Megaphylogeny resolves global patterns of mushroom evolution

Abstract

Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfill diverse roles in the ecosystem, including wood decomposers, pathogens or mycorrhizal mutualists. Despite the importance of mushroom-forming fungi, large-scale patterns of their evolutionary history are poorly known, in part due to the lack of a comprehensive and dated molecular phylogeny. Here, using multigene and genome-based data, we assemble a 5,284-species phylogenetic tree and infer ages and broad patterns of speciation/extinction and morphological innovation in mushroom-forming fungi. Agaricomycetes started a rapid class-wide radiation in the Jurassic, coinciding with the spread of (sub)tropical coniferous forests and a warming climate. A possible mass extinction, several clade-specific adaptive radiations, and morphological diversification of fruiting bodies followed during the Cretaceous and the Paleogene, convergently giving rise to the classic toadstool morphology, with a cap, stalk, and gills (pileate-stipitate morphology). This morphology is associated with increased rates of lineage diversification, suggesting it represents a key innovation in the evolution of mushroom-forming fungi. The increase in mushroom diversity started during the Mesozoic-Cenozoic radiation event, an era of humid climate when terrestrial communities dominated by gymnosperms and reptiles were also expanding.

Mycena genomes resolve the evolution of fungal bioluminescence

“…Phylogeny reconstruction suggested that luciferase originated in early Agaricales. Armillaria and Omphalotus belong to the marasmioid clade, whereas Mycena was recently found to be sister of the marasmioid clade 7 . Recent genome sequencing efforts in the marasmioid clade revealed diverse genomic and life history traits, including genome expansion and pathogenicity in Armillaria spp.…”

Complementary molecular methods reveal comprehensive phylogenetic diversity integrating inconspicuous lineages of early-diverged wood-decaying mushrooms

“…harbour inconspicuous thin resupinate basidiocarps 29,31,34,35 . Other mushroom-forming basidiomycetes, Agaricomycetes, and Tremellomycetes, which constitute Agaricomycotina with Dacrymycetes, display variously shaped fruiting bodies, such as stipitate agaricoid, coralloid, and corticoid fruiting bodies, yet their early-diverged lineages tend to feature inconspicuous small or thin fruiting bodies 1,3 . These classes contain species that play ecologically significant roles, e.g.…”

“…Moreover, the taxon is a noteworthy lineage for studying the evolution of wood-decaying mushrooms. Dacrymycetes species are considered to represent an ancestral lineage of wood-decaying basidiomycetes that diverged approximately 350 million years ago 1,28,29 and brown rot fungi that are critical for understanding the early evolution of fungal wood decomposers 30 . Diversity surveys and phylogenetic analyses of Dacrymycetes have been conducted primarily based on visible fruiting bodies [29][30][31][32] .…”

How important is it to consider lineage diversification heterogeneity in in macroevolutionary studies: lessons from the lizard family Liolaemidae

“…Even though models that do not include hidden states are not suitable for trees including groups with heterogeneous diversification patterns, they are still commonly applied in macroevolutionary studies without careful assessment. For instance, the Geographic State Speciation and Extinction model (GeoSSE; Goldberg et al 2011) was recently used in biogeographic studies of lizards (Esquerré et al 2019), tanagers and tortoises (Román-Palacios and Wiens 2018), plants (Canal et al 2019), including palms (Bacon et al 2018) and oaks (Hipp et al 2018), and a recent mega-phylogeny of mushrooms (Varga et al 2019). Given the above-noted limitations of this model, these empirical cases should be revisited (e.g.…”