity associated with the euryoecious lichen-forming ascomycete DOI

Borcard D., Legendre P., Avois-Jacquet C., Tuomisto H. (2004). Dissecting the spatial structure of ecological data at multiple scales.

Casano L. M., del Campo E., García-Breijo F., Reig-Armiñana J., Gasulla F., del Hoyo A., et al. (2011). Two Trebouxia algae with different physiological performances are ever present in lichen thalli of Ramalina farinacea. Coexistence versus competition? PubMed DOI

Chagnon P. L., Magain N., Miadlikowska J., Lutzoni F. (2019). Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera. DOI

Crespo A., Bridge P. D., Cubero O. F., Hawksworth D. L. (1997). Determination of genotypic variability in the lichen-forming fungus Parmelia sulcata.

Crespo A., Bridge P. D., Hawksworth D. L., Grube M., Cubero O. F. (1999). Comparison of rRNA genotype frequencies of

Crespo A., Kauff F., Divakar P. K., del Prado R., Pérez-Ortega S., de Paz G., et al. (2010). Phylogenetic generic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence. DOI

Crespo A., Molina M. C., Blanco O., Schroeter B., Sancho L. G., Hawksworth D. L. (2002). rDNA ITS and beta-tubulin gene sequence analyses reveal two monophyletic groups within the cosmopolitan lichen Parmelia saxatilis. DOI

Crespo A., Rico V. J., Garrido E., Lumbsch H. T., Divakar P. K. (2020). A revision of species of the

Currie D. J., Mittelbach G. G., Cornell H. V., Field R., Guégan J. F., Hawkins B. A., et al. (2004). Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. DOI

Dal Grande F., Rolshausen G., Divakar P. K., Crespo A., Otte J., Schleuning M., et al. (2018). Environment and host identity structure communities of green algal symbionts in lichens. PubMed DOI

Darriba D., Taboada G. L., Doallo R., Posada D. (2012). jModelTest 2, more models, new heuristics and parallel computing. PubMed DOI PMC

del Campo E. M., Gimeno J., De Nova J. P. G., Casano L. M., Gasulla F., García-Breijo F., et al. (2010). South European populations of

Divakar P. K., Leavitt S. D., Molina M. C., Del-Prado R., Lumbsch H. T., Crespo A. (2016). A DNA barcoding approach for identification of hidden diversity in

Divakar P. K., Molina M. C., Lumbsch H. T., Crespo A. (2005). Parmelia barrenoae, a new lichen species related to

Drummond A. J., Suchard M. A., Xie D., Rambaut A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. PubMed DOI PMC

Dumitru C. (2019).

Ertz D., Guzow-Krzemińska B., Thor G., Łubek A., Kukwa M. (2018). Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. PubMed DOI PMC

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. PubMed DOI

Gardes M., Bruns T. D. (1993). ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. PubMed DOI

Garrido-Benavent I., Molins A., Barreno E. (2021). Genetic variation of the symbiont partners in the endangered macrolichen DOI

Grube M., Wedin M. (2016). Lichenized fungi and the evolution of symbiotic organization. PubMed DOI

Guindon S., Gascuel O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. PubMed DOI

Hale M. E., Jr. (1987). A monograph of the lichen genus DOI

Hawksworth D. L., Blanco O., Divakar P. K., Ahti T., Crespo A. (2008). A first checklist of parmelioid and similar lichens in Europe and some adjacent territories, adopting revised generic circumscriptions and with indications of species distributions. DOI

Hawksworth D. L., Divakar P. K., Crespo A., Ahti T. (2011). The checklist of parmelioid and similar lichens in Europe and some adjacent territories: additions and corrections. DOI

Hawksworth D. L., Honegger R. (1994). “The lichen thallus: a symbiotic phenotype of nutritionally specialized fungi and its response to gall producers,” in

Helms G., Friedl T., Rambold G. (2003). Phylogenetic relationships of the physciaceae inferred from rDNA sequence data and selected phenotypic characters. PubMed DOI

Hillis D. M., Bull J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis.

Jackson D. A. (1993). Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. DOI

Jüriado I., Kaasalainen U., Jylhä M., Rikkinen J. (2019). Relationships between mycobiont identity, photobiont specificity and ecological preferences in the lichen genus DOI

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. PubMed PMC

Katoh K., Misawa K., Kuma K., Miyata T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. PubMed DOI PMC

Katoh K., Toh H. (2008). Recent developments in the MAFFT multiple sequence alignment program. PubMed DOI

Khakhina L. N., Margulis L., McMenamin M. (1993).

