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Major fungal lineages are derived from lichen symbiotic ancestors

Nature volume 411, pages 937–940 (2001)Cite this article

Abstract

About one-fifth of all known extant fungal species form obligate symbiotic associations with green algae, cyanobacteria or with both photobionts. These symbioses, known as lichens, are one way for fungi to meet their requirement for carbohydrates1,2. Lichens are widely believed to have arisen independently on several occasions, accounting for the high diversity and mixed occurrence of lichenized and non-lichenized (42 and 58%, respectively) fungal species within the Ascomycota3,4. Depending on the taxonomic classification chosen2,5,6, 15–18 orders of the Ascomycota include lichen-forming taxa, and 8–11 of these orders (representing about 60% of the Ascomycota species) contain both lichenized and non-lichenized species. Here we report a phylogenetic comparative analysis of the Ascomycota, a phylum that includes greater than 98% of known lichenized fungal species5. Using a Bayesian phylogenetic tree sampling methodology7,8 combined with a statistical model of trait evolution9, we take into account uncertainty about the phylogenetic tree and ancestral state reconstructions. Our results show that lichens evolved earlier than believed, and that gains of lichenization have been infrequent during Ascomycota evolution, but have been followed by multiple independent losses of the lichen symbiosis. As a consequence, major Ascomycota lineages of exclusively non-lichen-forming species are derived from lichen-forming ancestors. These species include taxa with important benefits and detriments to humans, such as Penicillium and Aspergillus10,11,12.

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Figure 1: The rate of loss of lichenization exceeds the rate of gain of lichenization, independently of tree topology.
Figure 2: Bayesian posterior probabilities for reconstructed evolution of the lichen symbiosis and for each node of the Ascomycota phylogeny.

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References

  1. Hawksworth, D. L. The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol. Res. 95, 641–655 (1991).

    Article  Google Scholar 

  2. Hawksworth, D. L., Kirk, P. M., Sutton, B. C. & Pegler, D. N. Dictionary of the Fungi (CAB, Wallingford, 1995).

    Google Scholar 

  3. Barinaga, M. Origins of lichen fungi explored. Science 268, 1437 (1995).

    Article  ADS  CAS  Google Scholar 

  4. Gargas, A., DePriest, P. T., Grube, M. & Tehler, A. Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny. Science 268, 1492–1495 (1995).

    Article  ADS  CAS  Google Scholar 

  5. Honegger, R. in Lichen Biology (ed. Nash, T. H.) 24–36 (Cambridge Univ. Press, Cambridge, 1996).

    Google Scholar 

  6. Hafellner, J. in Handbook of Lichenology Vol. 3 (ed. Galun, M.) 41–52 (CRC, Boca Raton, 1988).

    Google Scholar 

  7. Larget, B. & Simon, D. L. Markov chain monte carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol. Biol. Evol. 16, 750–759 (1999).

    Article  CAS  Google Scholar 

  8. Huelsenbeck, J. P., Rannala, B. & Masly, J. P. Accomodating phylogenetic uncertainty in evolutionary studies. Science 288, 2349–2350 (2000).

    Article  ADS  CAS  Google Scholar 

  9. Pagel, M. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48, 612–622 (1999).

    Article  Google Scholar 

  10. Berbee, M. L., Yoshimura, A., Sugiyama, J. & Taylor, J. W. Is Penicillium monophyletic? An evaluation of phylogeny in the family Trichocomaceae from 18S, 5.8S, and ITS ribosomal DNA sequence data. Mycologia 87, 210–222 (1995).

    Article  CAS  Google Scholar 

  11. Alexopoulos, C. J., Mims, C. W. & Blackwell, M. Introductory Mycology (John Wiley & Sons, New York, 1996).

    Google Scholar 

  12. Suh, S.-O. & Blackwell, M. Molecular phylogeny of the cleistothecial fungi placed in Cephalothecaceae and Pseudeurotiaceae. Mycologia 91, 836–848 (1999).

    Article  CAS  Google Scholar 

  13. Berbee, M. L. & Taylor, J. W. From 18S ribosomal sequence data to evolution of morphology among the fungi. Can. J. Bot. (Suppl. 1) 73, S677–S683 (1995).

    Article  CAS  Google Scholar 

  14. Spatafora, J. W. Ascomal evolution of filamentous ascomycetes: evidence from molecular data. Can. J. Bot. (Suppl. 1) 73, S811–S815 (1995).

    Article  CAS  Google Scholar 

  15. Berbee, M. L., Carmean, D. A. & Winka, K. Ribosomal DNA and resolution of branching order among the Ascomycota: how many nucleotides are enough? Mol. Phyl. Evol. 17, 337–344 (2000).

