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1 Department of Botany and Plant Pathology, Oregon State University,
Corvallis, OR 97331–2902, U.S.A.
2 Mycology Laboratory, National Center for Genetic Engineering and
Biotechnology, Science Park, Pathum Thani, Thailand
3 Department of Applied Biology and Entomopathogenic Fungal Culture
Collection (EFCC), Kangwon National University, Chuncheon 200-701, Republic of
Korea
4 Phylogenetics Laboratory, National Center for Genetic Engineering and
Biotechnology, Science Park, Pathum Thani, Thailand.
*Correspondence: Gi-Ho Sung,
sungg{at}science.oregonstate.edu
| Abstract |
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(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. Taxonomic novelties: New family: Ophiocordycipitaceae G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora. New genera: Elaphocordyceps G.H. Sung & Spatafora, Metacordyceps G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora. New species: Metacordyceps yongmunensis G.H. Sung, J.M. Sung & Spatafora; Ophiocordyceps communis Hywel-Jones & Samson. New combinations: Cordyceps confragosa (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, C. ninchukispora (C.H. Su & H.-H. Wang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora; Elaphocordyceps capitata (Holmsk.) G.H. Sung, J.M. Sung & Spatafora, E. delicatistipitata (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. fracta (Mains) G.H. Sung, J.M. Sung & Spatafora, E. inegoënsis (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. intermedia (S. Imai) G.H. Sung, J.M. Sung & Spatafora, E. japonica (Lloyd) G.H. Sung, J.M. Sung & Spatafora, E. jezoënsis (S. Imai) G.H. Sung, J.M. Sung & Spatafora, E. longisegmentis (Ginns) G.H. Sung, J.M. Sung & Spatafora, E. minazukiensis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung & Spatafora, E. miomoteana (Kobayasi & Shimizu) G.H. Sung, J.M. Sung & Spatafora, E. ophioglossoides (Ehrh.) G.H. Sung, J.M. Sung & Spatafora, E. paradoxa (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. ramosa (Teng) G.H. Sung, J.M. Sung & Spatafora, E. rouxii (Cand.) G.H. Sung, J.M. Sung & Spatafora, E. subsessilis (Petch) G.H. Sung, J.M. Sung & Spatafora, E. szemaoënsis (M. Zang) G.H. Sung, J.M. Sung & Spatafora, E. tenuispora (Mains) G.H. Sung, J.M. Sung & Spatafora, E. toriharamontana (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. valliformis (Mains) G.H. Sung, J.M. Sung & Spatafora, E. valvatistipitata (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. virens (Kobayasi) G.H. Sung, J.M. Sung & Spatafora; infraspecific: E. intermedia f. michinokuënsis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung & Spatafora, E. ophioglossoides f.alba (Kobayasi & Shimizu ex Y.J. Yao) G.H. Sung, J.M. Sung & Spatafora, E. ophioglossoides f. cuboides (Kobayasi) G.H. Sung, J.M. Sung & Spatafora; Metacordyceps brittlebankisoides (Z.Y. Liu, Z.Q. Liang, Whalley, Y.J. Yao & A.Y. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, M. campsosterni (W.M. Zhang & T. H. Li) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, M. chlamydosporia (H.C. Evans) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, M. liangshanensis (M. Zang, D. Liu & R. Hu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, M. taii (Z.Q. Liang & A.Y. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora; Ophiocordyceps agriotidis (A. Kawam.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ainictos (A. Möller) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. amazonica (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. aphodii (Mathieson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. appendiculata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. arachneicola (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. arbuscula (Teng) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. armeniaca (Berk. & M.A. Curtis) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. asyuënsis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. aurantia (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. australis (Speg.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. barnesii (Thwaites) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. bicephala (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. bispora (Stifler) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. brunneipunctata (Hywel-Jones) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cantharelloides (Samson & H.C. Evans) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. carabidicola (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cicadicola (Teng) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. clavata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. coccidiicola (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. coccigena (Tul. & C. Tul.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cochlidiicola (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. corallomyces (A. Möller) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. crassispora (M. Zang, D. R. Yang & C.D. Li) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. crinalis (Ellis ex Lloyd) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cucumispora (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. curculionum (Tul. & C. Tul.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cusu (Pat.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cylindrostromata (Z.Q. Liang, A.Y. Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. dayiensis (Z.Q. Liang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. dermapterigena (Z.Q. Liang, A.Y. Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. dipterigena (Berk. & Broome) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. discoideicapitata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ditmarii (Quél.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. dovei (Rodway) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. elateridicola (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. elongata (Petch) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. elongatiperitheciata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. elongatistromata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. emeiensis (A.Y. Liu & Z.Q. Liang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. engleriana (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. entomorrhiza (Dicks.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. evdogeorgiae (Koval) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. falcata (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. falcatoides (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. fasciculatistromata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ferruginosa (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. filiformis (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. formicarum (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. forquignonii (Quél.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. furcicaudata (Z.Q. Liang, A.Y. Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. gansuënsis (K. Zhang, C. Wang & M. Yan) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. geniculata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. gentilis (Ces.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. glaziovii (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. goniophora (Speg.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. gracilioides (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. gracilis (Grev.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. heteropoda (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. hiugensis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. huberiana (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. humbertii (C.P. Robin) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. insignis (Cooke & Ravenel) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. irangiensis (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. japonensis (Hara) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. jiangxiensis (Z.Q. Liang, A.Y. Liu & Y.C. Jiang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. jinggangshanensis (Z.Q. Liang, A.Y. Liu & Y.C. Jiang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. kangdingensis (M. Zang & Kinjo) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. kniphofioides (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. koningsbergeri (Penz. & Sacc.) G. H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. konnoana (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. lachnopoda (Penz. & Sacc.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. larvarum (Westwood) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. lloydii (H.S. Fawc.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. longissima (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. lutea (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. melolonthae (Tul. & C. Tul.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. michhganensis (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. minutissima (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. monticola (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. mrciensis (J.C. Jung, Z.Q.Liang, Soytong & K.D. Hyde) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. multiaxialis (M. Zang & Kinjo) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. myrmecophila (Ces.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. neovolkiana (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nepalensis (M. Zang & Kinjo) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nigra (Samson, H.C. Evans & Hoekstra) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nigrella (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nigripes (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nutans (Pat.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. obtusa (Penz. & Sacc.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. octospora (M. Blackwell & Gilb) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. odonatae (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. osuzumontana (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ouwensii (Höhn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. owariensis (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. oxycephala (Penz. & Sacc.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. pentatomae (Koval) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. petchii (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. proliferans (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. pseudolloydii (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. pseudolongissima (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. purpureostromata (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ravenelii (Berk. & M.A. Curtis) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. robertsii (Hook.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. rubiginosiperitheciata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. rubripunctata (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ryogamiensis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. salebrosa (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. scottiana (Olliff) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. selkirkii (Olliff) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sichuanensis (Z.Q. Liang & B. Wang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sinensis (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. smithii (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sobolifera (Hill ex Watson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sphecocephala (Klotzsch ex Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. stipillata (Z.Q. Liang & A.Y. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. stylophora (Berk. & Broome) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. subflavida (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. superficialis (Peck) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. takaoënsis (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. taylorii (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. thyrsoides (A. Möller) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. tricentri (Yasuda) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. uchiyamae (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. variabilis (Petch) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. voeltzkowii (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. volkiana (A. Möller) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. wuyishanensis (Z.Q. Liang, A.Y. Liu & J.Z. Huang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. yakusimensis (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. zhangjiajiensis (Z.Q. Liang & A.Y. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora; infraspecific: O. amazonica var. neoamazonica (Kobayasi & Hara) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cucumispora var. dolichoderi (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. kniphofioides var. dolichoderi (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. kniphofioides var. monacidis (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. kniphofioides var. ponerinarum (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. lloydii var. binata (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. melolonthae var. rickii (Lloyd) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. owariensis f. viridescens (Uchiyama & Udagawa) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. purpureostromata f. recurvata (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. superficialis f. crustacea (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora; Pochonia parasitica (G.L. Barron) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora.
Keywords Clavicipitaceae / Cordyceps / Cordycipitaceae / Elaphocordyceps / Metacordyceps / multigene phylogeny / Ophiocordyceps / Ophiocordycipitaceae
| INTRODUCTION |
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Modern infrageneric classifications of Cordyceps have been based primarily on the taxonomic studies of Kobayasi (1941, 1982) and Mains (1958) (but see Massee 1895). Kobayasi (1941, 1982) recognized three subgenera (C. subg. Cordyceps, C. subg. Ophiocordyceps, and C. subg. Neocordyceps), emphasizing arrangement of perithecia and morphology of asci, ascospores and part-spores. Species of C. subg. Cordyceps (type C. militaris) were characterized by the production of either immersed or superficial perithecia produced at approximately right angles (ordinal) to the surface of the stroma and ascospores that disarticulate into part-spores at maturity. Cordyceps subg. Ophiocordyceps (Petch) Kobayasi (type C. blattae Petch) was distinguished by the production of whole ascospores that do not disarticulate into part-spores and, in some species, asci lacking pronounced apical hemispheric caps. Cordyceps subg. Neocordyceps Kobayasi (type C. sphecocephala (Klotzsch ex Berk.) Berk. & M.A. Curtis) was characterized by perithecia immersed at oblique angles in the clava region of the stroma and ascospores that disarticulate into part-spores upon maturity.
Mains (1958) expanded the infrageneric classification with a different emphasis on diagnostic characters and recognized two additional subgenera, C. subg. Racemella (Ces.) Sacc. and C. subg. Cryptocordyceps Mains. Cordyceps subg. Racemella (type C. memorabilis (Ces.) Sacc.) included species that produce superficial perithecia and asci with hemispheric to short cylindrical caps. Cordyceps subg. Cryptocordyceps (type C. ravenelii Berk. & M.A. Curtis) was diagnosed by the production of brown, partly immersed to superficial perithecia in a palisade-like layer at more or less right angles to the surface of the stroma. Kobayasi and Mains also differed in their treatments of C. subg. Ophiocordyceps and C. subg. Neocordyceps. In contrast to Kobayasi (1941), who essentially adopted the diagnosis of Petch (1931) but at the rank of subgenus, Mains (1958) placed only C. blattae and C. peltata Wakef. in C. subg. Ophiocordyceps based on their lack of a thickened ascus apex, thus deemphasizing the importance of ascospore disarticulation at the subgeneric level. Furthermore, Mains (1958) did not recognize C. subg. Neocordyceps, rather he included species with oblique perithecia in C. subg. Cordyceps sect. Cremastocarpon subsect. Entomogenae. Currently, the subgenera C. subg. Cordyceps, C. subg. Ophiocordyceps, and C. subg. Neocordyceps sensu Kobayasi (1941) have been arguably the most widely used infrageneric taxa of Cordyceps (Zang & Kinjo 1998, Artjariyasripong et al. 2001, Hywel-Jones 2002, Sung & Spatafora 2004, Stensrud et al. 2005) with the relatively recent addition of C. subg. Bolacordyceps O.E. Erikss., which is characterized by the production of bola-ascospores (Eriksson 198). Although this ascospore form has been likened to the South American bola or the East Asian ninchuk (martial arts weapon), the overall form is best likened to that of a skipping rope. The two handles of the skipping rope are two terminal sets of four cells. The `rope' is a slender hyphal thread, which appears to lack cytoplasm or, at most, has relic quantities.
In addition to the morphological characters discussed above, host affiliation has played an important role in the classification of Cordyceps (Massee 1895, Kobayasi 1982). Cordyceps species that parasitize the truffle genus Elaphomyces have been recognized as a unique taxon. The genus Cordylia Fr. (1818) was once assigned for the mycogenous Cordyceps species (Massee 1895) although it is a homonym of Cordylia Pers. 1807. Kobayasi (1941, 1982) also recognized the mycogenous Cordyceps species as taxonomic units (e.g., C. subg. Cordyceps sect. Cystocarpon subsect. Eucystocarpon ser. Mycogenae) and emphasized the utility of host affiliations in delimiting closely related species of arthropod pathogens. Mains (1958) adopted Kobayasi's treatment of the parasites of Elaphomyces, but questioned whether morphologically similar species on different insect hosts (e.g., C. irangiensis Moureau and C. sphecocephala attacking ants and wasps, respectively) are conspecific. The applicability of hosts as a taxonomic character is complicated, however, due to the difficulty in identifying immature hosts (e.g., larvae and pupae) and insufficient host identification for many herbarium collections.
Several phylogenetic studies employing ribosomal DNA (Artjariyasripong et al. 2001, Sung et al. 2001, Stensrud et al. 200) have been conducted to test and refine the classification of Cordyceps. Such studies were restricted by both limited taxon sampling and the inadequate resolution power of ribosomal DNA, resulting in limited conclusions regarding systematics of the genus. Recent phylogenetic studies (Spatafora et al. 2007, Sung et al. 2007) based on multiple independent loci provided a greater level of resolution and support, and revealed that neither Cordyceps nor the family Clavicipitaceae is monophyletic. Three monophyletic groups of the clavicipitaceous fungi were recognized, all of which include species of Cordyceps. These results reject the current infrafamilial classification (Diehl 1950) and indicate that the phylogenetic diversity of Cordyceps is representative of the entire family Clavicipitaceae (Spatafora et al. 2007, Sung et al. 2007). Therefore, a new classification of Cordyceps and the Clavicipitaceae is necessary to reflect the current hypotheses of phylogenetic relationships and to be predictive in nature.
Here, we conducted the most extensive multi-gene phylogenetic analyses to provide a basis for the phylogenetic classification of Cordyceps and the clavicipitaceous fungi. The main objectives of this study are to 1) reassess the morphological traits used in the current classifications of Cordyceps in the context of phylogeny, 2) investigate the taxonomic utility of the anamorphic forms in classification of Cordyceps and better understand the teleomorph–anamorph connections, and 3) revise the classification of Cordyceps and Clavicipitaceae to be consistent with phylogenetic relationships.
| MATERIALS AND METHODS |
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(tef1), and the
largest and second largest subunits of RNA polymerase II (rpb1 and
rpb2). These sequences were combined with data from 91 taxa, which
were obtained from Sung et al.
(2007). Information pertaining
to voucher numbers concerning the sequences is provided in
Table 1.
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Sequence alignment and phylogenetic analyses
Sequences were edited using SeqEd 1.0.3 (Applied Biosystems Inc.) and
contigs were assembled using CodonCode Aligner 1.4 (CodonCode Inc.). Sequences
of each gene partition were initially aligned with Clustal W 1.64
(Thompson et al.
1994) and appended to an existing alignment
(Sung et al. 2007).
This initial alignment was manually edited as necessary in MacClade 4.0
(Maddison & Maddison
2000). All five gene regions sampled in this study were
concatenated into a single, combined data set (162-taxon -gene data set) with
ambiguously aligned regions excluded from phylogenetic analyses. Sequences
from two additional gene regions, β-tubulin (tub) and
mitochondrial ATP6 (atp6), from Sung et al.
(2007) were also combined with
the 162-taxon 7-gene data set to generate a supermatrix of 162-taxon 7-gene
data set.