Kosecka M., Jabłońska A., Flakus A., Rodriguez-Flakus P., Kukwa M., Guzow-Krzemińska B. (2020). Trentepohlialean algae (Trentepohliales, Ulvophyceae) show preference to selected mycobiont lineages in lichen symbioses. PubMed DOI

Kroken S., Taylor J. W. (2000). Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus 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 PubMed DOI

Leavitt S. D., Kraichak E., Vondrak J., Nelsen M. P., Sohrabi M., Pérez-Ortega S., et al. (2016). Cryptic diversity and symbiont interactions in rock-posy lichens. PubMed DOI

Lefeuvre P. (2018).

Lücking R., Hodkinson B. P., Leavitt S. D. (2017). The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – approaching one thousand genera.

Magain N., Miadlikowska J., Goffinet B., Sérusiaux E., Lutzoni F. (2017). Macroevolution of specificity in cyanolichens of the genus Peltigera section polydactylon (Lecanoromycetes, Ascomycota). PubMed DOI

Mark K., Laanisto L., Bueno C. G., Niinemets Ü, Keller C., Scheidegger C. (2020). Contrasting co-occurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. PubMed DOI

Miadlikowska J., Kauff F., Hofstetter V., Fraker E., Grube M., Hafellner J., 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. PubMed DOI

Miller M., Pfeiffer W., Schwartz T. (2011). “CIPRES science gateway: a community resource for phylogenetic analyses,” in

Molina M. C., Divakar P. K., Millanes A. M., Sanchez E., Del-Prado R., Hawksworth D. L., et al. (2011a). DOI

Molina M. C., Del-Prado R., Divakar P. K., Sánchez-Mata D., Crespo A. (2011b). Another example of cryptic diversity in lichen-forming fungi: the new species DOI

Molina M. C., Divakar P. K., Goward T., Millanes A. M., Lumbsch H. T., Crespo A. (2017). Neogene diversification in the temperate lichen-forming fungal genus DOI

Molina M. D., Crespo A., Blanco O., Lumbsch H. T., Hawksworth D. L. (2004). Phylogenetic relationships and species concepts in

Molins A., Moya P., Muggia L., Barreno E. (2021). Thallus growth stage and geographic origin shape microalgal diversity in Ramalina farinacea lichen holobionts. PubMed DOI

Monaghan M. T., Wild R., Elliot M., Fujisawa T., Balke M., Inward D. J. G., et al. (2009). Accelerated species inventory on Madagascar using coalescent-based models of species delineation. PubMed DOI

Moya P., Chiva S., Molins A., Garrido-Benavent I., Barreno E. (2021). Unravelling the symbiotic microalgal diversity in Buellia zoharyi (lichenized Ascomicota) from the Iberian Peninsula and Balearic Islands using DNA Metabarcoding. DOI

Moya P., Chiva S., Molins A., Jadrná I., Škaloud P., Peksa O., et al. (2018). Myrmecia israeliensis as the primary symbiotic microalga in squamulose lichens growing in European and Canary Island terricolous communities. DOI

Moya P., Molins A., Chiva S., Bastida J., Barreno E. (2020). Symbiotic microalgal diversity within lichenicolous lichens and crustose hosts on Iberian Peninsula gypsum biocrusts. PubMed DOI PMC

Moya P., Molins A., Martínez-Alberola F., Muggia L., Barreno E. (2017). Unexpected associated microalgal diversity in the lichen PubMed DOI PMC

Muggia L., Grube M. (2018). Fungal diversity in lichens: from extremotolerance to interactions with algae. PubMed DOI PMC

Muggia L., Leavitt S., Barreno E. (2018). The hidden diversity of lichenised Trebouxiophyceae (Chlorophyta). DOI

Muggia L., Nelsen M., Kirika P. M., Barreno E., Beck A., Lindgren H., et al. (2020). Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus PubMed DOI

Muggia L., Pérez-Ortega S., Fryday A., Spribille T., Grube M. (2014). Global assessment of genetic variation and phenotypic plasticity in the lichen-forming species DOI

Muggia L., Vančurová L., Škaloud P., Peksa O., Wedin M., Grube M. (2013). The symbiotic playground of lichen thalli – a highly flexible photobiont association in rock-inhabiting lichens. PubMed DOI

Nash T. H. (2008).

