Systematics and phylogeny of Cordyceps and the Clavicipitaceae with emphasis on the evolution of host affiliation.

摘要

Cordyceps is a genus of perithecial ascomycetes. It includes over 400 species that are pathogens of arthropods and parasites of the truffle genus Elaphomyces. Based on the morphology of cylindrical asci, thickened ascus apices and filiform ascospores, it is classified in the Clavicipitaceae (Hypocreales), which also includes endophytes and epiphytes of the grass family (e.g., Claviceps and Epichloe). Multi-gene phylogenetic analyses rejected the monophyly of the Clavicipitaceae. Clavicipitaceous fungi formed three strongly supported clades of which one was monophyletic with the Hypocreaceae. Furthermore, the monophyly of Cordyceps was also rejected as all three clades of Clavicipitaceae included species of the genus. These results did not support the utility of most of the characters (e.g., ascospore morphology and host affiliation) used in current classifications and warranted significant taxonomic revisions of both Cordyceps and the Clavicipitaceae. Therefore, taxonomic revisions were made to more accurately reflect phylogenetic relationships. One new family Ophiocordycipitaceae was proposed and two families (Clavicipitaceae and Cordycipitaceae) were emended for the three clavicipitaceous clades. Species of Cordyceps were reclassified into Cordyceps sensu stricto, Elaphocordyceps gen. nov., Metacordyceps gen. nov., and Ophiocordyceps and a total of 147 new combinations were proposed. In teleomorph-anamorph connection, the phylogeny of the Clavicipitaceae s. l. was also useful in characterizing the polyphyly of Verticillium sect. Prostrata and in integrating the following major anamorphic genera with their teleomorphic genera in a new classification system (teleomorphic genera: anamorphic genera): Cordyceps: Beauveria, Lecanicillium, Isaria; Hypocrella: Aschersonia; Metacordyceps: Metarhizium, Pochonia; Ophiocordyceps: Hirsutella, Hymenostilbe . In addition to multi-gene phylogenetic analyses, phylogenetic dating and ancestral host state reconstruction were conducted to understand the evolution of host affiliation in Clavicipitaceae s. l. and the Hypocreales. These analyses suggested that fungal-animal symbioses of the Clavicipitaceae s. l. initiated in the Jurassic by a series of inter-kingdom host jumps from plant-based nutrition to animal pathogens. A total of 9-14 inter-kingdom host jumps were hypothesized for the Clavicipitaceae s. l., including 5-7 onto fungi, 2-4 onto animals, and 2-3 onto plants, with dominant ecology as pathogens of arthropods. The total evidence of the Cretaceous radiation of the Clavicipitaceae s. l. indicated that the current diversity of its fungal-arthropod symbioses may be correlated with the coevolutionary interactions between arthropods and angiosperms in the Cretaceous.