In order to detect incongruence among the five individual gene regions sampled in this study, bootstrap proportions were used for each individual data set with the 107 taxa that was complete for all five genes (Table 1). Bootstrap proportions (BP) were determined in a maximum-parsimony framework using the program PAUP* 4.0b10 (Swofford 2002). Only parsimony-informative characters were used with the following search options: 100 replicates of random sequence addition, TBR branch swapping, and MulTrees OFF. The incongruence was assumed to be significant if two different relationships for the same set of taxa were both supported with greater than 70 % bootstrap proportions by different genes (Mason-Gamer & Kellogg 1996, Wiens 1998). Previous studies revealed that tub was double copy in some clavicipitaceous species (Spatafora et al. 2007), and Sung et al. (2007) also showed that while atp6 possessed conflicting data for a limited number of taxa, the conflict was localized and the locus simultaneously provided increased level of support for other nodes. Thus, although we focused our sampling and analyses of the five aforementioned loci, we also conducted phylogenetic supermatrix analyses with tub and atp6 (162-taxon 7-gene) to detect any increased nodal support provided by those two loci.
Maximum parsimony (MP) analyses were conducted on the 162-taxon 5-gene and the 162-taxon 7-gene data set (Table 1, Fig. 3). All characters were equally weighted and unordered. MP analyses were performed using only parsimony-informative characters with the following settings: 100 replicates of random sequence addition, TBR branch swapping, and MulTrees ON. Phylogenetic confidence was assessed by nonparametric bootstrapping (Felsenstein 198). A total of 200 bootstrap replicates were used to calculate bootstrap proportions; bootstrapping used the same search options with five replicates of random sequence addition per bootstrap replicate.
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) and employed the model separately for each partition. In an
initial analysis, a B-MCMCMC analysis with five million generations and four
chains was conducted in order to test the convergence of log-likelihood. Trees
were sampled every 100 generations, for a total of 50,000 trees. For a second
analysis, five independent Bayesian runs with two million generations and
random starting trees were conducted to reconfirm log-likelihood convergence
and mixing of chains. In addition to the analyses with 162-taxon 5-gene data set, a series of analyses were conducted in MP, ML, and Bayesian frameworks with different taxon samplings (107- and 152-taxon 5-gene data sets) to address the potential topological effects of missing data. Previous phylogenetic and simulation studies demonstrated that the phylogenetic analyses are often not negatively affected if less than 50 % characters are missing for each taxon in the phylogenetic analyses (Wiens 2003, Phylippe et al. 2004). In this study, we assumed that the phylogenetic analysis is not confounded if the taxa were complete for at least three out of five gene partitions. Therefore, ten taxa (Table 1) in the 162-taxon 5-gene data set that were complete for only two gene partitions were excluded to generate the 162-taxon 5-gene data set. A 107-taxon 5-gene data set that does not contain any missing data in gene partitions was also prepared to compare the phylogenetic relationships between 107-taxon and 152-taxon 5-gene analyses. MP, ML, and Bayesian analyses based on the 162-taxon 5-gene data set (Figs 1, 2) showed that the C. sphecocephala clade is characterized by long-branch lengths relative to the rest of the clavicipitaceous fungi. To address the impact of the C. sphecocephala clade on the phylogenetic resolution, we excluded all members of the C. sphecocephala clade from the 152-taxon 5-gene data set and constructed a 147-taxon 5-gene data set.
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| RESULTS |
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Phylogenetic analyses
The reciprocal comparisons of 70 % bootstrap trees from individual data
sets of the 162-taxon 5-gene dataset did not reveal any significantly
supported contradictory nodes (data not shown). These results were interpreted
as indicating that no strong incongruence existed among the individual data
sets that would be indicative of different phylogenetic gene histories (e.g.,
lineage sorting or horizontal gene transfer). As a result, all five individual
data sets were combined in simultaneous analyses.
MP analyses of the 162-taxon 5-gene data set resulted in 156 equally parsimonious trees. These trees were 21,323 steps with a consistency index (CI) of 0.1598 and a retention index (RI) of 0.6131. One of 156 equally parsimonious trees is shown in Fig. 1. Nodes that collapse in the strict consensus tree are denoted with asterisks. ML analyses of the 162-taxon 5-gene data set resulted in a tree with a log-likelihood (–ln) of 92019.95. In the Bayesian analyses, the five-million generation analysis converged on the log-likelihood (harmonic mean = –ln 9951.22) at approximately around 250,000 generations. The results from five of two-million generation analyses also showed a convergence on the log-likelihood at approximately 2 0,000 generations and the topologies were identical. As a result, the 3,000 trees from the first 300,000 generations were deleted from the five million generation analysis to generate a 50 % majority-rule consensus tree.
A 50 % majority consensus tree (Fig.
2) was generated from the million generation analysis. Since the
topology of ML analyses (tree not shown) was nearly identical to that of the
Bayesian consensus tree of Fig.
2, the bootstrap proportions of ML analyses are provided above the
corresponding nodes in Fig. 2.
Previous studies have shown that in interpreting the supports of the
phylogenetic estimates of relationships, the posterior probability tends to
overestimate the phylogenetic confidence
(Doaudy et al. 2003,
Lutzoni et al. 2004,
Reeb et al. 2004). As
a result, the posterior probabilities were used as a supplementary indicator
to bootstrap proportions. In this study, nodes were considered strongly
supported when supported by both bootstrap proportions (BP
70 %) and
posterior probabilities (PP
0.95)
(Lutzoni et al.
2004).
Phylogenetic relationships of the clavicipitaceous fungi
All MP, ML, and Bayesian analyses of the five-gene 162-taxon 5-gene data
set recognized three well-supported clades of clavicipitaceous fungi (Figs
1,
2), designated here as
Clavicipitaceae clades A, B, and C (Figs
1,
2), following the convention of
the previous phylogenetic studies
(Spatafora et al.
2007, Sung et al.
2007). These clades were statistically well supported by the
bootstrap proportions of the MP (MP-BP) and ML (ML-BP) analyses and posterior
probabilities (PP) of the Bayesian analyses (clade A: MP-BP = 98 %, ML-BP = 99
%, PP = 1.00; clade B: MP-BP = 93 %, ML-BP = 98 %, PP = 1.00; clade C: MP-BP =
100 %, ML-BP = 100 %, PP = 1.00). A sister-group relationship between clades A
and B was also strongly supported (MP-BP = 72 %, ML-BP = 90 %, PP = 1.00). The
monophyletic group of clade C and Hypocreaceae was moderately to
strongly supported (MP-BP = 63 %, ML-BP = 92 %, PP = 1.00).
Clavicipitaceae clade A comprised five statistically well-supported subclades (Figs 1, 2, 4). These were labelled in Figs 1, 2, and 4 as the C. taii clade (MP-BP = 73 %, ML-BP = 78 %, PP = 1.00), the Claviceps clade (MP-BP = 95 %, ML-BP = 98 %, PP = 1.00), the Hypocrella clade (MP-BP = 99 %, ML-BP = 99 %, PP = 1.00), the Shimizuomyces clade (MP-BP = 100 %, ML-BP = 100 %, PP = 1.00), and the Torrubiella luteorostrata clade (MP-BP = 100 %, ML-BP = 100 %, PP = 1.00). As indicated previously by Sung et al. (2007), internal relationships among these five subclades were not strongly supported in MP and ML analyses (Figs 1, 2, 4).
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Clavicipitaceae clade C comprised two well-supported subclades (Figs 1, 2, 8). The Simplicillium subclade (MP-BP = 100 %, ML-BP = 100 %, PP = 1.00) consisted of isolates of the anamorph genus Simplicillium, most of which were isolated as parasites of other fungi. The Cordyceps subclade (MP-BP = 98 %, ML-BP = 100 %, PP = 1.00) included numerous species of Torrubiella and species of Cordyceps that produce pallid to brightly coloured stromata with ascospore morphologies ranging from whole ascospores to part-spores to bola-ascospores according to species. Importantly, the Clavicipitaceae clade C included C. militaris and represents the core Cordyceps clade. The remaining species, Torrubiella wallacei H.C. Evans, was also a member of the Cordyceps clade with strong support (ML-BP = 91 %, PP = 1.00) in ML and Bayesian analyses (Figs 2, 8), but could not be confidently assigned to either subclade in MP analyses (Fig. 1).
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| DISCUSSION |
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The phylogenetic hypothesis presented here contradicts current infrafamilial classification of the Clavicipitaceae. Diehl (1950) proposed three subfamilies, Oomycetoideae, Clavicipitoideae, and Cordycipitoideae, based on the development of stromata, anamorphic characters and host affiliations. However, these three subfamilies do not coincide with the three clades of the Clavicipitaceae inferred in the present analyses (Figs 1, 2). Clavicipitaceae clade A includes members of all three subfamilies (e.g., Claviceps of Clavicipitoideae, Cordyceps of Cordycipitoideae, and Hypocrella of Oomycetoideae), whereas the remaining clades only comprise members of Cordycipitoideae (e.g., Cordyceps and Torrubiella). Importantly, all three major clades include members of Cordyceps, indicating that Cordyceps, like Clavicipitaceae, is not monophyletic (Figs 1, 2). As a result, the three recognized well-supported clades (clades A–C) of the clavicipitaceous fungi represent a robust phylogenetic framework for the taxonomic revision of Cordyceps and the Clavicipitaceae.
In the current infrageneric classification of the genus, Cordyceps comprises four subgenera (C. subg. Bolacordyceps, C. subg. Cordyceps, C. subg. Neocordyceps, and C. subg. Ophiocordyceps) based on ascospore morphology and arrangement of the perithecia in the stromata (Kobayasi 1941, 1982, Eriksson 1986). However, most of these characters are not consistent with the new phylogenetic hypothesis and are not diagnostic of monophyletic taxa (e.g., subgenera and genera) (Figs 1, 2). For example, Kobayasi (1941, 1982) emphasized ascospore morphology and the lack of ascospore disarticulation into part-spores to delimit C. subg. Ophiocordyceps from the other subgenera. Species with non-disarticulating ascospores, however, are included in all three major clades (C. acicularis Ravenel of clade B, C. cardinalis G.H. Sung & Spatafora of clade C, and Cordyceps sp. EFCC 2131 and 2135 of clade A described below as Metacordyceps yongmunensis) (Figs 1, 2), indicating that non-disarticulating ascospores are not phylogenetically informative at this level (Figs 1, 2). Therefore, a reassessment of diagnostic characters, in the previous and current classifications of Cordyceps, is necessary for the three major clades to provide a basis for taxonomic revisions of Cordyceps and the Clavicipitaceae.
Species in Clavicipitaceae clade A
Clavicipitaceae clade A comprises five well-supported subclades
(Fig. 4). All known species of
Cordyceps in the clade are included in the C. taii clade.
Species of Cordyceps in the clade possess partially or completely
immersed perithecia on clavate to cylindrical fertile parts of the stromata
(Zang et al. 1982,
Liang et al. 1991,
Zare et al. 2001).
They produce ascospores that either disarticulate or remain intact at maturity
and include species that possess ordinal and obliquely embedded perithecia. In
the current classification, clade A includes species of Cordyceps
that were formerly classified in three subgenera of Cordyceps. Cordyceps
liangshanensis M. Zang, D. Liu & R. Hu forms ordinal perithecia and
possess disarticulating ascospores, consistent with C. subg.
Cordyceps (Kobayasi
1982, Zang et al.
1982). Cordyceps chlamydosporia H.C. Evans possesses
nondisarticulating ascospores, consistent with C. subg.
Ophiocordyceps (Zare et
al. 2001). Cordyceps taii Z.Q. Liang & A.Y. Liu,
a known teleomorph species linked to the anamorph genus Metarhizium
Sorokin, produces disarticulating ascospores and obliquely embedded perithecia
in the stromata, a trait used to recognize C. subg.
Neocordyceps (Liang et
al. 1991). Importantly, Cordyceps sp. EFCC 2131 and
2135 (described below as Metacordyceps yongmunensis) produce
non-disarticulating ascospores and obliquely embedded perithecia in the
stromata, characters inconsistent with any of the subgenera in the current
classification.
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Species in Clavicipitaceae clade B
Species of Cordyceps in Clavicipitaceae clade B possess
disarticulating or non-disarticulating ascospores and produce superficial to
completely immersed perithecia that are ordinally or obliquely inserted in the
stromata. As with the Cordyceps species of clade A, this clade also
includes members of the former C. subg. Cordyceps (e.g.,
C. ophioglossoides (Ehrh.) Link and C. variabilis Petch),
C. subg. Ophiocordyceps (e.g., C. acicularis and
C. unilateralis (Tul. & C. Tul.) Sacc.), and C. subg.
Neocordyceps (e.g., C. nutans Pat. and C.
sphecocephala). The majority of Cordyceps species in this clade
produce wiry to pliant or fibrous stromata that typically are completely or
partially darkly pigmented and parasitize subterranean or wood-inhabiting
hosts, which are buried in soil or embedded in decaying wood. Exceptions to
this morphology and ecology do exist, however; for example, C.
melolonthae (Tul. & C. Tul.) Sacc. is pigmented bright yellow but
stains darkly upon handling, and members of the C. sphecocephala
clade parasitize adult insects.
Clade B consists of five subclades. All subclades include either species of Cordyceps or anamorphs with potential links to Cordyceps (e.g., Nomuraea atypicola (Yasuda) Samson linked to C. cylindrica Petch) (Fig. 6, Evans & Samson 1987). The well-resolved tree in the present study (Fig. 6) provides the basis to characterize three of the five subclades of clade B. Due to insufficient taxon sampling, it is not possible to characterize the members of the Cordyceps species in the C. gunnii and Pa. lilacinus subclades. In the light of this, we focus on the remaining three subclades that include sufficient numbers of Cordyceps species.
The C. ophioglossoides subclade primarily consists of Cordyceps species that parasitize species of the genus Elaphomyces (e.g., C. ophioglossoides and C. capitata (Holmsk.) Link) and the nymphs of cicadas (e.g., C. inegoënsis Kobayasi and C. paradoxa Kobayasi) buried in soil (Kobayasi 1939, Mains 1957, Kobayasi & Shimizu 1960, 1963). Species in this subclade produce partially or completely immersed perithecia, in clavate to capitate fertile parts of stromata that are darkly pigmented with olivaceous tints (Kobayasi & Shimizu 1960, 1963). Because they produce disarticulating ascospores and ordinal perithecia, all known species of this clade are classified in C. subg. Cordyceps.
Cordyceps subsessilis Petch is unique to the C. ophioglossoides subclade (Fig. 6). It produces perithecia on white or pallid reduced stromata, arising from a rhizomorph-like structure from scarabaeid beetle larvae (Hodge et al. 1996). It is the only member of the subclade that parasitizes beetles embedded in decaying wood (Hodge et al. 1996). Therefore, C. subsessilis differs greatly in ecology and morphology of its stromata from most other taxa in the C. ophioglossoides clade, but it possesses several characters shared by its close relative, C. ophioglossoides (Kobayasi & Shimizu 1960, Hodge et al. 1996). Both species grow axenically on simple media, produce verticilliate anamorphs (C. subsessilis has a Tolypocladium anamorph, whereas C. ophioglossoides has verticillium-like conidiophores), possess nearly identical part-spore morphologies, and produce stromata that are connected to their hosts via rhizomorph-like structures. In contrast, C. capitata/C. longisegmentis have not successfully been grown in culture, they are attached directly to the host, and an anamorph is unknown.
