Analyses of trait evolution and diversification reveal multiple adaptive periods in the fungal order Hymenochaetales

Abstract

Mushroom-forming fungi (Agaricomycetes) represent one of the most speciose and morphologically diverse life forms, which radiated into most niches on Earth and evolved diverse morphologies and life histories. The order Hymenochaetales comprises a species-rich group of important wood decayers and tree parasites, however, patterns of macroevolution across the order and thus the origins of key traits, such as pathogenicity are currently unknown. Here, using a novel, nearly comprehensive phylogeny of the Hymenochaetales, we show that its evolution has been shaped by an early adaptive period, followed by a general rate slowdown interrupted by local rapid radiations in the Cretaceous. We inferred that the ancestor of the order has undergone rapid phenotypic diversification into a range of morphologies and lifestyles, of which crust-like morphologies and pileate-sessile forms typical of bracket-fungi became dominant among extant taxa. Net diversification rate showed significant correlations with paleoclimate, morphological and ecological traits, however, teasing apart the contributions of individual clades revealed that these were mostly driven by the Mid-late Cretaceous rapid radiation of the genus Phylloporia, a diverse group of plant parasites. Together, this study unraveled a complex evolutionary history of the Hymenochaetales and uncovered novel patterns of phenotype evolution and diversification in mushroom-forming fungi.