Host jumping onto close relatives and across kingdoms by Tyrannicordyceps (Clavicipitaceae) gen. nov. and Ustilaginoidea_(Clavicipitaceae).

PREMISE OF STUDY: This research seeks to advance understanding of conditions allowing movement of fungal pathogens among hosts. The family Clavicipitaceae contains fungal pathogens exploiting hosts across three kingdoms of life in a pattern that features multiple interkingdom host shifts among plants, animals, and fungi. The tribe Ustilaginoideae potentially represents a third origin of plant pathogenesis, although these species remain understudied. Fungal pathogens that cause ergot are linked morphologically with Clavicipitaceae, but are not yet included in phylogenetic studies. The placement of Ustilaginoideae and ergot pathogens will allow differentiation between the host habitat and host relatedness hypotheses as mechanisms of phylogenetic diversification of Clavicipitaceae.
METHODS: A multigene data set was assembled for Clavicipitaceae to test phylogenetic placement and ancestral character-state reconstructions for Ustilaginoidea virens and U. dichromonae as well as the ergot mycoparasite Cordyceps fratricida. Microscopic morphological observations of sexual and asexual states were also performed. KEY
RESULTS: Phylogenetic placement of U. virens and U. dichromonae represents a third acquisition of the plant pathogenic lifestyle in Clavicipitaceae. Cordyceps fratricida was also placed in Clavicipitaceae and recognized as a new genus Tyrannicordyceps. Ancestral character state reconstructions indicate initially infecting hemipteran insect hosts facilitates subsequent changes to a plant pathogenic lifestyle. The ancestor of T. fratricida is inferred to have jumped from grasses to pathogens of grasses.
CONCLUSIONS: The host habitat hypothesis best explains the dynamic evolution of host affiliations seen in Clavicipitaceae and throughout Hypocreales. Co-occurrence in the same habitat has allowed for host shifts from animals to plants, and from plants to fungi.