    Article  CAS  Google Scholar 

  16. Bhattacharya, D. et al. Widespread occurrence of spliceosomal introns in the rDNA genes of ascomycetes. Mol. Biol. Evol. 17, 1971–1984 (2000).

    Article  CAS  Google Scholar 

  17. Liu, Y. J., Whelen, S. & Hall, B. D. Phylogenetic relationships among ascomycetes: evidence from the RNA polymerase II subunit. Mol. Biol. Evol. 16, 1799–1808 (1999).

    Article  CAS  Google Scholar 

  18. Collins, T. M., Wimberger, P. H. & Naylor, G. J. P. Compositional bias, character-state bias, and character-state reconstruction using parsimony. Syst. Biol. 43, 482–496 (1994).

    Article  Google Scholar 

  19. Maddison, D. R. Phylogenetic methods for inferring the evolutionary history and process of change in discretely valued characters. Ann. Rev. Entomol. 39, 267–292 (1994).

    Article  Google Scholar 

  20. Pagel, M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255, 37–45 (1994).

    Article  ADS  Google Scholar 

  21. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).

    Article  ADS  CAS  Google Scholar 

  22. Elix, J. A. in Lichen Biology (ed. Nash, T. H.) 154–180 (Cambridge Univ. Press, Cambridge, 1996).

    Google Scholar 

  23. Rambold, G. & Triebel, D. The inter-lecanoralean associations. Bibliotheca Lichenologica 48, 1–201 (1992).

    Google Scholar 

  24. Hibbett, D. S., Gilbert, L.-B. & Donoghue, M. J. Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407, 506–508 (2000).

    Article  ADS  CAS  Google Scholar 

  25. Lutzoni, F. & Vilgalys, R. Omphalina (Basidiomycota, Agaricales) as a model system for the study of coevolution in lichenized fungi. Crypt. Bot. 5, 82–97 (1995).

    Google Scholar 

  26. Lutzoni, F. Phylogeny of lichen- and non lichen-forming omphalinoid mushrooms and the utility of testing for combinability among multiple data sets. Syst. Biol. 46, 373–406 (1997).

    Article  CAS  Google Scholar 

  27. Lutzoni, F. & Pagel, M. Accelerated evolution as a consequence of transition to mutualism. Proc. Natl Acad. Sci. USA 94, 11422–11427 (1997).

    Article  ADS  CAS  Google Scholar 

  28. Kranner, I. & Lutzoni, F. in Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganization (ed. Lerner, H. R.) 591–628 (Marcel Dekker, New York, 1999).

    Google Scholar 

  29. Wilson, I. & Balding, D. Genealogical inference from microsatellite data. Genetics 150, 499–510 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Hillis, D. M., Moritz, C. & Mable, B. K. Molecular Systematics 2nd edn (Sinauer, Sunderland, 1996).

    Google Scholar 

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Acknowledgements

We thank P. Lewis and K. Pryer for insightful suggestions; J. Spatafora, D. Armaleo, C. and W. Culberson for initiating the first phase of this project; U. Søchting, J. Spatafora, J. Johnson and S. LaGreca for providing unpublished sequences; J. Bélisle for assistance with Figs 1 and 2; J. Crodian for technical assistance; I. Brodo, D. Gernandt, C. Keller, T. Lumbsch, J. Miadlikowska, J. Platt and U. Søchting for providing lichen material or DNA samples; F. Kauff, T. Bjelland, B. Büdel, P. M. Jørgensen and M. Schultz for the identification of some lichen specimens; and M. Blackwell for comments on the manuscript. This work was supported by a grant from the US National Science Foundation to F.L. and the Pritzker Foundation Fund of The Field Museum. M.P. is supported by the Leverhulme Trust and the Biotechnology and Biological Sciences Research Council of the UK.

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  1. François Lutzoni & Valérie Reeb

    Present address: Department of Biology, Duke University, Durham, North Carolina, 27708, USA

Authors and Affiliations

  1. Department of Botany, The Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, 60605, Illinois, USA

    François Lutzoni & Valérie Reeb

  2. School of Animal and Microbial Sciences, University of Reading, Whiteknights, RG6 6AJ, Reading, UK

    Mark Pagel

  3. Department of Biological Sciences, University of Illinois at Chicago (M/C 066), Chicago, 60607, Illinois, USA

    Valérie Reeb

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Correspondence to François Lutzoni.

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Lutzoni, F., Pagel, M. & Reeb, V. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411, 937–940 (2001). https://doi.org/10.1038/35082053

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