Advances in molecular systematics of clavicipitaceous fungi (Sordariomycetes: Hypocreales)

Graduation date: 2011Access restricted to the OSU Community at author's request from Dec. 17, 2010 - June 17, 2011.Historical concepts of Clavicipitaceae have included a broad range of species that display diverse morphologies, ecological modes and host associations. When subjected to multigene phylogenetic investigation of evolutionary history, the family was found to be polyphyletic, largely driven by diversity in the genus Cordyceps, previously containing over 400 taxa. The majority of Cordyceps sensu lato now resides in the families Cordycipitaceae, for which the genus Cordyceps has been retained owing to the placement of the type C. militaris, and the genera Ophiocordyceps and Elaphocordyceps in Ophiocordycipitaceae. The genus Metacordyceps was defined for species of Cordyceps remaining in Clavicipitaceae sensu stricto and contains relatively few species owing to convergent morphologies. Clavicipitaceae remains considerably diverse and its members attack hosts across three kingdoms of life, including insects and rotifers, plants and other fungi. There remains a significant number of Cordyceps species for which molecular or morphological data are insufficient, and are therefore considered incertae sedis with\ud regards to family until new material is available for examination. This work expands the sampling of taxa in Clavicipitaceae sensu lato for inclusion in phylogenetic reconstruction, with particular emphasis on residual species of Cordyceps. The resulting phylogenies were then used to refine concepts morphological features that define boundaries between taxa and explore the evolution of host association, morphology and ecology with ancestral character-state reconstruction.\ud Taxon sampling was increased by extensive field collections and collaborations with other researchers. The diversity present in newly acquired specimens represents all three pathogen groups. The inclusion of these taxa in a five-gene dataset (nrSSU, nrLSU, TEF, RPB1, RPB2) advances understanding of systematic relationships within Clavicipitaceae. Molecular data supports the movement of seven species from Cordyceps sensu lato to Metacordyceps, doubling the number of species known for the genus. The addition of new species reveals significant structure within the genus and allows for a reevaluation and strengthening of morphological concepts attributed to the genus. A clade of species sister to Clavicipitaceae was identified as Veterocordyceps gen. nov. This finding provides clarity to the results of previous workers who considered species in the genus as members of Ophiocordyceps based on morphological data and a more limited molecular dataset. Cordyceps fratricida, a pathogen of ergot, and the rice pathogen Ustilaginoidea virens were placed phylogenetically within Clavicipitaceae. The genus Tyrranocordyceps gen. nov. was established for fungal pathogens that attack closely related species of ergot. Tyrranocordyceps represents a sexual state for a clade of\ud fungal pathogens known only from asexual states. Ustilaginoidea virens was found to occupy a separate lineage of plant pathogens, representing a third clade of clavicipitaceous fungi deriving their nutrition from a plant source. Ancestral character-state reconstruction reveals plant pathogens/endophytes have arisen multiple times during the history of the family and T. fratricida evolved from a plant pathogenic ancestor. The switch to a plant based nutritional mode appears to be facilitated by an ancestral host association with scale insects (Hemiptera: Sternorrhycha:Coccoidea). These insects are sessile in their adult stage and insert their mouthparts directly into living plant tissues, a characteristic that might mediate the acquisition of plant nutrients by their fungal pathogens and eventually result in bypassing the insect host all together. Finally, ancestral character-state reconstructions were performed on a phylogeny representing teleomorphic taxa from throughout Hypocreales for the characters of stipe (absence or presence) and habitat (terrestrial or arboreal). Hypocreales was found to have evolved from a terrestrial, astipitate ancestor. Stipitate morphologies were derived multiple times over the evolution of the order. This observation accounts for the phylogenetic signal in the stipe characters of color and texture. The characters of stipe and habitat were found to be highly correlated. Species occurring in arboreal habitats tend to be astipitate. This was inferred to be the retention of the ancestral state for early diverging members of Cordycipitaceae. However, all other astipitate, arboreal species were inferred to have lost the stipe after moving from a terrestrial habitat. This is likely an evolutionary\ud response to release from evolutionary pressures to elevate reproductive tissues above a substrate