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

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.

Keywords: Agaricomycetes; diversification; ectomycorrhizal fungi; gasteroid forms; megaphylogeny.

Fig. 1.

Examples of the basic fruiting body forms in Agaricomycetes. (A) Resupinate (Phanerochaete sp.). (B) Pileate-sessile (Ischnoderma resinosum). (C) Clavarioid-coralloid (Ramariopsis kunzei). (B and C) Image credit: Mike Wood (photographer). (D) Pileate-stipitate (Amanita diemii). (E) Gasteroid (Calostoma cinnabarinum).

Fig. 2.

(A–C) Macroevolutionary dynamics of fruiting body forms in Agaricomycetes. (D–F) Macroevolutionary dynamics of nutritional modes in Agaricomyctes. (A and D) Stochastic mapping of five fruiting body forms and four nutritional modes, respectively. The yellow dots indicate shifts in diversification rates according to BAMM. Only major orders of Agaricomycetes are labeled. (B and E) The posterior probability distributions of net diversification rates (speciation minus extinction) from the MuSSE model. The bar underneath each distribution represents the 95% credible interval obtained from the posterior distribution. (C and F) The number of average transitions between character states estimated from a set of 100 stochastic maps by SIMMAP and transition rates estimated by MuSSE (NA = not applicable). The absence of arrows between states indicates zero transitions as well as transition rates.