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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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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for initiating the first phase of this project; U. Søchting, J. Spatafora, J. Johnson and S. LaGreca for providing unpublished sequences; J. Bélisle for assistance with Figs 1 and 2; J. Crodian for technical assistance; I. Brodo, D. Gernandt, C. Keller, T. Lumbsch, J. Miadlikowska, J.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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