Scale-dependent co-occurrence patterns of closely related genotypes in a lichen species complex

Abstract

The ‘competition-relatedness’ hypothesis postulates that co-occurring taxa should be more distantly related, because of lower competition. This hypothesis has been criticized for its dependence on untested assumptions and its exclusion of other assembly forces beyond competition and habitat filtering to explain the co-existence of closely related taxa. Here we analyzed the patterns of co-occurring individuals of lichenized fungi in the Graphis scripta complex, a monophyletic group of species occurring in temperate forests throughout the Northern Hemisphere. We generated sequences for three nuclear ribosomal and protein markers (nuLSU, RPB2, EF-1) and combined them with previously generated sequences to reconstruct an updated phylogeny for the complex. The resulting phylogeny was used to determine the patterns of co-occurrences at regional and at sample (tree) scales by calculating standard effect size of mean pairwise distance (SES.MPD) among co-occurring samples to determine whether they were more clustered than expected from chance. The resulting phylogeny revealed multiple distinct lineages, suggesting the presence of several phylogenetic species in this complex. At the regional and local (site) levels, SES.MPD exhibited significant clustering for five out of six regions. The sample (tree) scale SES. MPD values also suggested some clustering but the corresponding metrics did not deviate significantly from the null expectation. The differences in the SES.MPD values and their significance indicated that habitat filtering and/or local diversification may be operating at the regional level, while the local assemblies on each tree are interpreted as being the result of local competition or random colonization.

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  • Acharius, E. 1809. Förteckning pa de i Sverige växande arter af Lafvarnes famille. Kongliga Vetenskaps Academiens Nya Handlingar 30: 145–169.

  • Alexandrou, M. A., Cardinale, B. J., Hall, JD., Delwiche, C. F., Fritschie, K., Narwani, A., Venail, P. A., Bentlage, B., Pankey, M. S. & Oakley, T. H. 2014. Evolutionary relatedness does not predict competition and co-occurrence in natural or experimental communities of green algae. Proceedings of The Royal Society B: Biological Science 282(1799): 20141745.

  • Armstrong, R. A. 1986. Competition between three lichen species using a factorial experimental design. New Phytologist 104: 637–641.

  • Armstrong, R. A. & Bradwell, T. 2010. Growth of crustose lichens: A review. Geografiska Annaler, Series A: Physical Geography 92: 3–17.

  • Armstrong, R. A., & Welch, A. R. 2007. Competition in lichen communities. Symbiosis 43: 1–12.

  • Bolliger, J., Bergamini, A., Stofer, S., Kienast, F. & Scheidgger, C. 2007 Predicting the potential spatial distributions of epiphytic lichen species at the landscape level. The Lichenologist 39: 279–291.

  • Bowker, M. A. & Maestre, F. T. 2012. Inferring local competition intensity from patch size distributions: A test using biological soil crusts. Oikos 121: 1914–1922.

  • Burns, J. H. & Strauss, S. Y. 2011. More closely related species are more ecologically similar in an experimental test. Proceedings of the National Academy of Sciences of the United States of America 108: 5302–5307.

  • Cahill, J. F., Kembel, S. W., Lamb, E. G. & Keddy, P. A. 2008. Does phylogenetic relatedness influence the strength of competition among vascular plants? Perspectives in Plant Ecology, Evolution and Systematics 10: 41–50.

  • Cavender-Bares, J., Keen, A. & Miles, B. 2006 Phylogenetic structure of floridian plant communities depends on taxonomic and spatial scale. Ecology 87: S109–S122.

  • Cavender-Bares J., Kozak, K. H., Fine, P. V. A. & Kembel, S. W. 2009. The merging of community ecology and phylogenetic biology. Ecology Letters 12: 693–715.

  • Cooper, N., Rodriguez, J. & Purvis, A. 2008. A common tendency for phylogenetic overdispersion in mammalian assemblages. Proceedings of The Royal Society B: Biological Science 275: 2031–2037.

  • Darwin, C. 1859. On the Origin of the Species. John Murray, London.

  • Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.

  • Gause, G. F. 1934. The Struggle for Existence. Williams and Wilkins, Baltimore.

  • Genet, A., Grabarnik, P., Sekretenko, O. & Pothier, D. 2014. Incorporating the mechanisms underlying inter-tree competition into a random point process model to improve spatial tree pattern analysis in forestry. Ecological Modelling 288: 143–154.