The C. ophioglossoides subclade (Fig. 6) also includes parasites of subterranean cicada nymphs (e.g., C. inegoënsis and C. paradoxa), which are grouped with their close relatives (e.g., C. jezoënsis S. Imai and C. ophioglossoides) that parasitize subterranean truffles of Elaphomyces. Despite low support of inter-species relationships within the C. ophioglossoides subclade due to short branch lengths, C. paradoxa and C. inegoënsis are morphologically more similar to C. jezoënsis and C. ophioglossoides than to any other members of the clade. These taxa produce clavate fertile parts of the stromata rather than capitate stromata like other members of the clade (e.g., C. capitata and C. fracta Mains). Many of these species (e.g., C. jezoënsis and C. paradoxa) are also known to connect to their hosts via rhizomorph-like structures (Kobayasi & Shimizu 1960, 1963), supporting a close phylogenetic relationship.
The C. unilateralis subclade includes the most morphologically diverse assemblages of Cordyceps species (Fig. 6). Most of the species in the clade parasitize larval, pupal or nymph stages of arthropods (Kobayasi 1941, Mains 1958). Species of this clade produce superficial to completely immersed perithecia on the stromata with morphologies ranging from capitate to clavate to filiform (Kobayasi 1941, Mains 1958). They typically possess tough, pliant, or fibrous stromata that are entirely or partially darkly pigmented, although some exceptions (e.g., C. melolonthae and C. variabilis) do exist, which produce brightly pigmented stromata (Mains 1958). Many species in the clade (e.g., C. brunneipunctata Hywel-Jones, C. stylophora Berk. & Broome, and C. unilateralis) are also differentiated by aperithecial stromatal apices while the production of perithecia occurs in subterminal regions of the stroma.
Similar to Cordyceps species in clade A, the C. unilateralis subclade includes species that produce disarticulating or non-disarticulating (intact) ascospores. For example, some species in the C. unilateralis subclade (e.g., C. sinensis (Berk.) Sacc. and C. unilateralis) were formerly classified in C. subg. Ophiocordyceps. But these species are interspersed among other species (e.g., C. agriotidis A. Kawam. and C. robertsii (Hook.) Berk.) that are classified in C. subg. Cordyceps. This indicates that, while ascospore morphology is useful in delimiting closely related Cordyceps species and uniting others in species complexes, it is not diagnostic of the C. unilateralis subclade itself (Fig. 6).
Most members of C. subg. Neocordyceps, as classically treated by Kobayasi (1941, 1982) and others (e.g., Artjariyasripong et al. 2001, Stensrud et al. 2005), form a monophyletic group labelled as the C. sphecocephala subclade within the C. unilateralis group (Fig. 6). The majority of species in the C. sphecocephala subclade produce long, thin, pliant, brightly coloured (or dark marasmioid in a few species) stromata, which terminate in clavate to elongated fertile parts, and possess ascospores that disarticulate into sixty-four part-spores (Kobayasi 1941, 1982, Hywel-Jones 2002). Species in this clade produce perithecia, which are partially or completely immersed in the stromata at strongly oblique angles (Kobayasi 1941, 1982, Mains 1958, Hywel-Jones 1996). This clade is one of the best characterized by its morphology (obliquely embedded perithecia in a well-defined clava) and its ecology of parasitizing adult stages of insects.
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Species of Cordyceps in clade C produce superficial to partially immersed perithecia on fleshy stromata that are pallid to brightly pigmented. This is in contrast to Cordyceps species in clade B, which produce darkly pigmented, wiry to pliant or fibrous stromata. This suggests that pigmentation and texture of stromata may be phylogenetically informative at a higher level of classification. It should be noted, however, that some Cordyceps species in clade C are morphologically similar to distantly related Cordyceps species (e.g., C. melolonthae and C. variabilis) in stromatal pigmentation. Although these characters are useful in recognizing Cordyceps species of clade C, the utility of these characters for any future infrageneric classification is probably limited (Fig. 8). For example, C. militaris is macroscopically similar to C. cardinalis and C. pseudomilitaris. All three species produce orangish to red-coloured and fleshy stromata; however, these species differ in ascospore and anamorph morphology (Sung & Spatafora 2004). Furthermore, C. militaris is known as exhibiting considerable variability in stroma morphology (Sung & Spatafora 2004). Potentially conspecific species, such as C. roseostromata Kobayasi & Shimizu and C. kyusyuënsis A. Kawam., differ in stroma morphology, but are closely related to C. militaris and possess identical ascospore and ascus morphologies (Fig. 8, Hywel-Jones 1994, Sung & Spatafora 2004).
The variation in ascospore morphology of Clavicipitaceae clade C combined with old descriptions and unavailable type material complicates species identification for many taxa, as is the case for much of Cordyceps. For example, this study reveals a close relationship between the anamorphic species, Mariannaea pruinosa Z.Q. Liang from China, C. cf. pruinosa from Korea and Thailand, and Phytocordyceps ninchukispora from Taiwan (Fig. 8). The teleomorph of M. pruinosa is C. pruinosa Petch, which was originally described as producing disarticulating ascospores and reddish orange stromata, parasitizing lepidopteran cocoons (Petch 1924, Kobayasi 1941, Liang 1991). Although the isolate of M. pruinosa was obtained from ascospores (Liang 1991), the morphology of the ascospores was not well characterized. The species was identified primarily based on its host affiliation and macroscopic characters. In our study, C. cf. pruinosa EFCC 5197 and N.H.J. 10627 were collected from the same host family (Lepidoptera, Limacodidae) in Korea and Thailand. They are also closely related and produce reddish orange stromata (Fig. 8) and bola-ascospores and not the typical C. subg. Cordyceps part-spores. It should be noted, however, that Petch did not provide any drawings or images of ascospores and it is possible that the terminal cells of bola-ascospores could easily be interpreted as part-spores. Thus, at this time we use the name C. pruinosa for the Chinese, Korean and Thai collections and, if further attempts fail to locate type material for C. pruinosa, one of these may have to be designated a neotype. The C. pruinosa collections are closely related to and morphologically indistinguishable from P. ninchukispora with the exception of host affiliation, suggesting the possibility of host misidentification in the original description of P. ninchukispora. Because the tree topology of the C. pruinosa/P. ninchukispora complex is indicative of greater phylogenetic species diversity, i.e., the Korean, Thai, and Taiwanese material may represent unique phylogenetic species (Fig. 8), we retain the use of both names until more detailed sampling and analyses have been conducted.
Clavicipitaceae clade C not only includes members of Cordyceps but also species of the genus Torrubiella, which generally parasitize spiders and scale insects (Kobayasi & Shimizu 1982). The genus Torrubiella is morphologically characterized by the production of superficial perithecia on a mycelial subiculum that partially or completely surrounds the host (Kobayasi & Shimizu 1982, Humber & Rombach 1987). Species of Torrubiella also produce disarticulating (e.g., T. ratticaudata Humber & Rombach) and intact (e.g., T. wallacei) ascospores. Among species of Cordyceps, C. tuberculata (Lebert) Maire, a pathogen of adult Lepidoptera, has been considered an intermediate species between Torrubiella and Cordyceps (Humber & Rombach 1987, Kobayasi 1941, Mains 1958). Phylogenetic analyses in this study indicate that the members of Torrubiella do not form a monophyletic group within clade C and are interspersed among species of Cordyceps. This suggests that the stipitate stromata of Cordyceps have been gained or lost several times during the evolution of these fungi. Currently, more than 50 species of Torrubiella have been described and the members of genus Torrubiella are clearly undersampled in this study (Kobayasi & Shimizu 1982).
In summary, the characters of ascospore morphology and the arrangement of perithecia used in the current classification of the genus Cordyceps are not congruent with the three higher clades inferred in these analyses. These characters are likely to prove useful, however, in lower level classifications, such as the delimitation of closely related species and species complexes. The characters most congruent with the three higher clades of clavicipitaceous fungi are texture, pigmentation and morphology of the stromata, but with exceptions. Although we have divided Cordyceps species into three major clades, it is difficult to characterize Cordyceps species within the Clavicipitaceae clade A due to the relatively few teleomorph species that are part of this clade (see key on p. 54). They tend to produce green to white stromata, often with lilac tints, but additional sampling is needed to more definitively characterize the teleomorphs of these species. However, the majority of species within clades B and C are morphologically and/or ecologically distinct (Figs 1, 2).
The majority of Cordyceps species in clade B are characterized by darkly pigmented, wiry, pliant or fibrous stromata. The dominant form of parasitism exhibited by these species is on subterranean or wood-inhabiting hosts, buried in soil or embedded in decaying wood, such as larval and pupal stages of arthropods. In contrast, Cordyceps species of clade C have brightly pigmented and fleshy stromata and parasitize their hosts in relatively more accessible environments, such as leaf litter, moss, or the uppermost soil layer. Exceptions to these morphological and ecological traits are found in some Cordyceps species in clade B. Cordyceps melolonthae, for example, produces brightly-coloured stromata, although it bruises dark upon handling and its hosts are the larvae of cockchafers or June beetles buried in soil (Mains 1958). Cordyceps unilateralis parasitizes adult ants, but is darkly pigmented with a wiry stroma and subterminal production of perithecia, and members of the C. sphecocephala clade are at least partially brightly pigmented and are restricted to adult stages of insects. These findings suggest that the traits described above are not universally informative, but collectively useful in characterizing Cordyceps species within clade B. That is, there have been gains, losses, and diversifications of most if not all traits during the evolution of these fungi, but general trends in character state evolution are evident.
The taxonomic utility of anamorphic forms in classification of Cordyceps
The genus Cordyceps is characterized by a diverse assemblage of
more than 25 anamorph genera (e.g., Beauveria Vuill.,
Hirsutella Pat., Hymenostilbe Petch, Isaria Fr.,
Lecanicillium W. Gams & Zare, Metarhizium, and
Tolypocladium W. Gams) (Kobayasi
1982, Samson et al.
1988, Gams & Zare
2003, Hodge 2003).
The anamorph genera of Cordyceps are hyphomycetes with conidiogenous
cells that are hyaline to brightly coloured and produce conidia in dry chains
or slimy drops (Samson et al.
1988). Some anamorph genera (e.g., Hymenostilbe) are
known as a useful diagnostic character in recognizing monophyletic groups of
Cordyceps species
(Artjariyasripong et al.
2001, Kobayasi
1941,
1982), while other anamorph
morphologies and genera are placed in more than one clade of the
Clavicipitaceae. Therefore, the distribution of anamorphic forms is
discussed to evaluate their phylogenetic utility in characterizing the three
clades of Cordyceps and Clavicipitaceae and to better
understand teleomorph–anamorph connections.
Anamorphs of Clavicipitaceae clade A
Clavicipitaceae clade A includes isolates of the anamorph genera
Aschersonia Mont., Metarhizium, Nomuraea Maublanc,
Pochonia Bat. & O.M. Fonseca, Paecilomyces s. l.,
Rotiferophthora G.L. Barron, Tolypocladium W. Gams, and
verticillium-like (Fig. 4).
Nomuraea, Paecilomyces, and Tolypocladium are found in other
clades of Clavicipitaceae (Figs
1,
2). Significantly,
Verticillium s. s. is known from the Plectosphaerellaceae,
which is closely related with the Glomerellaceae in the
Sordariomycetidae (Zare et al.
2007). Paecilomyces s. s. is in the Eurotiales
(Eurotiomycetidae), but species of Paecilomyces s. l. are
also present elsewhere in the Hypocreales
(Luangsa-ard et al.
2004). In contrast, the anamorph genera Aschersonia,
Metarhizium, Pochonia and Rotiferophthora are restricted to
clade A (Figs 1,
2).
Anamorph taxa of the C. taii subclade include Nomuraea rileyi (Farl.) Samson, Paecilomyces carneus (Duché & R. Heim) A.H.S. Brown & G. Smith and Pa. marquandii (Massee) S. Hughes, Pochonia, Tolypocladium parasiticum, and Metarhizium (Fig. 4). The genera Nomuraea, Pochonia and Tolypocladium are not monophyletic, although Pochonia is restricted to clade A. Nomuraea rileyi and Metarhizium are entomogenous; Pa. carneus is a common soil fungus considered a weak insect pathogen, while Pa. marquandii, Pochonia and T. parasiticum are also common soil fungi and can be parasitic on nematodes. Metarhizium is the only monophyletic anamorph genus of clade A (Fig. 4). The conidiogenous cells in the genus Metarhizium are cylindrical to clavate without a neck and produced in candelabrum-like or palisade-like fashion (Rombach et al. 1986, Driver et al. 2000, Evans 2003). The genus is most similar to Nomuraea and differs in the compact conidiophores that form a hymenial layer (Evans 2003). Nomuraea rileyi groups with species of Metarhizium, while N. atypicola (Yasuda) Samson belongs to the Pa. lilacinus clade in clade B. Interestingly, N. rileyi produces greenish-coloured conidia, as do species of Metarhizium in the C. taii subclade, while N. atypicola possesses lavender-coloured conidia similar to those of Pa. lilacinus (Coyle et al. 1990, Hywel-Jones & Sivichai 1995, Evans 2003). Currently, three teleomorphic species of Metarhizium (C. brittlebankisoides, C. campsosterni, and C. taii) have been reported (Liang et al. 1991, Liu et al. 2001, Zhang et al. 2004). The species M. taii was described with its teleomorph species, C. taii (Liang et al. 1991) and recently synonymized with M. anisopliae var. majus (Huang et al. 2005). Cordyceps brittlebankisoides was once also considered to have the anamorph M. anisopliae var. 0majus (Liu et al. 2001), but it is likened to M. flavoviride (Huang et al. 2005). In general, Metarhizium species show extensive variation in size and colour of conidia (Driver et al. 2000, Evans 2003) and more intensive sampling of anamorphs and teleomorphs is needed for this group.
The genus Tolypocladium is characterized by producing single or whorled (verticillate) conidiogenous cells (phialides), which are flask-shaped with enlarged bases that taper into a needle-like neck usually bent from the axis of the phialides (Gams 1971, Bissett 1983). The type of the genus Tolypocladium, T. inflatum W. Gams, is linked to the teleomorph C. subsessilis (Hodge et al. 1996, Gams & Zare 2003). Tolypocladium inflatum is placed in clade B and is distantly related to T. parasiticum in the C. taii clade. Tolypocladium parasiticum was described from the rotifer host Adineta and described with underwater conidiation (Barron 1980). Morphologically, T. parasiticum differs from other species of Tolypocladium, as it is the only member of the genus that produces chlamydospores in vivo (Barron 1980) and in culture (Bissett 1983, Zare et al. 2001, Gams & Zare 2003). In a recent treatment of Verticillium sect. Prostrata W. Gams, the genus Pochonia was also reclassified based on production of dictyochlamydospores or at least swollen hyphal cells (Gams & Zare 2001, Zare et al. 2001), supporting the close phylogenetic relationship of T. parasiticum and Pochonia species demonstrated in this study (Fig. 4). Hence, T. parasiticum is transferred to Pochonia below, rendering the remaining species in Tolypocladium monophyletic. Paecilomyces marquandii also produces infrequent chlamydospores in culture, as does the anamorph of Metacordyceps yongmunensis sp. nov. (discussed below). As suggested by Barron & Onions (1966), the presence of chlamydospores can be a taxonomically informative character.
