Phylogenetic classification of Cordyceps and the clavicipitaceous fungi

Abstract

Cordyceps, comprising over 400 species, was historically classified in the Clavicipitaceae, based on cylindrical asci, thickened ascus apices and filiform ascospores, which often disarticulate into part-spores. Cordyceps was characterized by the production of well-developed often stipitate stromata and an ecology as a pathogen of arthropods and Elaphomyces with infrageneric classifications emphasizing arrangement of perithecia, ascospore morphology and host affiliation. To refine the classification of Cordyceps and the Clavicipitaceae, the phylogenetic relationships of 162 taxa were estimated based on analyses consisting of five to seven loci, including the nuclear ribosomal small and large subunits (nrSSU and nrLSU), the elongation factor 1α (tef1), the largest and the second largest subunits of RNA polymerase II (rpb1 and rpb2), β-tubulin (tub), and mitochondrial ATP6 (atp6). Our results strongly support the existence of three clavicipitaceous clades and reject the monophyly of both Cordyceps and Clavicipitaceae. Most diagnostic characters used in current classifications of Cordyceps (e.g., arrangement of perithecia, ascospore fragmentation, etc.) were not supported as being phylogenetically informative; the characters that were most consistent with the phylogeny were texture, pigmentation and morphology of stromata. Therefore, we revise the taxonomy of Cordyceps and the Clavicipitaceae to be consistent with the multi-gene phylogeny. The family Cordycipitaceae is validated based on the type of Cordyceps, C. militaris, and includes most Cordyceps species that possess brightly coloured, fleshy stromata. The new family Ophiocordycipitaceae is proposed based on Ophiocordyceps Petch, which we emend. The majority of species in this family produce darkly pigmented, tough to pliant stromata that often possess aperithecial apices. The new genus Elaphocordyceps is proposed for a subclade of the Ophiocordycipitaceae, which includes all species of Cordyceps that parasitize the fungal genus Elaphomyces and some closely related species that parasitize arthropods. The family Clavicipitaceae s. s. is emended and includes the core clade of grass symbionts (e.g., Balansia, Claviceps, Epichloë, etc.), and the entomopathogenic genus Hypocrella and relatives. In addition, the new genus Metacordyceps is proposed for Cordyceps species that are closely related to the grass symbionts in the Clavicipitaceae s. s. Metacordyceps includes teleomorphs linked to Metarhizium and other closely related anamorphs. Two new species are described, and lists of accepted names for species in Cordyceps, Elaphocordyceps, Metacordyceps and Ophiocordyceps are provided.

Current nomenclatural changes inCordyceps sensu latoand its multidisciplinary impacts

“…Sung et al and Tyrannicordyceps Kepler & Spatafora that together accommodated more than 180 Cordyceps spp. (Sung et al 2007; Kepler et al 2012b) (Figure 1). Besides transfer of many Cordyceps spp.…”

“…Elaphocordyceps, Ophiocordyceps and other allied genera formed a separate clade and were placed in a new family Ophiocordycipitaceae that formed a sister clade with Clavicipitaceae s.s . (Sung et al 2007). Cordyceps s.s .…”

“…Tul. within Clavicipitaceae (Sung et al 2007). Cordyceps sensu stricto was, hence, circumscribed to a clade that consisted of its type species C. militaris (L.) Fr., and new genera were proposed for other clades outside Cordyceps s.s.: Metacordyceps G.H.…”

“…(~ 170 spp.) still remain incertae sedis (of uncertain placement) within Hypocreales, because of lack of molecular phylogenetic studies or inconclusive morphological and ecological assessment (Sung et al 2007).

10.1080/21501203.2017.1386242-F0001Figure 1.Genera segregated from Cordyceps s.l.

…”

“…(Sung et al 2007). Tyrannicordyceps is a small genus placed within a clade of Balansia, Claviceps and Epichloë , to which all five spp.…”