Impact of model assumptions on the inference of the evolution of ectomycorrhizal symbiosis in fungi.

Ectomycorrhiza (ECM) is a symbiotic relation between plant and fungi that is essential for nutrient uptake of many stand forming trees. There are two conflicting views about the evolution of ECM in fungi suggesting (1) relatively few transitions to ECM followed by reversals to non-ECM, or (2) many independent origins of ECM and no reversals. In this study, we compare these, and other, hypotheses and test the impact of different models on inference. We assembled a dataset of five marker gene sequences (nuc58, nucLSU, nucSSU, rpb1, and rpb2) and 2,174 fungal taxa covering the three subphyla: Agaricomycotina, Mucoromycotina and Pezizomycotina. The fit of different models, including models with variable rates in clades or through time, to the pattern of ECM fungal taxa was tested in a Bayesian framework, and using AIC and simulations. We find that models implementing variable rates are a better fit than models without rate shift, and that the conclusion about the relative rate between ECM and non-ECM depend largely on whether rate shifts are allowed or not. We conclude that standard constant-rate ancestral state reconstruction models are not adequate for the analysis of the evolution of ECM fungi, and may give contradictory results to more extensive analyses.

Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi.

With ∼36,000 described species, Agaricomycetes are among the most successful groups of Fungi. Agaricomycetes display great diversity in fruiting body forms and nutritional modes. Most have pileate-stipitate fruiting bodies (with a cap and stalk), but the group also contains crust-like resupinate fungi, polypores, coral fungi, and gasteroid forms (e.g., puffballs and stinkhorns). Some Agaricomycetes enter into ectomycorrhizal symbioses with plants, while others are decayers (saprotrophs) or pathogens. We constructed a megaphylogeny of 8,400 species and used it to test the following five hypotheses regarding the evolution of morphological and ecological traits in Agaricomycetes and their impact on diversification: 1) resupinate forms are plesiomorphic, 2) pileate-stipitate forms promote diversification, 3) the evolution of gasteroid forms is irreversible, 4) the ectomycorrhizal (ECM) symbiosis promotes diversification, and 5) the evolution of ECM symbiosis is irreversible. The ancestor of Agaricomycetes was a saprotroph with a resupinate fruiting body. There have been 462 transitions in the examined morphologies, including 123 origins of gasteroid forms. Reversals of gasteroid forms are highly unlikely but cannot be rejected. Pileate-stipitate forms are correlated with elevated diversification rates, suggesting that this morphological trait is a key to the success of Agaricomycetes. ECM symbioses have evolved 36 times in Agaricomycetes, with several transformations to parasitism. Across the entire 8,400-species phylogeny, diversification rates of ectomycorrhizal lineages are no greater than those of saprotrophic lineages. However, some ECM lineages have elevated diversification rates compared to their non-ECM sister clades, suggesting that the evolution of symbioses may act as a key innovation at local phylogenetic scales.