The genus Aschersonia is a monophyletic lineage labelled as Hypocrella subclade (Fig. 4). The genus Aschersonia is characterized by its pycnidial or acervular conidiomata with hymenial phialides and its ecology of parasitizing only the nymphs of scale insects and whiteflies (Petch 1921, Hywel-Jones & Evans 1993). The teleomorphs of Aschersonia have long been linked to the species of Hypocrella and more than 25 species have been reported (Petch 1921, Mains 1959). While this study does not focus on sampling of Hypocrella and Aschersonia, these findings corroborate that the unique morphology of Aschersonia is phylogenetically informative and diagnostic of a monophyletic group of clavicipitaceous fungi (Fig. 4).
Anamorphs of Clavicipitaceae clade B
Clavicipitaceae clade B includes several anamorph genera including
Haptocillium W. Gams & Zare, Hirsutella, Hymenostilbe
and Tolypocladium (Fig.
6). Several of the anamorphic forms in the clade are
phylogenetically informative. Hirsutella and Hymenostilbe
occur dominantly in the C. unilateralis subclade.
Hirsutella is characterized by its typical basally-subulate phialides, narrowing into one (usually) or more (occasionally) very slender needle-like necks, on synnemata or mononematous mycelium (Hodge 1998, Gams & Zare 2003). Hirsutella species normally produce a few (<5) conidia in mucus and the phialides are not usually bent in their needle-like necks such as in the genus Tolypocladium, but also single conidia as in Hi. thompsonii F.E. Fisher. Not all Cordyceps species in the C. unilateralis subclade are connected to Hirsutella anamorphs. Some are connected to Paecilomyces s. l., Paraisaria Samson & B.L. Brady, and Syngliocladium Petch, whereas anamorphic forms are not known for many of the Cordyceps species, especially in the C. ravenelii subclade (e.g., C. heteropoda Kobayasi). However, most Cordyceps species in the rest of the C. unilateralis subclade have been linked to Hirsutella anamorphs (Fig. 6). These results suggest that Hirsutella anamorphs are phylogenetically informative for at least part of the C. unilateralis subclade or possibly symplesiomorphic for the C. unilateralis subclade as a whole.
The taxonomic utility of Hirsutella anamorphs is exemplified by the teleomorph–anamorph connection of the genus Cordycepioideus Stifler, a termite pathogen, which does not have typical ascospore and ascus morphologies of clavicipitaceous fungi (Blackwell & Gilbertson 1984, Suh et al. 1998). It possesses thick-walled multiseptate ellipsoid ascospores and its asci lack the thickened ascus tip characteristic of most clavicipitaceous fungi (Blackwell & Gilbertson 1984, Ochiel et al. 1997). The anamorph of Cordycepioideus bisporus Stifler is a synnematous Hirsutella that is either conspecific with or closely related to Hi. thompsonii (Ochiel et al. 1997, Suh et al. 1998, Sung et al. 2001). Although Cordycepioideus bisporus differs greatly from other members of the C. unilateralis subclade in its teleomorphic characters, molecular data strongly support it as a member of the C. unilateralis subclade, a finding consistent with its Hirsutella anamorph. It should be noted that species of Cordyceps outside of clade B have been described with atypical Hirsutella anamorphs (e.g., C. pseudomilitaris), but upon further investigation were more accurately characterized in other anamorph genera (e.g., Simplicillium W. Gams & Zare).
The C. unilateralis clade includes the members of the C. sphecocephala subclade, which possess a Hymenostilbe anamorph. The genus Hymenostilbe usually produces cylindrical to clavate conidiogenous cells, which are produced in a more or less dense palisade in synnemata (Samson et al. 1988). It is differentiated from closely related genera (e.g., Akanthomyces Lebert and Hirsutella) by its polyblastic conidiogenous cells, which holoblastically produce single conidia on short denticles or scars (Samson et al. 1988, Hywel-Jones 1996). The results from the present study indicate that Hymenostilbe anamorphs may be derived from within Hirsutella (Fig. 6). The close phylogenetic relationship between Hirsutella and Hymenostilbe anamorphs is exemplified by the morphologically intermediate synnematous Hirsutella/Hymenostilbe species. For example, Hy. lecaniicola (Jaap) Mains, the anamorph of C. clavulata (Schwein.) Ellis & Everh. (Hodge 1998), was previously classified in Hirsutella although it possesses extensively polyphialidic conidiogenous cells in a discontinuous layer (Mains 1950, 1958, Samson & Evans 1975, Hodge 1998). In addition, some Hirsutella species (e.g., Hi. rubripunctata Samson, H.C. Evans & Hoekstra) produce only a single conidium without a mucous sheath on denticles of extensively polyphialidic conidiogenous cells. Therefore, the modes of asexual reproduction in Hirsutella and Hymenostilbe may overlap to some extent and additional work is necessary to address the relationships between the two genera (Hodge 1998, Gams & Zare 2003).
In addition to the C. unilateralis subclade, the remaining three subclades contain Haptocillium, Tolypocladium and verticillium-like anamorphs. The genus Haptocillium was reclassified from the former Verticillium sect. Prostrata primarily based on its adhesive conidia and its ability to parasitize free-living nematodes (Zare & Gams 2001b). This study shows that the genus is a monophyletic group in the C. gunnii subclade (Fig. 6). However, the teleomorph–anamorph connection has not been established for any of the species in the clade or its close relative, C. gunnii, and thus its taxonomic utility remains unclear. The C. ophioglossoides and Pa. lilacinus subclades include anamorphic forms of Paecilomyces s. l., Nomu-raea, Tolypocladium, and verticillium-like, all of which are polyphyletic as previously discussed (Figs 1, 2; Oborník et al. 2001, Luangsa-ard et al. 2004, 2005). Several teleomorph–anamorph connections have been reported for Cordyceps species in the C. ophioglossoides and Pa. lilacinus subclades although their taxonomic utility is limited. Cordyceps subsessilis is known to be the teleomorph of Tolypocladium inflatum (Hodge et al. 1996) and C. ophioglossoides produces a verticillium-like anamorph (Gams 1971). In the Pa. lilacinus subclade, N. atypicola is linked to C. cylindrica (Evans & Samson 1987, Hywel-Jones & Sivichai 1995).
Anamorphs of Clavicipitaceae clade C
The anamorph genera sampled that are members of clade C include
Beauveria, Isaria, Lecanicillium, Microhilum H.Y. Yip & A.C.
Rath, and Simplicillium. Species of Lecanicillium and
Simplicillium were previously placed in Verticillium sect.
Prostrata and recently reclassified based on the phylogenetic studies
of Sung et al. (2001)
and Zare & Gams (2001a,
b). The genus
Lecanicillium is characterized by producing slender aculeate
phialides that are produced singly or in whorls and usually arise from
prostrate aerial hyphae (Zare & Gams
2001a). Conidia are mostly produced at the tip of phialides and
attached in heads or fascicles (Zare
& Gams 2001a). The morphological delimitation of
Simplicillium from Lecanicillium is difficult although the
species of Simplicillium tend to produce phialides that more or less
arise singly from prostrate aerial hyphae
(Zare & Gams 2001a). This
study shows again that the species of Lecanicillium form a
paraphyletic group, as species of other well-delimited anamorphic genera
(e.g., Beauveria, Engyodontium G.S. de Hoog, and Isaria) are
interspersed among species of Lecanicillium
(Fig. 8).
Some Lecanicillium species are known to be anamorphic forms of Cordyceps and Torrubiella (Petch 1932, Evans & Samson 1982, Zare & Gams 2001a). For example, C. militaris produces a Lecanicillium anamorph in culture (Zare & Gams 2001a) and the anamorph of Torrubiella alba Petch is L. aranearum (Petch) Zare & W. Gams (Petch 1932). The type species of Lecanicillium is L. lecanii (Zimm.) Zare & W. Gams, which is connected to the teleomorph T. confragosa Mains, a pathogen of scale insects (Evans & Samson 1982), which we transfer here to Cordyceps. In addition to Lecanicillium anamorphs, other genera (e.g., Akanthomyces, Gibellula Cavara, Hirsutella, Paecilomyces (Isaria), and Simplicillium) have also been linked to Torrubiella (Kobayasi & Shimizu 1982, Samson et al. 1988, 1989, Zare & Gams 2001a).
Clavicipitaceae clade C also includes the species of Isaria, the generic name of which has been conserved with I. farinosa (Holmsk.) Fr. as the type, for some of the clavicipitaceous Paecilomyces species (Gams et al. 2005, Luangsa-ard et al. 2005). The genus Paecilomyces was a diverse genus, with molecular studies indicating its polyphyletic status (Oborník et al. 2001, Luangsa-ard et al. 2004, 2005). The type species, Pa. variotii Bainier, belongs to the order Eurotiales (Ascomycota) and is distantly related to the clavicipitaceous Paecilomyces species that were previously classified in Paecilomyces sect. Isarioidea (Samson 1974, Luangsa-ard et al. 2004). The previous taxonomy of Paecilomyces was primarily based on the monographic study by Samson (1974), which included approximately 22 species in Paecilomyces sect. Isarioidea. In a recent molecular study, Luangsa-ard et al. (2005) demonstrated that species in Paecilomyces sect. Isarioidea are subdivided into four monophyletic groups, three of which are statistically supported. As a result, eleven species of Paecilomyces sect. Isarioidea were reclassified in Isaria (e.g., I. fumosorosea Wize, I. javanica (Frieder. & Bally) Samson & Hywel-Jones and I. tenuipes Peck) (Luangsa-ard et al. 2005). The present study indicates that the four isolates of Isaria do not form a monophyletic group in clade C, as they are interspersed among other anamorphic forms in the clade. Thus, the taxonomic utility of Isaria anamorph is limited to clade C, as seen with Lecanicillium and Simplicillium anamorphs. Furthermore, few connections have been made between teleomorphs of the Clavicipitaceae and species of Isaria. Kobayasi (1941) reported that the anamorph of C. takaomontana Yakush. & Kumaz. is Isaria japonica Yasuda, which Samson (1974) synonymized with Pa. tenuipes (= I. tenuipes). Isaria farinosa is the anamorph of C. memorabilis (Pacioni & Frizzi 1978), but was once mistakenly linked to C. militaris (Petch 1936). Isaria farinosa was also connected to two Torrubiella species, T. gonylepticida (A. Möller) Petch and T. pulvinata Mains. The anamorph of the latter was reported as Spicaria pulvinata Mains, and Petch described the conidial state of T. gonylepticida as Spicaria longipes Petch, two Spicaria species that Samson (1974) synonymized with Paecilomyces farinosus (= I. farinosa). Although T. gonylepticida was originally described in combination with Cordyceps, Petch (1937) transferred the species to its current combination and redescribed the species. Isaria farinosa has been reported to occur on six insect orders (Lepidoptera, Coleoptera, Hemiptera, Homoptera, Diptera, and Hymenoptera) and also on spiders (Araneae). The simplicity and plasticity in the morphology of most Isaria species make it difficult to set boundaries among and between sister-taxa and the search for better markers in species delimitation must be a goal for further studies.
The closely related species, C. scarabaeicola Kobayasi and C. staphylinidicola Kobayasi & Shimizu produce Beauveria anamorphs (Fig. 8; Sung 1996), and C. bassiana Z.Z. Li, C.R. Li, B. Huang & M.Z. Fan and C. brongniartii Shimazu are known as teleomorphs of B. bassiana (Bals.) Vuill. and B. brongniartii (Sacc.) Petch, respectively (Shimazu et al. 1988, Li et al. 2001). The genus Beauveria is morphologically well-characterized by producing basally-inflated conidiogenous cells that sympodially produce conidia on divergent denticles (MacLeod 1954, de Hoog 1972). Beauveria has a cosmopolitan distribution with quite a broad host range (Mugnai et al. 1989, Evans 2003, Rehner & Buckley 2005). A recent molecular study (Rehner & Buckley 2005) that included 87 isolates of five Beauveria species (B. amorpha (Höhn.) Samson & H.C. Evans, B. bassiana, B. brongniartii, B. caledonica Bissett & Widden, and B. vermiconia de Hoog & V. Rao) demonstrated that the genus is monophyletic and one of the more phylogenetically-informative anamorphs of clade C.
In fungal systematics, the naming of anamorphic forms is allowed for Phyla Ascomycota and Basidiomycota by Article 59 of the International Code of Botanical Nomenclature (McNeill et al. 2006) and multiple names exist for the same organisms of teleomorphic and anamorphic taxa. Recently, molecular phylogenetics has played an important role in integrating teleomorphic and anamorphic forms in a unified classification system in the clavicipitaceous fungi (Reynolds & Taylor 1993, Sung et al. 2001, Luangsa-ard et al. 2005). In such efforts, Verticillium sect. Prostrata and Paecilomyces sect. Isarioidea have recently been reclassified into several anamorphic genera (e.g., Haptocillium, Isaria, Lecanicillium, Pochonia, Rotiferophthora, and Simplicillium) to be consistent with the current hypotheses of relationships (Zare & Gams 2001a, Zare et al. 2001, Luangsa-ard et al. 2005). The phylogeny presented here further improves our understanding of the teleomorph–anamorph connections in Cordyceps and implies that several anamorphic genera (e.g., Beauveria, Hirsutella, Hymenostilbe, and Metarhizium) are more restricted in their phylogenetic distribution and therefore phylogenetically informative in characterizing Cordyceps species (Figs 4, 6, 8).
| TAXONOMIC REVISION |
|---|
|
|
|---|
|
The family Clavicipitaceae s. s. includes the grass-associated genera Balansia Speg., Claviceps, Epichloë (Fr.) Tul. & C. Tul., and Myriogenospora G.F. Atk., which were classified in Clavicipitaceae subfam. Clavicipitoideae sensu Diehl 1950 (Fig. 10). Recent molecular studies show that Aciculosporium I. Miyake, Atkinsonella Diehl, Heteroëpichloë E. Tanaka, C. Tanaka, Gafur & Tsuda, Neoclaviceps J.F. White, Bills, S.C. Alderman & Spatafora, and Parepichloë J.F. White & P.V. Reddy are also members of this clade, thus supporting their classification in the Clavicipitaceae s. s. (White & Reddy 1998, Sullivan et al. 2001, Tanaka et al. 2002). Clavicipitaceae s. s. also includes the plant-associated Shimizuomyces paradoxus Kobayasi, which occurs on seeds of Smilax (Smilacaceae). In addition to plant-associated fungi, Clavicipitaceae s. s. contains four arthropod-associated lineages. Three of the four arthropod-associated lineages are characterized as pathogens of scale insects, including Hypocrella (pathogens of scale insects and white flies; Hywel-Jones & Evans 1993, Hywel-Jones & Samuels 1998), Regiocrella P. Chaverri & K.T. Hodge (pathogen of scale insects; Chaverri et al. 2006), and Torrubiella luteorostrata Zimm. (pathogen of scale insects; Hywel-Jones 1993). The fourth lineage is described here as Metacordyceps; it comprises former species of Cordyceps and their related anamorphs and as a genus displays relatively broad arthropod host associations.
|
Stromata or subiculum darkly or brightly coloured, fleshy or tough. Perithecia superficial to completely immersed, ordinal or oblique in arrangement. Asci cylindrical with thickened ascus apex. Ascospores usually cylindrical and multiseptate, disarticulating into part-spores or non-disarticulating.
