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

Significance

The Agaricomycetes is a conspicuous and successful group of Fungi, containing ∼36,000 described species. The group presents striking diversity in fruiting bodies, including those with a pileus (cap) and stipe (stalk), puffballs, coral fungi, crust-like forms, etc. Agaricomycetes also comprise ecologically diverse species, including decayers, mycorrhizal symbionts, and pathogens. We assembled a “megaphylogeny” with 8,400 species that represent ∼23% of the known diversity of Agaricomycetes and used it to investigate the relative impact of fruiting body forms and nutritional modes on diversification rates. Across all Agaricomycetes, a pileate-stipitate fruiting body is associated with increased diversification compared to other forms. No such relationship was found for nutritional modes, including mycorrhizal symbiosis. We conclude that morphological innovation has driven diversification in Agaricomycetes.

Abstract

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.