Nelsen M. P. (2021). Sharing and double-dating in the lichen world. PubMed DOI

Nelsen M. P., Gargas A. (2009). Symbiont flexibility in DOI

O’Brien H. E., Miadlikowska J., Lutzoni F. (2013). Assessing population structure and host specialization in lichenized cyanobacteria. PubMed DOI

Oksanen J., Blanchet F. G., Friendly M., Kindt R., Legendre P., Mcglinn D., et al. (2017).

Ossowska E., Guzow-Krzemińska B., Kolanowska M., Szczepańska K., Kukwa M. (2019). Morphology and secondary chemistry in species recognition of PubMed DOI PMC

Otálora M. A., Aragón G., Martínez I., Wedin M. (2013). Cardinal characters on a slippery slope – a re-evaluation of phylogeny, character evolution, and evolutionary rates in the jelly lichens (Collemataceae s. str). PubMed DOI

Otálora M. A., Martínez I., O’Brien H., Molina M. C., Aragón G., Lutzoni F. (2010). Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). PubMed DOI

Pardo-De la Hoz C. J., Magain N., Lutzoni F., Goward T., Restrepo S., Miadlikowska J. (2018). Contrasting symbiotic patterns in two closely related lineages of trimembered lichens of the genus PubMed DOI PMC

Peksa O., Škaloud P. (2011). Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga PubMed DOI

Piercey-Normore M. D. (2004). Selection of algal genotypes by three species of lichen fungi in the genus

Piercey-Normore M. D., DePriest P. T. (2001). Algal switching among lichen symbioses. PubMed DOI

Pino-Bodas R., Stenroos S. (2020). Global biodiversity patterns of the photobionts associated with the genus PubMed DOI PMC

Printzen C., Domaschke S., Fernández-Mendoza F., Pérez-Ortega S. (2013). Biogeography and ecology of DOI

R Core Team (2013).

Rambaut A. (2012).

Rambaut A., Drummond A. J., Xie D., Baele G., Suchard M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. PubMed DOI PMC

Řídká T., Peksa O., Rai H., Upreti D. K., Škaloud P. (2014). “Photobiont diversity in Indian DOI

Rivas-Martínez S., Penas Á, del Río S., González T. E. D., Rivas-Sáenz S. (2017). “Bioclimatology of the Iberian Peninsula and the Balearic Islands,” in 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. PubMed DOI PMC

Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., et al. (2012). MrBayes 3 2, efficient Bayesian phylogenetic inference and model choice across a large model space. PubMed DOI PMC

Sadowska-Deś A. D., Dal Grande F., Lumbsch H. T., Beck A., Otte J., Hur J. S., et al. (2014). Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont PubMed DOI

Sayers E. W., Barrett T., Benson D. A., Bolton E., Bryant S. H., Canese K., et al. (2011). Database resources of the national center for biotechnology information. PubMed PMC

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. PubMed DOI

Smith C. W., Aptroot A., Coppins B. J., Fletcher A., Gilbert O. L., James P. W., et al. (2009).

Sork V. L., Werth S. (2014). Phylogeography of Ramalina menziesii, a widely distributed lichen-forming fungus in western North America. PubMed DOI

Stamatakis A. (2006). RAxML-VI-HPC, maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. PubMed DOI

Stamatakis A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. PubMed DOI PMC

Stamatakis A., Hoover P., Rougemont J. (2008). A rapid bootstrap algorithm for the RAxML web servers. PubMed DOI

Steinová J., Škaloud P., Yahr R., Bestová H., Muggia L. (2019). Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in 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 PubMed DOI

White T. J., Bruns T., Lee S., Taylor J. (1990). “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in DOI

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. PubMed DOI

Xu M., De Boer H., Olafsdottir E. S., Omarsdottir S., Heidmarsson S. (2020). Phylogenetic diversity of the lichenized algal genus DOI

Yahr R., Vilgalys R., Depriest P. T. (2004). Strong fungal specificity and selectivity for algal symbionts in Florida scrub PubMed DOI

Yahr R., Vilgalys R., DePriest P. T. (2006). Geographic variation in algal partners of PubMed DOI

The application of haplotypes instead of species-level ranks modifies the interpretation of ecological preferences in lichen symbiont interactions in Parmelia