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.

Evolutionary priming and transition to the ectomycorrhizal habit in an iconic lineage of mushroom-forming fungi: is preadaptation a requirement?

“…The copyright holder for this preprint this version posted February 24, 2021. ; https://doi.org/10.1101/2021.02.23.432530 doi: bioRxiv preprint Comparative genomics of Russulales general ecological strategies, but adaptative functional specialization within ECM lineages is understudied and may be the key to understanding hyperdiversification and host dynamics within these groups (Looney et al 2018;Sánchez-García et al 2020). We hypothesize that niche partitioning is evident among ECM communities, with functional specialization followed by host switching driving diversification of ECM lineages.…”

“…The differential ability to scavenge nitrogen, phosphorus, and trace elements as key functions is mediated through these enzymes' ability to break down soil organic matter, which can be detected by the plant host to mediate and select for its mycorrhizal community (Hortal et al 2017). Traits that have been highlighted as potential drivers of diversification in ECM fungi have primarily looked at morphological traits of sexual reproduction and Comparative genomics of Russulales general ecological strategies, but adaptative functional specialization within ECM lineages is understudied and may be the key to understanding hyperdiversification and host dynamics within these groups (Looney et al 2018;Sánchez-García et al 2020). We hypothesize that niche partitioning is evident among ECM communities, with functional specialization followed by host switching driving diversification of ECM lineages.…”

“…ECM fungi have evolved from diverse ancestral trophic states, including white-rot saprotrophs, brown-rot saprotrophs, litter decomposers, and root endophytes, with each evolutionary history necessitating different selective pressures (Tedersoo & Smith 2013; Martin et al 2016; Pellitier & Zak 2018; Strullu-Derrien et al 2018; Miyauchi et al 2020). These evolutionary shifts in trophic strategy often led to specializations of function that contribute to changes in diversification rates that are defining for clades of fungi (Sánchez-García et al 2017; 2020; Lutzoni et al 2018).…”

The critical role of tree species and human disturbance in determining the macrofungal diversity in Europe

“…The majority of the macromycetes are in taxa from the phylum Basidiomycota, subphylum Agaricomycotina (Porter et al., 2008). The Agaricomycetes is a conspicuous group of fungi under the subphylum Agaricomycotina, presenting striking diversity in fruiting bodies and comprising ecologically diverse species with equally diverse functional roles (Sánchez‐García et al., 2020). There were seven orders under the Agaricomycetes class with a number of species ranking in the top 10 orders in our database, namely the Agaricales, Boletales, Cantharellales, Hymenochaetales, Polyporales, Russulales and Thelephorales.…”

Developmental innovations promote species diversification in mushroom-forming fungi

“…The most derived ones are called pileate-stipitate morphologies (mushrooms with cap and stalk), which evolved several times convergently and probably represent stable attractors in the morphospace (Hibbett, 2004, Varga et al 2019). Further, the emergence of complex morphologies correlate with higher diversification rates and may be a major driver of lineage diversification in mushroom-forming fungi (Agaricomycetes) (Sánchez-García et al, 2020; Varga et al, 2019). However, beyond the broadest morphological types, we know little about what drives the evolution of fruiting body morphologies and how novel fruiting body traits impact speciation and extinction patterns.…”