  • Gerhold, P., Cahill Jr., J. F., Winter, M., Bartish, I. V. & Prinzing, A. 2015. Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). Functional Ecology 29: 600–614.

  • Gnüchtel, A. 2014. Die Verbreitung der Arten des Graphis scripta-Komplexes in Sachsen und den angrenzenden Gebieten Nordböhmens. Sächsische Floristische Mitteilungen 16: 58–64.

  • Herben, T. & Goldberg, D. E. 2014. Community assembly by limiting similarity vs. competitive hierarchies: testing the consequences of dispersion of individual traits. Journal of Ecology 102: 156–166.

  • Horner-Devine, M. & Bohannan, B. J. M. 2006. Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87: S100–S108.

  • Huelsenbeck, J. P. & Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.

  • John, E. & Dale, M. R. T. 1989. Niche relationships amongst Rhizocarpon species at Jonas Rockslide, Alberta, Canada. The Lichenologist 21: 313–330.

  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., et al. 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

  • Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., Blomberg, S. P. & Webb, C. O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463–1464.

  • Kembel, S. & Hubbell, S. P. 2006. The phylogenetic structure of a Neotropical forest tree community. Ecology 87: S86–S99.

  • Kraft, N. J. B. & Ackerly, D. D. 2010. Functional trait and phylogenetic tests of community assembly across spatial scales in an Amazonian forest. Ecological Monographs 80: 401–422.

  • Kraichak, E., Lücking, R., Aptroot, A., Beck, A., Dornes, P. et al. 2015. Hidden diversity in the morphologically variable script lichen (Graphis scripta) complex (Ascomycota, Ostropales, Graphidaceae). Organisms Diversity and Evolution 15: 447–458.

  • Lange, O. L. 1990. Twenty-three years of growth measurements on the crustose lichen Caloplaca aurantia in the central Negev Desert. Israel Journal of Botany 39: 383–394.

  • Lawrey, J. D. 1981. Evidence for competitive release in simplified saxicolous lichen communities. American Journal of Botany 68: 1066–1073.

  • Lindblom, L. & Ekman, S. 2006. Genetic variation and population differentiation in the lichen-forming ascomycete Xanthoria parietina on the island Storfosna, central Norway. Molecular Ecology 15: 1545–1559.

  • Linnaeus, C. 1753. Species Plantarum. Salvius, Stockholm.

  • Lücking, R. 2001. Lichens on leaves in tropical rainforests: life in a permanently ephemerous environment. Dissertationes Botanicae 346: 41–77.

  • Lücking, R. & Bernecker-Lücking A. 2002. Distance, dynamics, and diversity in tropical rainforests: an experimental approach using foliicolous lichens on artificial leaves. I. Growth performance and succession. Ecotropica 8: 1–13.

  • Lücking, R., Johnston, M. K., Aptroot, A., Kraichak, E., Lendemer, J. C. et al. 2014. One hundred and seventy-five new species of Graphidaceae: closing the gap or a drop in the bucket? Phytotaxa 189: 7–38.

  • Lücking, R., Villaseñor, J. L., Herrera-Campos, M. A., Pérez-Pérez, R. E., Egan, R. S. et al. 2016. Phylogenetic structure of meta-communities in Mexican Parmeliaceae (lichenized Ascomycota: Lecanorales). Bibliotheca Lichenologica 110: 27–54.

  • Lücking, R., Archer, A. W. & Aptroot, A. 2009. A world-wide key to the genus Graphis (Ostropales: Graphidaceae). The Lichenologist 41: 363–452.

  • MacArthur, R. H. & Levins, R. 1967 Limiting similarity convergence and divergence of coexisting species. American Naturalist 101, 377–385.

  • Miller, M. A., Pfeiffer, W. & Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE), 2010: 1–8.

  • Naughton, H. R., Alexandrou, M. A., Oakley, T. H., & Cardinale, B. J. 2015. Phylogenetic distance does not predict competition in green algal communities. Ecosphere 6: 1–19.

  • Neuwirth G. 2013. Der Graphis scripta-komplex in Oberösterreich. Stapfia 99: 61–74.

  • Neuwirth, G. & Aptroot, A. 2011. Recognition of Four Morphologically Distinct Species in the Graphis scripta Complex in Europe. Herzogia 24: 207–230.

  • Otte, V. 1999. Karten zur Flechtenverbreitung in Brandenburg: Graphis scripta (L.) Ach. und Pyrenula nitida (Weigel) Ach. Gleditschia 27: 139–146.

  • Paradis, E., Claude, J. & Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.