Type: Claviceps Tul., Ann. Sci. Nat. Bot., Sér. 3, 20: 43. 1853.
Teleomorphic genera: Aciculosporium, Atkinsonella, Balansia, Claviceps, Epichloë, Heteroepichloë, Hypocrella, Metacordyceps gen. nov., Myriogenospora, Neoclaviceps, Parepichloë, Regiocrella, Shimizuomyces.
Anamorphic genera: Aschersonia, Ephelis Fr., Metarhizium, Neotyphodium A.E. Glenn, C.W. Bacon & Hanlin, Nomuraea, paecilomyces-like, Pochonia, Sphacelia Lév., verticillium-like.
METACORDYCEPS G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, gen. nov. MycoBank MB504182.
Stromata solitaria vel nonnulla aggregata, simplicia vel ramosa. Stipes carnosus vel tenax, albidus, viridi-luteus vel viridulus, cylindricus vel sursum dilatatus. Pars fertilis cylindrica vel clavata. Perithecia partim vel omnino in stromate immersa, perpendicularia vel oblique inserta. Asci cylindrici, apice inspissato. Ascosporae cylindricae, multiseptatae, in cellulas diffrangentes vel maturae integrae remanentes.
Stromata solitary or several, simple or branched. Stipe fleshy or tough, whitish, greenish yellow to greenish, cylindrical to enlarging in fertile part. Fertile part cylindrical to clavate. Perithecia partially or completely immersed in stromata, ordinal or oblique in arrangement. Asci cylindrical with thickened ascus apex. Ascospores cylindrical, multiseptate, disarticulating into part-spores or remaining intact at maturity.
Type: Cordyceps taii Z.Q. Liang & A.Y. Liu
Etymology: Greek meta = behind, a genus close to Cordyceps (and suggesting relationship to Metarhizium).
Anamorphic genera: Metarhizium, Nomuraea, paecilomyces-like, Pochonia.
Commentary: The genus Metacordyceps is proposed for species of Cordyceps s. l. in the Clavicipitaceae s. s. based on the phylogenetic placement of C. taii (Figs 1, 2, 10). The genus is applied to the C. taii clade, which is strongly supported (MP-BP = 73 %, ML-BP = 78 %, PP = 1.00 in Figs 1, 2, 10). Among the members of the clade, the best-known taxon is the anamorphic genus Metarhizium, because of its importance in biological control (Samson et al. 1988, Evans 2003). Currently, three species of Cordyceps (viz., C. brittlebankisoides, C. campsosterni, and C. taii) are known as teleomorphs of Metarhizium (Liang et al. 1991, Liu et al. 2001, Zhang et al. 2004). The genus name Metacordyceps is here used to emphasize that the clade includes the species of Cordyceps s. l. that produce Metarhizium anamorphs although other species of Cordyceps (e.g., C. chlamydosporia) in the clade are not connected to Metarhizium anamorphs.
Metacordyceps yongmunensis G.H. Sung, J.M. Sung & Spatafora, sp. nov. MycoBank MB504183. Figs 5B, 5F-K, 11A-G.
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Stromata nonnulla vel raro singula, clavata, simplicia vel saepius ramosa, in chrysalidibus Lepidopterarum. Pars fertilis alba vel dilute lutea, a stipite haud distincta. Perithecia sparsa vel dense aggregata, partim immersa, brunneo-lutea, dilute brunnea vel aurantiobrunnea, oblique inserta, fusiformia vel clavata, 550–800 x 450–500 µm. Asci 8-spori, hyalini, cylindrici, 205–360 x 5–7 µm, apice conspicue inspissato. Ascosporae filiformes, hyalinae, inconspicue multiseptatae, haud fragmentatae, 180–345 x 1 µm. Anamorphe Pochoniae similis.
Stromata several or rarely solitary, clavate, simple or more usually branched, on pupa of Lepidoptera. Fertile area white to pale yellow, not differentiated from stipe. Perithecia scattered or crowded, loosely immersed, brownish yellow, pale brown to orangish brown, oblique in arrangement, fusiform to clavate, 550–800 x 450–500 µm. Asci 8-spored, hyaline, cylindrical, 205– 360 x 5–7 µm, possessing a prominent apical cap. Ascospores filiform, hyaline, multiseptate with indistinct septation, not fragmenting into part-spores, 180–345 x 1 µm. Conidiophores erect, produced in prostrate aerial hyphae. Phialides hyaline, solitary, awl-shaped, 20–28 x 2–2.2 µm. Conidia hyaline, elliptical to oblong, in slimy heads, 2–3.5 x 1.5–2.4 µm. Chlamydospores present.
Etymology: Yongmunensis in reference to the known locality of the first record of the species being Mt. Yongmun, Republic of Korea.
Known distribution: Republic of Korea.
Specimens examined: Mt. Yongmun, Gyunggi Province, Republic of Korea: 13 June 1998, EFCC 2131 (holotype); 13 June 1998, EFCC 2134; 13 June 1998, EFCC 2135; 30 June 1999, EFCC 3379; 30 June 1999, EFCC 3380; 29 Aug. 1999, EFCC 4342; 8 Aug. 1999, EFCC 4343; 8 June 2000, EFCC 49 1; 30 June 2004, EFCC 12287; 30 June 2004, EFCC 12288; 30 June 2004, EFCC 12291; 8 Aug. 2004, EFCC 12467. Mt. Chiak, Kangwon Province, Republic of Korea: 8 Aug. 2000, EFCC 5750. Bukbang-myun, Kangwon Province, Republic of Korea: 21 June 2002, EFCC 8808. Living culture in EFCC.
Commentary: Most specimens of M. yongmunensis possess several stromata (up to 10), on a large pupa of Lepidoptera deeply buried in soil (Fig. 5B). Stroma of the species is typically branched in a dichotomous way at its basal or upper regions (Fig. 5B). Perithecia are usually obliquely inserted in the stromata with a few exceptions that are ordinally arranged, i.e. at right angles to the surface of the stromata (Fig. 5B). While some perithecia are characterized by an acute narrowing of the perithecium at the ostiole, producing a narrow terminal end (Fig. 5F), others are not significantly narrowed (Fig. 11B). In the asci the ascospores are arranged parallel for their entire length and almost reach the ascus foot, suggesting that ascospores are of approximately the same length as the asci (Figs 5I, 11A). Unlike the distinct septation of ascospores as seen in C. militaris (Fig. 9O), the septa of the ascospores are indistinct and discharged ascospores do not disarticulate into part-spores (Figs 5K, 11A).
In the anamorph of M. yongmunensis, cultures derived from ascospores are moderately fast growing in SDAY (Sabouraud-dextrose-yeast extract agar) and the colonies reach 25–35 mm diam at 25 °C in 10 d. Colonies are slightly cottony without zonation and white with a green margin, remaining greenish brown at the reverse side of the cultures. Conidiophores are erect and produced in prostrate aerial hyphae. Phialides are solitary, not in whorls, broader at the base and tapering towards the end, measuring 20–28 x 2.0–2.2 µm (Fig. 11C). Conidia are in slimy heads (with usually 2 or 3 conidia) and ellipsoidal to oblong, measuring 2–3.5 x 1.5–2.4 µm (Fig. 11C). In submerged areas of the cultures, chlamydospores are developed in chains or reduced to intercalary swollen structures (Figs 11E-G). The anamorph of M. yongmunensis is best classified as pochonia-like because of its subulate phialides and production of chlamydospores, although verticillium-like whorls of phialides were not observed (Zare et al. 2001). In Metacordyceps, M. yongmunensis is most similar to M. chlamydosporia (= C. chlamydosporia) in the shape of perithecia and its anamorph. Both species produce brownish perithecia that possess long terminal ends in white or pale yellow stromata (Zare et al. 2001). The anamorph of M. chlamydosporia is identical with the type of Pochonia. Thus the production of chlamydospores can be informative for recognizing some species of Metacordyceps.
Accepted names and new combinations for Metacordyceps
The following taxa are accepted species of Metacordyceps based on
their inclusion in molecular phylogenies presented herein1 (see
Table 1) or morphological
descriptions matching the characters described above2. The known
anamorph connection is provided for the species of Metacordyceps.
Cordyceps brittlebankisoides ZuoY. Liu, Z.Q. Liang,
Whalley, Y.-J. Yao & A.Y. Liu, J. Invert. Pathol. 78: 179. 2001.
Cordyceps campsosterni W.M. Zhang & T.H. Li, Fungal
Diversity 17: 240. 2004. [as C. `campsosterna'].
Cordyceps chlamydosporia H.C. Evans, in Zare et
al., Nova Hedwigia 73: 59. 2001.
Cordyceps liangshanensis M. Zang, D. Liu & R. Hu, Acta
Bot. Yunnanica 4: 174. 1982.
Cordyceps taii Z.Q. Liang & A.Y. Liu, Acta Mycol. Sin.
10: 257. 1991.
New combinations for anamorphs associated with Metacordyceps
T. parasiticum is transferred to the genus Pochonia based
on molecular phylogenies presented herein1.
Tolypocladium parasiticum G.L. Barron, Canad. J. Bot. 58:
439. 1980.
CLAVICIPITACEAE Clade B
Clavicipitaceae clade B is strongly supported (MP-BP = 93 %, ML-BP
= 98 %, PP = 1.00 in Figs 1,
2,
10) and the family
Ophiocordycipitaceae is proposed for it with the type genus
Ophiocordyceps Petch. Most species of the
Ophiocordycipitaceae produce darkly pigmented stromata that are
pliant to wiry, or fibrous to tough in texture. Ecologically, many species of
the family are known as pathogens of subterranean or wood-inhabiting hosts,
buried in soil or embedded in decaying wood. Notable exceptions do exist to
these traits with brightly coloured species that may or may not attack adult
stages of hosts and occur in exposed habitats.
OPHIOCORDYCIPITACEAE G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, fam. nov. MycoBank MB504190.
Stromata vel subiculum fusca vel raro laete colorata, tenacia, fibrosa vel flexibilia, raro carnosa, saepe ostiolis peritheciorum prominentibus, summa saepe peritheciis carentia. Perithecia superficialia vel omnino immersa, perpendicularia ad superficiem vel oblique inserta. Asci cylindrici, apice inspissato. Ascosporae cylindricae, multiseptatae, maturae in cellulas diffrangentes vel integrae remanentes.
Stromata or subiculum darkly pigmented or rarely brightly coloured, tough, fibrous to pliant, rarely fleshy, often with aperithecial apices or lateral pads. Perithecia superficial to completely immersed, ordinal or oblique in arrangement. Asci usually cylindrical with thickened ascus apex. Ascospores usually cylindrical, multiseptate, disarticulating into part-spores or nondisarticulating.
Type: Ophiocordyceps Petch, Trans. Brit. Mycol. Soc. 16: 74. 1931.
Teleomorphic genera: Elaphocordyceps, Ophiocordyceps
Anamorphic genera: Haptocillium, Harposporium Lohde, Hirsutella, Hymenostilbe, paecilomyces-like, Paraisaria, Syngliocladium, Tolypocladium, verticillium-like.
ELAPHOCORDYCEPS G.H. Sung & Spatafora, gen. nov. MycoBank MB504191.
Stromata singula vel nonnulla aggregata, simplicia vel ramosa. Stipes fibrosus vel tenax, raro carnosus, obscure brunneus vel olivaceo-viridulus, raro albidus, cylindricus vel sursum dilatatus. Stromata hospite insidentia vel rhizomorphis eo conjuncta. Pars fertilis clavata vel capitata, raro indistincta. Perithecia partim wel omnino in stromate immersa, perpendicularia ad superficiem. Asci cyindrici, apice inspissato. Ascosporae cylindricae, multiseptatae, maturae in cellulas diffrangentes. Anamorphe Verticillii similis vel absens.
Stromata solitary to several, simple or branched. Stipe fibrous to tough, rarely fleshy, dark brownish to greenish with olivaceous tint, rarely whitish, cylindrical to enlarging in the fertile part. Stroma connected directly to the host or indirectly through rhizomorph-like structures. Fertile part clavate to capitate, rarely undifferentiated. Perithecia partially or completely immersed in stromata, ordinal in arrangement. Asci cylindrical with thickened ascus apex. Ascospores cylindrical, multiseptate, disarticulating into part-spores.
Type: Cordyceps ophioglossoides (Ehrh.) Link
Etymology: Greek elaphe = deer, from the host fungus, Elaphomyces.
Commentary: The C. ophioglossoides clade is strongly supported (MP-BP = 71 %, ML-BP = 88 %, PP = 100 in Figs 1, 2, 10) and includes species of Cordyceps s. l. that parasitize the truffle-like genus Elaphomyces and cicada nymphs (e.g., C. inegoënsis and C. paradoxa) and beetles (e.g., C. subsessilis) (Figs 6, 10). Currently, 22 species are anticipated to be included in the C. ophioglossoides clade, of which more than 18 species are known as parasites of Elaphomyces (Mains 1957, Kobayasi & Shimizu 1960, 1963). The host affiliation of Elaphomyces parasites has long been recognized as a diagnostic character in Cordyceps classification (Massee 1895, Kobayasi 1941, 1982, Mains 1957, 1958). The oldest applicable genus name is Cordylia Fr. 1818 (Massee 1895). However, it cannot be applied to the C. ophioglossoides clade because it is a homonym of Cordylia Pers. 1807 (Mains 1958), which is also homonym of Cordyla Lour. 1790 (Leguminosae). Therefore, the genus Elaphocordyceps is proposed based on the phylogenetic placement of C. ophioglossoides and applied to the well-supported C. ophioglossoides clade. Although C. subsessilis is morphologically and ecologically distinct, the genus is well recognized by its dominant ecology as being pathogens of Elaphomyces and cicadas. The darkly pigmented, fibrous stromata with more or less olivaceous tint are also good diagnostic characters for recognizing the species of Elaphocordyceps.
Anamorphic genera: Tolypocladium, verticillium-like.
Accepted names and new combinations for Elaphocordyceps
The following taxa are accepted species of Elaphocordyceps based
on their inclusion in molecular phylogenies presented herein1 (see
Table 1) or morphological
descriptions matching the characters described above2. Where known
we provide anamorph connection for the species of
Elaphocordyceps.
Sphaeria capitata Holmsk., Beata Ruris Otia Fungis Danicis
1: 38. 1790 : Fries, Syst. Mycol. 2: 324, 1823.
Torrubia capitata (Holmsk.: Fr.) Tul. & C. Tul., Sel.
Fung. Carpol. 3: 22. 1865.
Cordyceps capitata (Holmsk. : Fr.) Link., Handbuch zur
Erkennung der nutzbarsten und am häufigsten vorkommenden Gewächse 3:
347. 1833.
Cordyceps capitata var. canadensis (Ellis &
Everh.) Lloyd, Mycol. Writ. 5: 609. 1916.
Cordyceps agariciformis (Bolt.) Seaver, North Amer. Fl. 3:
33. 1910.
Cordyceps delicatistipitata Kobayasi, Bull. Natn. Sci.
Mus. Tokyo 5: 79. 1960 (as C. `delicatostipitata').
Cordyceps fracta Mains, Bull. Torrey Bot. Club 84: 250.
1957.
Cordyceps inegoënsis Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 292. 1963.
Cordyceps intermedia S. Imai, Proc. Imp. Acad. Tokyo 10:
677. 1934.
Cordyceps intermedia f. michinokuënsis
Kobayasi & Shimizu, Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 116. 1982.
Cordyceps japonica Lloyd, Mycol. Writ. 6: 913. 1920.
Cordyceps jezoënsis S. Imai, Trans. Sapporo Nat.
Hist. Soc. 11: 33. 1929.
Cordyceps longisegmentis Ginns, Mycologia 80: 219.
1988.
Cordyceps minazukiensis Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 117. 1982.
Cordyceps miomoteana Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 8: 118. 1982.
Sphaeria ophioglossoides Ehrh., in
Pers., Comment de Fung. Clavaef. p. 12. 1797: Fries, Syst. Mycol. 2: 324.
1823.
Torrubia ophioglossoides (Ehrh. : Fr.) Tul., Sel. Fung.
Carpol. 3: 20. 1865.
Cordyceps ophioglossoides (Ehrh. : Fr.) Link, Handbuck zur
Erkennung der nutzbarsten und am häufigsten vorkommenden Gewächse 3:
347. 1833.
Cordyceps ophioglossoides f. alba Kobayasi &
Shimizu ex Y.J. Yao, in Yao, Li, Pegler & Spooner, Acta. Mycol. Sin. 14:
257. 1995.
Cordyceps ophioglossoides f. cuboides Kobayasi,
Bull. Natn. Sci. Mus. Tokyo 5: 77. 1960.
Cordyceps paradoxa Kobayasi, Bull. Biogeogr. Soc. Japan 9:
156. 1939.
Cordyceps ramosa Teng, Sinensia 7: 810. 1936.
Cordyceps rouxii Cand., Mycotaxon 4: 544. 1976.
Cordyceps subsessilis Petch, Trans. Brit. Mycol. Soc. 21:
39. 1937.
Cordyceps szemaoënsis M. Zang, Acta Bot. Yunnanica
23: 295. 2001.
Cordyceps tenuispora Mains, Bull. Torrey Bot. Club 84:
247. 1957.
Cordyceps toriharamontana Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 305. 1963.
Cordyceps valliformis Mains, Bull. Torrey Bot. Club 84:
250. 1957.
Cordyceps valvatistipitata Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 5: 81. 1960 (as C. volvatostipitata').
Cordyceps virens Kobayasi, J. Jap. Bot. 58: 222. 1983. OPHIOCORDYCEPS Petch, Trans. Brit. Mycol. Soc. 16: 73. 1931 emend. G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
= Cordycepioideus Stifler, Mycologia 33: 83. 1941.
Stromata or subiculum darkly pigmented or rarely brightly coloured, tough, fibrous, pliant to wiry, rarely fleshy, often with aperithecial apices or lateral pads. Perithecia superficial to completely immersed, ordinal or oblique in arrangement. Asci hyaline, cylindrical, usually with thickened ascus apex, rarely fusoid to ellipsoid. Ascospores usually cylindrical, multiseptate, disarticulating into part-spores or non-disarticulating.
Type: Cordyceps blattae Petch, Trans. Brit. Mycol. Soc. 16: 74. 1931.
Anamorphic genera: Hirsutella, Hymenostilbe, Paraisaria, Syngliocladium.
Commentary: The C. unilateralis clade is strongly supported (MP-BP = 88 %, ML-BP = 88 %, PP = 1.00 in Figs 3, 10) and includes the species of Ophiocordyceps (e.g., C. acicularis and C. unilateralis) (Petch 1931, 1933). The genus Ophiocordyceps was proposed by Petch (1931, 1933) for species of Cordyceps that produce non-disarticulating ascospores. The genus was not accepted by subsequent workers who reclassified the species of Ophiocordyceps as Cordyceps subg. Ophiocordyceps (Kobayasi 1941) or in multiple subgenera of Cordyceps (Mains 1958). The type of Ophiocordyceps Petch is O. blattae (= C. blattae), but it was not available for this taxonomic treatment. According to the morphological description, it fits in the present generic concept. Because O. unilateralis is a well-known species that was included in the original publication of Ophiocordyceps (Petch 1931) and because additional Ophiocordyceps species (e.g., O. acicularis) are members of this clade, we apply the name Ophiocordyceps based on the placement of O. unilateralis. The genus Ophiocordyceps includes the most morphologically diverse group of the species of Cordyceps s. l. including the members of C. subg. Neocordyceps (Figs 6, 10). For most of the species in Ophiocordyceps, the stromata are fibrous to tough or wiry to pliant in texture and darkly pigmented in at least some part of the stroma. The genus includes many species of Cordyceps s. l. that produce perithecia in subterminal regions of the stromata resulting in aperithecial apices. Of particular note, Ophiocordyceps is characterized by the dominant occurrence of Hirsutella and Hymenostilbe anamorphs (Fig. 6). Although the genus Cordycepioideus possesses thick-walled multiseptate ellipsoid ascospores and its asci lack the thickened ascus tip of most clavicipitaceous fungi (Blackwell & Gilbertson 1984, Ochiel et al. 1997), this study indicates that the genus Cordycepioideus can be merged with Ophiocordyceps according to its placement in molecular analyses and because of the Hirsutella anamorph (Fig. 10, Ochiel et al. 1997, Suh et al. 1998).
Ophiocordyceps communis Hywel-Jones & Samson, sp. nov. MycoBank MB504216. Figs 12A–G.
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Stromata ex duabus (tribus) termitis adultis oriunda, mycelio albo circumdata, filiformia; 50–100 mm sub superficie stramenti oriunda, 300–600 µm lata, albido-grisea, 70–130 mm super stramentum emergentia, 600–1000 µm lata, cuius 30–40 mm pars inferior hyphis sterilibus dematiaceis (luteo-brunneis) tomentosa; pars superior, ca 90 mm longa, fertilis, levis, griseo-brunnea vel grisea, conidia in strato griseo ferens et perithecia dense aggregata. Perithecia superficialia, subterminalia, 285–675 x 195–390 µm. Asci apice conspicue inspissato, 8-spori, filiformes, 215–250 x 15 µm. Ascosporae integrae, crassitunicatae, dilute pigmentatae, (100–)120–150(–180) x 5–6 µm. Cellulae conidiogenae hymenium hyalinum formantes, cylindricae, 10–14 x 2.7–3.3 µm, unum (raro duos) denticulos fertiles apicales ferentes. Blastoconidia hyalina, amygdaliformia, 8–9 x 2.5–3 µm. Anamorphe Hirsutellae vel Hymenostilbe similis.
Hosts two (rarely three) adult termites surrounded by loose, coarse white mycelium. Stromata filiform, 50–100 mm below ground, 300–600 µm wide, whitish-grey; 70–130 mm emerging above leaf litter, 600–1000 µm wide; lower 30–40 mm of above-ground portion usually hirsute with sterile, dematiaceous (yellow-brown) hairs becoming smooth, silver-brown to grey along terminal fertile (anamorph) part of ca 90 mm. Perithecia superficial subterminal; emerging through grey anamorph, tightly packed around the stipe, 285–675 x 195–390 µm. Asci with stout cap, 8-spored, filiform, 215–250 x 15 µm. Ascospores whole, stout, lightly pigmented (100–)120–150(–180) x 5–6 µm. Conidiogenous cells in a palisade, hyaline, cylindrical, 10–14 x 2.7–3.3 µm, solitary (rarely two), prominent, terminal denticle. Conidia hyaline, almond-shaped, 7–9 x 2.5–3 µm.
Etymology: refers to the communal nature of the stromata, i.e. the fact that 600–1000 Cordyceps stromata can be found in a small area (20 x 20 metres).
Type: Holotype: N.H.J. 10673, isotypes: N.H.J. 10674, N.H.J. 10675, N.H.J. 10676, N.H.J. 10677, all on termites; coll. R. Nasit; Khao Yai National Park, Gong Giao Nature Trail; 13 June 2000.
Commentary: Most collections of O. communis were from Khao Yai National Park with the type locality (Gong Giao Nature Trail) regularly having epizootics containing (in any one season) several hundred stromata over a 20 x 20 metre area. A few other collections were from Khao Soi Dao Wildlife Sanctuary (N.H.J. 6422 and N.H.J. 6452) and Sam Lan National Park (N.H.J. 6332). All collections of the species were from adult termites. Although surveys were made over an eighteen-year period from the far north of Thailand to the far south and from sea level to over 2500 metres, O. communis is only known from these three sites in central Thailand below 800 metres elevation.
In any year there appeared to be a single `flush' with O. communis first appearing at the start of the rainy season in May/June. The earliest collections were made in May (10 May 1994: N.H.J. 3687, N.H.J. 3681 and N.H.J. 3683, Heo Sawat Waterfall; 23 May 1996; N.H.J. 6330, Gong Giao Nature Trail). In the first 2–3 weeks after appearance, the stromata appeared slender and acicular with the lower part having a shiny silken appearance and the terminal part dull greyish. The terminal grey region consisted of a palisade of tightly packed conidiogenous cells with typically a stout elongate denticle, giving rise to a single conidium.
This anamorph is intermediate between a typical Hirsutella (e.g., Hi. formicarum, Hi. citriformis, and Hi. saussurei) and a typical Hymenostilbe (e.g., Hy. dipterigena – closer to the latter) (Figs 12F–G). The palisade of crowded conidiogenous cells is indicative of Hymenostilbe rather than Hirsutella, where conidiogenous cells are sparse and mostly immature at any given time (Fig. 12F). The denticulate nature of the conidiogenous cell also is indicative of Hymenostilbe. However, in all specimens examined to date there is no evidence of multiple denticles (five or more) usually associated with Hymenostilbe; only a few conidiogenous cells were seen with two denticles (Figs 12F–G).
The anamorph of O. communis is closest to Hy. ventricosa Hywel-Jones (Hywel-Jones 1995). That species infects cockroaches and is found attached to the under side of leaves. As with the anamorph of O. communis, Hy. ventricosa produces conidiogenous cells with only a single terminal stout denticle. Conidia of Hy. ventricosa have a pronounced point and are not typical of the clavate shape usually associated with Hymenostilbe. Similarly, the conidia of the O. communis anamorph are also fattened naviculate, appearing similar to those of Hy. ventricosa but without the processed tip.
The perithecia erupt through the dull greyish anamorph spike appearing first as longitudinal splits in the palisade of conidiogenous cells at the base of the anamorph spike. Each develops as a superficial perithecium, but they become crowded and give the overall appearance of a brown subterminal fertile region (Kobayasi 1941; Figs 12A–B). The ascus shape and the form of the ascus cap comes close to Kobayasi's Figs 12C–D (Kobayasi 1941) being typical of species in the C. unilateralis clade (with Hirsutella as an anamorph). Mature perithecia eject pigmented, whole ascospores (Fig. 12E) and often the ostiole becomes blocked with these half-emerged ascospores.
Only a few species of Cordyceps sensu Kobayasi and Mains have been reported from termites. Currently accepted species include O. koningsbergeri (= C. koningsbergeri Penz. & Sacc.), which is known only from the type locality (Java, Indonesia) (Kobayasi 1941), and C. termitophila Kobayasi & Shimizu) which is known from Japan and Taiwan (Kobayasi & Shimizu 1976, 1978). Penzig & Saccardo (1904) found O. koningsbergeri to be similar to O. myrmecophila in that it had a terminal, globose head with immersed perithecia. In this feature alone it differs significantly from O. communis with its subterminal and superficial perithecia. However, as with O. communis, Penzig & Saccardo (1904) described whole ascospores of O. koningsbergeri, which were 150 x 1 µm compared with 120–150 x 5–6 µm for O. communis. Cordyceps termitophila differs from O. communis in having a `pale rosy-grey' stroma, much smaller perithecia (280–320 x 175–190 µm for C. termitophila versus 285–675 x 195–390 µm for O. communis) and smaller ascospores (100–125 x 3 µm).
Accepted names and new combinations for Ophiocordyceps
The following taxa are accepted species of Ophiocordyceps based on
their inclusion in molecular phylogenies presented herein1 or
morphological descriptions matching the characters described
above2. Where known, the anamorph connection is provided for the
species of Ophiocordyceps.
Cordyceps acicularis Ravenel, J. Linn. Soc. 1: 158.
1857.
Cordyceps agriotidis A. Kawam., Icon. Jap. Fungi 8: 837.
1955. [as C. `agriota']
Cordyceps ainictos A. Möller, Phycomyceten u.
Ascomyceten, p. 226. 1901.
Cordyceps amazonica Henn., Hedwigia 43: 247. 1904.
Cordyceps amazonica var. neoamazonica Kobayasi
& Hara, J. Jap. Bot. 57: 17. 1982.
Cordyceps aphodii Mathieson, Trans. Brit. Mycol. Soc. 32:
134. 1949.
Cordyceps appendiculata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 6. 1983.
Cordyceps arachneicola Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku, Sect. B,: 123. 1941.
Cordyceps arbuscula Teng, Sinensia 7: 812. 1936.
Cordyceps armeniaca Berk. & M.A. Curtis, J. Linn. Soc.
1: 158. 1857.
Cordyceps asyuënsis Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 6: 138. 1980.
Cordyceps aurantia Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 125. 1980.
Cordyceps unilateralis var. australis Speg.,
Anales Soc. Ci. Argent. 12: 215. 1881.
Cordyceps australis (Speg.) Speg., Syll. Fung. 2: 571.
1883.
Cordyceps barnesii Thwaites, J. Linn. Soc. 14: 110.
1875.
Torrubia barnesii (Thwaites) Ces., Atti Accad. Sci. Fis.
Mat., Napoli 8: 14. 1879.
Cordyceps bicephala Berk., J. Bot. (Hooker) 8: 278.
1856.
Cordycepioideus bisporus Stifler, Mycologia 33: 85.
1941.
Cordyceps blattae Petch, Trans. Brit. Mycol. Soc. 10: 35.
1924.
Cordyceps brunneipunctata Hywel-Jones, Mycol. Res. 99:
1195. 1995. [as C. `brunneapunctata']
Cordyceps caloceroides Berk. & M.A. Curtis, J. Linn.
Soc. 10: 375. 1868.
Cordyceps cantharelloides Samson & H.C. Evans, Proc.
Indian Acad. Sci., Pl. Sci. 94: 312. 1985.
Cordyceps carabidicola Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 85. 1980. [as C. `carabidiicola']
Cordyceps cicadicola Teng, Sinensia 6: 191. 1935.
Cordyceps clavata Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 140. 1980.
Sphaeria clavulata Schwein., Trans. Amer. Philos. Soc. New
Ser. 4, 188. 1832.
Xylaria clavulata (Schwein.) Berk. & M. A. Curtis, J.
Linn. Soc. 10: 380. 1868.
Torrubia clavulata (Schwein.) Peck, Ann. Rep. N. Y. State
Mus. 28: 70. 1876.
Cordyceps clavulata (Schwein.) Ellis & Everh., North
Amer. Pyrenom. p. 61. 1892.
Torrubia pistillariiformis (Berk. & Broome) Cooke,
Handb. Brit. Fungi 2: 771. 1871.