  • Pastore, A. I., Prather, C. M., Gornish, E. S., Ryan, W. H. & Ellis, R. D. 2014. Testing the competition-colonization trade-off with a 32-year study of a saxicolous lichen community. Ecology 95: 306–15.

  • Peterson, G., Allen, C. R. & Holling, C. S. 1998. Ecological resilience, biodiversity, and scale. Ecosystems 1: 6–18.

  • Printzen, C. & Ekman, S. 2003. Local population subdivision in the lichen Cladonia subcervicornis as revealed by mitochondrial cytochrome oxidase subunit 1 intron sequences. Mycologia 95: 399–406.

  • Rambaut A. 2012. FigTree. Version 1.4.4.

  • Rivas Plata, E., Parnmen, S., Staiger, B., Mangold, A., Frisch, A. et al. 2013. A molecular phylogeny of Graphidaceae (Ascomycota, Lecanoromycetes, Ostropales) including 428 species. MycoKeys 6: 55–94.

  • Schei, F. H., Blom, H. H., Gjerde, I., Grytnes, J-A., Heegaard, E. & Saetersdal, M. 2012. Fine-scale distribution and abundance of epiphytic lichens: environmental filtering or local dispersal dynamics? Journal of Vegetation Science 23: 459–470.

  • Sillett, S. C., McCune, B., Peck, J. L. E., Rambo T. R. & Ruchty, A. 2000. Dispersal limitations of epiphytic lichens result in species dependent on old-growth forests. Ecological applications 10: 789–799.

  • Slingsby, J. A. & Verboom, G. A. 2006. Phylogenetic relatedness limits co-occurrence at fine spatial scales: evidence from the schoenoid sedges (Cyperaceae: Schoeneae) of the Cape Floristic Region, South Africa. American Naturalist 168: 14–27.

  • Smith, A. B., Sandel, B. S., Kraft, N. J. B. & Carey, S. 2013. Characterizing scale-dependent community assembly using the functional-diversity-area relationship. Ecology 94: 2392–2402.

  • Stamatakis, A. 2006. RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics 22: 2688–2690.

  • Stamatakis, A., Hoover, P. & Rougemont, J. 2008. A Rapid Bootstrap Algorithm for the RAxML Web Servers. Systematic Biology 57: 758–771.

  • Swenson, N. G., Enquist, B. J., Pither, J., Thompson, J. & Zimmerman, J. K. 2006. The problem and promise of scale dependency in community phylogenetics. Ecology 87: 2418–2424.

  • Vamosi, S. M., Heard, S. B., Vamosi, J. C. & Webb, C. O. 2009. Emerging patterns in the comparative analysis of phylogenetic community structure. Molecular Ecology 18: 572–592.

  • Verdú, M. & Pausas, J. G. 2007. Fire drives phylogenetic clustering in Mediterranean Basin woody plant communities. Journal of Ecology 95: 1316–1323.

  • Violle, C., Nemergut, D. R., Pu, Z. & Jiang, L. 2011. Phylogenetic limiting similarity and competitive exclusion. Ecology Letters 14: 782–787.

  • Walser, J. C., Holderegger, R., Gugerli, F., Hoebee, S. E. & Scheidegger, C. 2005. Microsatellites reveal regional population differentiation and isolation in Lobaria pulmonaria, an epiphytic lichen. Molecular Ecology 14: 457–467.

  • Webb, C. O. 2000. Exploring the Phylogenetic Structure of Ecological Communities: An Example for Rain Forest Trees. American Naturalist 156: 145–155.

  • Webb, C. O., Ackerly, D. D. & Kembel, S. W. 2008. Phylocom: Software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24: 2098–2100.

  • Webb, C. O., Ackerly, D. D. & McPeek, M. A. 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33: 475–505.

  • Whiton, J. C., Lawrey, J. D. 1984. Inhibition of crustose lichen spore germination by lichen acids. The Bryologist 87: 42–43.

  • Wirth, V., Hauck, M. & Schultz, M. 2013. Die Flechten Deutschlands: Band 1 und 2. Ulmer, Stuttgart.

  • Yemets, O. A., Solhaug, K. A., Gauslaa, Y. 2014. Spatial dispersal of airborne pollutants and their effects on growth and viability of lichen transplants along a rural highway in Norway. The Lichenologist 46: 809–823.

  • Zahlbruckner, A. 1923. Catalogus lichenum universalis. Gebrüder Borntraeger: Leipzig.

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