Cordyceps coccidiicola Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 4: 57. 1978.
Torrubia coccigena Tul. & C. Tul., Sel. Fung. Carpol.
3: 19. 1865.
Cordyceps coccigena (Tul. & C. Tul.) Sacc., Michelia
1: 320. 1879.
Cordyceps cochlidiicola Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 6: 128. 1980.
Cordyceps corallomyces A. Möller, Phycomyceten u.
Ascomyceten, p. 217. 1901.
Cordyceps crassispora M. Zang, D.R. Yang & C.D. Li,
Mycotaxon 37: 58. 1990.
Cordyceps crinalis Ellis ex Lloyd, Mycol. Writ. 6: 912.
1920.
Cordyceps cucumispora H.C. Evans & Samson, Trans.
Brit. Mycol. Soc. 79: 442. 1982.
Cordyceps cucumispora var. dolichoderi H.C. Evans
& Samson, Trans. Brit. Mycol. Soc. 79: 445. 1982.
Torrubia curculionum Tul. & C. Tul., Sel. Fung.
Carpol. 3: 20. 1865.
Cordyceps curculionum (Tul. & C. Tul.) Sacc., Michelia
1: 320. 1879.
Cordyceps bicephala subsp. curculionum (Tul.
& C. Tul.) Moureau, Mém. Inst. Roy. Colon. Belge 7: 50. 1949.
Cordyceps cylindrostromata Z.Q. Liang, A.Y. Liu & M.H.
Liu, Fungal Diversity 14: 97. 2003.
Cordyceps dayiensis Z.Q. Liang, Fungal Diversity 12: 131.
2003.
Cordyceps dermapterigena Z.Q. Liang, A.Y. Liu & M.H.
Liu, Fungal Diversity 14: 96. 2003 (as C. `dermapteoigena').
Cordyceps dipterigena Berk. & Broome, J. Linn. Soc.
14: 111. 1875.
Cordyceps discoideicapitata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 85. 1982 (as C.
`discoideocapitata').
Cordyceps ditmarii Quél., Bull. Soc. Bot. France
24: 330 1877. [as C. ditmari]
Cordyceps dovei Rodway, Paper Proc. Roy. Soc. Tasmania for
1898–1899, p. 101. 1900.
Cordyceps elateridicola Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 4. 1983.
Cordyceps elongata Petch, Trans. Brit. Mycol. Soc. 21: 47.
1937.
Cordyceps elongatiperitheciata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 6: 126. 1980 (as C.
`elongatoperitheciata').
Cordyceps elongatistromata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 12. 1983 (as C.
`elongatostromata').
Cordyceps emeiensis A.Y. Liu & Z.Q. Liang, Mycosystema
16: 139. 1997.
Cordyceps engleriana Henn., Bot. Jahrb. Syst. 23: 538.
1897.
Sphaeria entomorrhiza Dicks., Plant. Crypt. Brit., Fasc.
1: 22. 1785.
Cordyceps entomorrhiza (Dicks.) Fr., Obs. Mycol. 2: 317.
1818.
Torrubia entomorrhiza (Dicks.) Tul. & C. Tul, Sel.
Fung. Carpol. 3: 13. 1865.
Cordyceps cinerea (Tul. & C. Tul.) Sacc., Michelia 1:
320. 1879.
Cordyceps evdogeorgiae Koval, Bot. Mater. Otd. Sporov.
Rast. 14: 160. 1961.
Cordyceps falcata Berk., J. Bot. (Hooker) 6: 211. 1854
[Decad. Fung. No. 479].
Cordyceps falcatoides Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 91. 1980.
Cordyceps fasciculatistromata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 83. 1982 (as C.
`fasciculatostromata').
Cordyceps ferruginosa Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 139. 1980.
Cordyceps filiformis Moureau, Mém. Inst. Roy.
Colon. Belge 7: 14. 1949.
Cordyceps formicarum Kobayasi, Bull. Biogeogr. Soc. Japan
9: 28. 1939.
Cordyceps forquignonii Quél., 16th Suppl. Champ.
Jura et Vosges, p. 6. 1887.
Cordyceps furcicaudata Z.Q. Liang, A.Y. Liu & M.H.
Liu, Fungal Diversity 14: 95. 2003 (as C. `furcicaodata').
Cordyceps gansuënsis K. Zhang, C. Wang & M. Yan,
Trans. Mycol. Soc. Japan 30: 295. 1989.
Cordyceps geniculata Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 85. 1980.
Torrubia gentilis Ces., Atti Accad. Sci. Fis. Mat.,
Napoli, 8: 14. 1879.
Cordyceps gentilis (Ces.) Sacc., Syll. Fung. 2: 569.
1883.
Cordyceps glaziovii Henn., Naturw. Wochenschr. 6: 318.
1896.
Cordyceps goniophora Speg., Bol. Acad. Nac. Ci.
Córdoba 11: 307 1889.
Cordyceps gracilioides Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku, Sect. B, 5: 140. 1941.
Xylaria gracilis Grev., Scot. Crypt. Fl. 2. t. 8.
1824.
Cordyceps gracilis (Grev.) Durieu & Mont., Fl.
Algérie Crypt. 1: 449. 1846.
Cordyceps gryllotalpae Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku 5: 70. 1942 [non Lloyd 1924].
Cordyceps koreana Kobayasi, Bull. Natn. Sci. Mus. Tokyo,
Ser. B, 7: 8. 1981.
Cordyceps heteropoda Kobayasi, Bull. Biogeogr. Soc. Japan
9: 158. 1939.
Cordyceps hiugensis Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 3. 1983.
Cordyceps huberiana Henn., Hedwigia 48: 105. 1909.
Cordyceps humbertii C.P. Robin, in Tul. & C. Tul.,
Sel. Fung. Carpol. 3: 18. 1865 (as C. `humberti').
Cordyceps insignis Cooke & Ravenel, Grevillea 12: 38.
1883.
Cordyceps irangiensis Moureau, Lejeunia, Mém. 15:
33. 1961.
Cordyceps japonensis Hara, Bot. Mag. Tokyo 28: 351.
1914.
Cordyceps jiangxiensis Z.Q. Liang, A.Y. Liu & Yong C.
Jiang, Mycosystema 20: 30. 2001.
Cordyceps jinggangshanensis Z.Q. Liang, A.Y. Liu &
Yong C. Jiang, Mycosystema 20: 307. 2001.
Cordyceps kangdingensis M. Zang & N. Kinjo, Mycotaxon
66: 221. 1998.
Cordyceps kniphofioides H.C. Evans & Samson, Trans.
Brit. Mycol. Soc. 79: 434. 1982.
Cordyceps kniphofioides var. dolichoderi H.C.
Evans & Samson, Trans. Brit. Mycol. Soc. 79: 437. 1982.
Cordyceps kniphofioides var. monacidis H.C. Evans
& Samson, Trans. Brit. Mycol. Soc. 79: 439. 1982.
Cordyceps kniphofioides var. ponerinarum H.C.
Evans & Samson, Trans. Brit. Mycol. Soc. 79: 441. 1982.
Cordyceps koningsbergeri Penz. & Sacc., Malpighia 11:
522. 1897.
Cordyceps konnoana Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 84. 1980.
Cordyceps lachnopoda Penz. & Sacc., Malpighia 11: 521.
1897.
Sphaeria larvarum Westwood, Proc. Entomol. Soc. Lond. 2:
6. 1836.
Cordyceps larvarum (Westwood) Olliff, Gaz. New South Wales
6: 410. 1895.
Cordyceps lloydii H.S. Fawc., Ann. Mag. Nat. Hist., Ser.
5, 18: 317. 1886.
Cordyceps lloydii var. binata H.C. Evans &
Samson, Trans. Brit. Mycol. Soc. 82: 133. 18: 31. 1984.
Cordyceps longissima Kobayasi, Bull. Natn. Sci. Mus. Tokyo
6: 300. 1963.
Cordyceps lutea Moureau, Mém. Inst. Roy. Colon.
Belge 7: 41. 1949.
Cordyceps macularis (Mains) Mains, Pap. Michigan Acad.
Sci. 25: 82. 1940.
Torrubia melolonthae Tul. & C. Tul., Sel. Fung.
Carpol. 3: 12. 1865.
Cordyceps melolonthae (Tul. & C. Tul.) Sacc., Michelia
1: 320. 1879.
Cordyceps rickii Lloyd, Mycol. Writ. 6: 914. 1920.
Cordyceps melolonthae var. rickii (Lloyd) Mains,
Mycologia 50: 198 1958.
Cordyceps michiganensis Mains, Proc. Amer. Philos. Soc.
74: 266. 1934.
Cordyceps minutissima Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 77. 1980.
Cordyceps monticola Mains, Mycologia 32: 310. 1940.
Cordyceps mrciensis Aung, J.C. Kang, Z.Q.Liang, Soytong
& K.D. Hyde, Mycotaxon 97: 236. 2006.
Cordyceps multiaxialis M. Zang & Kinjo, Mycotaxon 66:
224. 1998.
Cordyceps myrmecophila Ces., Bot. Zeitung 4: 877.
1846.
Torrubia myrmecophila (Ces.) Tul. & C. Tul., Sel.
Fung. Carpol. 3: 18. 1865.
Cordyceps neovolkiana Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku, Sect. B, 5: 169. 1941.
Cordyceps nepalensis M. Zang & Kinjo, Mycotaxon 66:
224. 1998.
Cordyceps nigra Samson, H.C. Evans & E.S. Hoekstra,
Proc. K. Ned. Akad. Wet., Ser. C, Biol. Med. Sci. 85: 596. 1982.
Cordyceps nigrella Kobayasi & Shimizu, Icon. Veg.
Wasps and Plant Worms p. 145. 1983.
Cordyceps nigra Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo 9(1): 13. 1983 [non Samson et al. 1982]
Cordyceps nigripes Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 8: 116. 1982 (as C. `nigripoda').
Cordyceps nutans Pat., Bull. Soc. Mycol. France 3: 127.
1887.
Cordyceps bicephala subsp. nutans (Pat.) Moureau,
Mém. Inst. Roy. Colon. Belge 7: 47. 1949.
Cordyceps obtusa Penz. & Sacc., Malpighia 11: 523.
1897.
Cordycepioideus octosporus M. Blackwell & Gilb.,
Mycologia 73: 358. 1981.
Cordyceps odonatae Kobayasi, Bull. Natn. Sci. Mus. Tokyo,
Ser. B, 7: 6. 1981.
Cordyceps osuzumontana Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 77. 1980.
Cordyceps owariensis Kobayasi, Bull. Biogeogr. Soc. Japan
9: 166. 1939.
Cordyceps owariensis f. viridescens Uchiyama
& Udagawa, Mycoscience 43: 136. 2002.
Cordyceps oxycephala Penz. & Sacc., Malpighia 11: 521.
1897.
Cordyceps sphecocephala f. oxycephala
(Penz. & Sacc.) Kobayasi, Trans. Mycol. Soc. Japan 23: 361. 1982.
Cordyceps paludosa (Mains) Mains, Pap. Michigan Acad. Sci.
25: 83. 1940.
Cordyceps pentatomae Koval, Nov. Sist. Niz. Rast. 1: 166.
1964. (as C. `pentatomi')
Cordyceps petchii Mains, Bull. Torrey Bot. Club 86: 47.
1959.
Cordyceps ramosa Petch, Trans. Brit. Mycol. Soc 21: 42.
1937 [non Teng 1936].
Cordyceps proliferans Henn., Hedwigia 43: 248. 1904.
Cordyceps pseudolloydii H.C. Evans & Samson, Trans.
Brit. Mycol. Soc. 82: 133. 1984.
Cordyceps pseudolongissima Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 119. 1982.
Cordyceps purpureostromata Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 6: 136. 1980. Type Shimizu No. 128, preserved in TNS; therefore
the basionym was valid from the beginning.
Cordyceps purpureostromata f. recurvata Kobayasi,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 6: 138. 1980.
Cordyceps ravenelii Berk. & M.A. Curtis, J. Linn. Soc.
1: 159. 1857.
Cordyceps rhizoidea Höhn., Sitzungsber. Kaiserl.
Akad. Wiss. Wien 118: 307. 1909.
Cordyceps ridleyi Massee, Bull. Misc. Inform. Roy. Bot.
Gard. Kew, p. 173. 1899.
Sphaeria robertsii Hook. Icon. Plant. 1 pl. 6. 1837.
Cordyceps robertsii (Hook.) Berk., Fl. New Zealand 2: 202.
1855.
Cordyceps rubripunctata Moureau, Mém. Inst. Roy.
Colon. Belge 7: 26. 1949.
Cordyceps rubiginosiperitheciata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 9: 14. 1983 (as C.
`rubiginosoperitheciata').
Cordyceps ryogamiensis Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 4. 1983.
Cordyceps salebrosa Mains, Mycologia 39: 541. 1947.
Cordyceps scottiana Olliff, Agric. Gaz. New South Wales 6:
407. 1895.
Cordyceps selkirkii Olliff, Agric. Gaz. New South Wales 6:
411. 1895.
Cordyceps sichuanensis Z.Q. Liang & B. Wang, Fungal
Diversity 12: 129. 2003.
Sphaeria sinensis Berk., J. Bot. (Hooker) 2: 207.
1843.
Cordyceps sinensis (Berk.) Sacc., Michelia 1: 320.
1879.
Cordyceps smithii Mains, J. Elisha Mitchell Sci. Soc. 55:
127. 1939.
Clavaria sobolifera Hill ex Watson, Philos. Trans. Roy.
Soc. Lond. 53: 271. 1763.
Sphaeria sobolifera (Hill ex Watson) Berk., J. Bot.
(Hooker) 2: 207. 1843.
Torrubia sobolifera (Hill ex Watson) Tul. & C. Tul.,
Sel. Fung. Carpol. 3: 10. 1865.
Cordyceps sobolifera (Hill ex Watson) Berk. & Broome,
J. Linn. Soc. 14: 110. 1875.
Sphaeria sphecocephala Klotzsch ex Berk., J. Bot. (Hooker)
2: 206. 1843.
Torrubia sphecocephala (Klotzsch ex Berk.) Tul. & C.
Tul., Sel. Fung. Carpol. 3: 18. 1865.
Cordyceps sphecocephala (Klotzsch ex Berk.) Berk. &
M.A. Curtis, in Berkeley, J. Linn. Soc., Bot. 10: 376. 1868.
Cordyceps stipillata Z.Q. Liang & A.Y. Liu,
Mycosystema 21: 11. 2002.
Cordyceps stylophora Berk. & Broome, J. Linn. Soc. 1:
158. 1857.
Cordyceps subflavida Mains, Bull. Torrey Bot. Club 86: 47.
1959.
Cordyceps albida Pat. & Gaillard, Bull. Soc. Mycol.
France 7: 116. 1888 [non Berk. & M.A. Curtis ex Cooke 1884].
Cordyceps subunilateralis Henn., Hedwigia 41: 168.
1902.
Torrubia superficialis Peck, Rep. N. Y. State Botanist 28:
70. 1876.
Cordyceps superficialis (Peck) Sacc., Syll. Fung. 2: 574.
1883.
Cordyceps superficialis f. crustacea Kobayasi
& Shimizu, Bull. Natn. Sci. Mus. Tokyo, Ser. B, 6: 82. 1980.
Cordyceps sobolifera var. takaoënsis
Kobayasi, Bull. Biogeogr. Soc. Japan 9: 165. 1939.
Cordyceps takaoënsis (Kobayasi) Kobayasi, Sci. Rep.
Tokyo Bunrika Daigaku, Sect. B, 5: 130. 1941.
Sphaeria taylorii Berk., J. Bot. (Hooker) 2: 209.
1843 (as S. `taylori').
Cordyceps taylorii (Berk.) Sacc., Michelia 1: 320.
1879.
Cordyceps thyrsoides A. Möller, Phycomyceten u.
Ascomyceten, p. 221. 1901.
Cordyceps tricentri Yasuda, in Lloyd, Mycol. Writ. 4: 568.
1915 (as C. `tricentrus').
Cordyceps uchiyamae Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 125. 1980.
Torrubia unilateralis Tul. & C. Tul., Sel. Fung.
Carpol. 3: 18. 1865.
Cordyceps unilateralis (Tul. & C. Tul.) Sacc., Syll.
Fung. 2:570. 1883.
Cordyceps formicivora (Tul. & C. Tul.) J.
Schröt., Krypt.-Fl. Schlesien 3(2) 27. 1894.
Cordyceps unilateralis var. clavata (Kobayasi)
Kobayasi, Sci. Rep. Tokyo Bunrika Daigaku, Sect. B, 5: 78. 1941.
Cordyceps variabilis Petch, Trans. Brit. Mycol. Soc. 21:
42. 1937.
Cordyceps voeltzkowii Henn., in Voeltzkow, Reise Ostafrica
3: 29. 1908.
Cordyceps volkiana A. Möller, Phycomyceten u.
Ascomyceten, p. 233. 1901.
Cordyceps wuyishanensis Z.Q. Liang, A.Y. Liu & J.Z.
Huang, Mycosystema 21: 162. 2002.
Cordyceps yakusimensis Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 302. 1963.
Cordyceps zhangjiajiensis Z.Q. Liang & A.Y. Liu,
Mycosystema 21: 163. 2002.
CLAVICIPITACEAE Clade C
Clavicipitaceae clade C is a strongly supported group that
includes the type species, C. militaris, of Cordyceps (MP-BP
= 100 %, ML-BP = 100 %, PP = 1.00 in Figs
1,
2). Because of the
non-monophyly of Cordyceps, we reintroduce the preexisting family
name Cordycipitaceae for Clavicipitaceae clade C. This
family name was not validly published and it is validated herein based on the
type genus Cordyceps. Most of the species in the family parasitize
hosts in leaf litter, moss, or upper soil layers and produce superficial to
partially immersed to completely immersed perithecia on a fleshy stroma or
subiculum that is pallid or brightly coloured. The family contains species of
Cordyceps and Torrubiella (Figs
5,
7). The unispecific genus
Phytocordyceps is also recognized as a member of this family and
transferred to Cordyceps (Fig.
6). In addition, the recent molecular study shows that species of
the genera Ascopolyporus A. Möller and Hyperdermium J.
White, R. Sullivan, G. Bills & N. Hywel-Jones 2000 [non Link], both
pathogens of scale insects, are also inferred to be members of the family
(Sullivan et al.
2000, Bischoff et al.
2005).
CORDYCIPITACEAE Kreisel 1969 ex G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, fam. nov. MycoBank MB504360.
Cordycipitaceae Kreisel, Grundz. Natürl. Syst. Pilze: 112. 1969 [nom. inval., Art. 36].
Stromata vel subiculum pallida vel laete colorata, carnosa. Perithecia superficialia vel omnino immersa, perpendicularia ad superficiem. Asci cylindrici, apice inspissato. Ascosporae cylindricae, multiseptatae, maturae diffrangentes vel integrae remanentes.
Stromata or subiculum pallid or brightly pigmented, fleshy. Perithecia superficial to completely immersed, oriented at right angles to the surface of the stroma. Asci cylindrical with thickened ascus apex. Ascospores usually cylindrical, multiseptate, disarticulating into part-spores or remaining intact at maturity.
Type: Cordyceps Fr.
Teleomorphic genera: Ascopolyporus, Cordyceps, Hyperdermium, Torrubiella.
Anamorphic genera: Beauveria, Engyodontium, Isaria, Lecanicillium, mariannaea-like, Microhilum, Simplicillium.
CORDYCEPS Fr., Observ. Mycol. 2 (revis.): 316. 1818 emend. G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
= Phytocordyceps C.H. Su & H.-H. Wang, Mycotaxon 2: 338. 1986.
Stromata or subiculum pallid or brightly pigmented, fleshy. Perithecia superficial to completely immersed, ordinal in arrangement. Asci hyaline, cylindrical with thickened ascus apex. Ascospores hyaline, cylindrical, multiseptate, disarticulating into part-spores or nondisarticulating, rarely possessing a thread-like structure connecting the fusiform ends.
Type: Cordyceps militaris (L.: Fr.) Fr., Observ. Mycol. 2(revis.): 317. 1818.
Anamorphic genera: Beauveria, Isaria, Lecanicillium, mariannaea-like, Microhilum, Simplicillium.
Commentary: Species of Cordyceps s. s. are characterized by possessing fleshy stromata that are pallid or brightly coloured. Because species of Torrubiella are interspersed among Cordyceps species in the basal part of the Cordycipitaceae, its ultimate application to a monophyletic taxon within the Cordycipitaceae is not clear, however (Fig. 10). The genus Torrubiella was erected in 1885 by Boudier with the type species T. aranicida Boud. (Kobayasi & Shimizu 1982). Our sampling included several species of Torrubiella that were interspersed amongst species of Cordycipitaceae, but we could not get hold of T. aranicida. Thus, Cordyceps s. s. is narrowly applied to the strongly supported clade (MP-BP = 98 %, ML-BP = 98 %, PP = 1.00 in Figs 1, 2, 10) that includes Cordyceps species closely related to C. militaris. Cordyceps species that are placed outside of the Cordyceps s. s. node, but within the Cordycipitaceae, are provisionally retained within Cordyceps s. l. Torrubiella species that are part of the Cordyceps s. s. are transferred accordingly. The full extent to which the names Cordyceps and Torrubiella will ultimately be applied awaits additional sampling of Torrubiella, especially that of T. aranicida with the possibility that Torrubiella will need to be synonymized with Cordyceps. Although Phytocordyceps is characterized by its possession of bola-ascospores, it is also synonymized with Cordyceps because of its phylogenetic placement (Figs 8, 10).
Accepted names and new combinations for Cordyceps s. s.
The following taxa are accepted species of Cordyceps s. s. based
on their inclusion in molecular phylogenies presented herein1 (see
Table 1) or morphological
descriptions matching the characters described above2. Where known
we provide the anamorph connection for the species of Cordyceps s.
s.
Torrubiella confragosa Mains, Mycologia 41: 305. 1949.
Clavaria militaris L., Sp. Plantarum, p. 1182. 1753.
Hypoxylon militare (L.) Mérat, Nouv. Fl. Envir.
Paris, p. 137. 1821.
Xylaria militaris (L.) Gray, Nat. Arr. Brit. Pl. (London),
p. 510. 1821.
Sphaeria militaris (L.: Fr.) Fr., Syst. Mycol. 2: 325.
1823.
Torrubia militaris (L.: Fr.) Tul. & C. Tul., Sel.
Fung. Carpol. 3: 6. 1865.
Phytocordyceps ninchukispora C.H. Su & H.-H. Wang,
Mycotaxon 26: 338. 1986.
Acrophyton tuberculatum Lebert, in Sieb & Köll.,
Z. Wiss. Zool. 9: 448. 1858.
Cordyceps sphingum (Tul. & C. Tul.) Berk. & M.A.
Curtis, in Berkeley, J. Linn. Soc. 10: 375. 1868.
Cordyceps moelleri Henn., Hedwigia 3: 221. 1897.
Cordyceps crista A. Möller, Phycomyceten u.
Ascomyceten, p. 212. 1901.
Ophionectria cockerellii Ellis & Everh., in Cockerell,
J. Inst. Jamaica 1: 141. 1892.
Cordyceps cockerellii (Ellis & Everh.) Ellis, in
Seaver, North Am. Flora 3: 52. 1910.
Clavicipitaceae incertae sedis
The following teleomorph genera could not be confidently assigned in the
new classification because they were either not sampled as part of this study,
were not sampled as part of other molecular phylogenetic studies, or the
assessment of their morphology and ecology was inconclusive:
Berkelella (Sacc.) Sacc., Cavimalum Yoshim. Doi, Dargan
& K.S. Thind, Dussiella Pat., Epicrea Petr.,
Helminthascus Tranzschel, Konradia Racib.,
Moelleriella Bres., Mycomalus A. Möller,
Neobarya Lowen, Neocordyceps Kobayasi, Podocrella
Seaver, Romanoa Thirum., Sphaerocordyceps Kobayasi, and
Stereocrea Syd. & P. Syd.
Residual species of Cordyceps
The following species of Cordyceps s. l. could not be confidently
assigned in the new classification because they were either not assigned in
any of the proposed genera in this study, were not sampled as part of this or
other molecular phylogenetic studies, or the assessment of their morphology
and ecology was inconclusive. These species are provisionally retained within
Cordyceps s. l. until further phylogenetic analyses are conducted to
classify them in a phylogenetic system. Where known we provide the anamorph
connection for the species of Cordyceps s. l.
Torrubia adpropinquans Ces., Atti Accad. Sci. Fis. Mat.,
Napoli 8: 14. 1879.
azy & Bujak., Mycotaxon 25: 11.
1986.
Racemella memorabilis Ces., Comment. Soc. Crittog. Ital.
1: 65. 1861. | KEY TO THE GENERA OF FUNGI FORMERLY CLASSIFIED IN CORDYCEPS |
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To assist the user we briefly define some characters of stromatal texture and morphology that may not be intuitive:
|
Cordyceps s. s. consists almost entirely of pallid to brightly coloured species that produce soft fleshy stromata (e.g., C. militaris). The majority of species attack larvae and pupae of Lepidoptera and Coleoptera in leaf litter, moss or upper soil layers. Numerous species that produce highly reduced stromata, loosely organized hyphae, or a subiculum on the host also occur in this genus (e.g. C. tuberculata), some of which were previously classified in Torrubiella (e.g., T. confragosa).
Elaphocordyceps includes all species that parasitize Elaphomyces and closely related species that attack nymphs of cicadas. The morphology of the Elaphomyces parasites and the cicada pathogens are remarkably similar and attest to the recent history of inter-kingdom host-jumps in a common subterranean environment (Nikoh & Fukatsu 2000). The exception to this genus is E. subsessilis, which macroscopically and ecologically is distinct from the rest of the species, but is well supported as being a member of the genus based on molecular data and micromorphology.
Metacordyceps includes only a limited number of described species, of which all but one are only known from East Asia. The stromatal colour of fresh specimens ranges from white to lilac, purple or green, and the darker pigments are almost black in dried specimens. The texture of the stromata is fibrous and not fleshy like Cordyceps s. s., and the hosts are almost always buried in soil.
Ophiocordyceps is the largest genus of arthropod-pathogenic fungi. Many species are darkly pigmented and occur on immature stages of hosts buried in soil or in decaying wood. Notable exceptions exist for both of these traits among species that attack adult stages of hosts, however. For example, O. unilateralis is common on adult ants and occurs on the under sides of leaves, and O. sphecocephala is common on adult wasps and is found in leaf litter. Stromatal morphology is diverse, ranging from filiform and wiry to clavate and fibrous, according to species, and many species produce their perithecia in nonterminal regions of the stroma, either distinctly superficial, or in broad irregular patches, or in lateral pads.
| Acknowledgments |
|---|
| References |
|---|
|
|
|---|
Artjariyasripong S, Mitchell JL, Hywel-Jones NL, Jones EBG (2001). Relationships of the genus Cordyceps and related genera, based on parsimony and spectral analysis of partial 18S and 28S ribosomal gene sequences. Mycoscience 42:503 –517.[CrossRef]
Barron GL (1980). Fungal parasites of rotifers: a new Tolypocladium with underwater conidiation. Canadian Journal of Botany 58:439 –442.
Barron GL, Onions AHS (1966). Verticillium chlamydosporium and its relationships to Diheterospora, Stemphyliopsis, and Paecilomyces. Canadian Journal of Botany 44:861 –869.
Bischoff JF, Chaverri P, White JF Jr. (2005).
Clarification of the host substrate of Ascopolyporus and description
of Ascopolyporus philodendrus sp. nov.
Mycologia 97:710
–717.
Bissett J (1983). Notes on Tolypocladium and related genera. Canadian Journal of Botany 61:1311 –1329.
Blackwell M, Gilbertson RL (1984). New information on Cordycepioideus bisporus and Cordycepioideus octosporus.Mycologia 76:763 –765.[CrossRef]
Chaverri P, Bischoff JF, Evans HC, Hodge KT (2006). Regiocrella, a new entomopathogenic genus with a pycnidial anamorph and its phylogenetic placement in the Clavicipitaceae.Mycologia 97(2005):122 –1237.
Coyle FA, Goloboff PA, Samson RA (1990). Actinopus trapdoor spiders (Araneae, Actinopodidae) killed by the fungus, Nomuraea atypicola (Deuteromycotina). Acta Zoologica Fennica 190:89 –93.
Diehl WW (1950). Balansia and the Balansiae in America. Agric. Monogr. No. 4. USDA, Washington.
Doaudy CJ, Delsuc F, Boucher Y, Doolittle WF, Douzery EJP
(2003). Comparison of the Bayesian and maximum likelihood
bootstrap measures of phylogenetic reliability. Molecular Biology
and Evolution 20:248
–254.
Driver F, Milner RJ, Trueman JWH (2000). A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycological Research 104:134 –150.[CrossRef]
Earle FS (1901). Collections of Alabama fungi. In: Plant life of Alabama (Mohr C, ed). Contr. U. S. Natl. Herb.: 150–263.
Eriksson OE (1982). Cordyceps bifusispora spec. nov. Mycotaxon 15:185 –188.
Eriksson OE (1986). Notes on ascomycete systematics. Systema Ascomycetum 5:113 –174.
Eriksson OE, Hawksworth DL (1985). Outline of the Ascomycetes–1985. Systema Ascomycetum 4:1 –79.
Evans HC (2003). Use of clavicipitalean fungi for the biological control of arthropod pests. In: Clavicipitalean fungi: Evolutionary biology, Chemistry, Biocontrol and Cultural impacts (White, JF Jr., Bacon CW, Hywel-Jones NL, Spatafora JW, eds.). Marcel Dekker Inc., New York: 517–548.
Evans HC, Samson RA (1982). Entomogenous fungi from the Galapagos islands. Canadian Journal of Botany 60:2325 –2333.
Evans HC. Samson RA (1987). Fungal pathogens of spiders. Mycologist 1:152 -159.
Felsenstein J (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783 –791.[CrossRef][Web of Science]
Gams W (1971). Cephalosporium-artige Schimmelpilze (Hyphomycetes). G. Fischer, Stuttgart.
Gams W, Hodge KT, Samson RA, Korf RP, Seifert KA (2005). Proposal to conserve the name Isaria (anamorphic fungi) with a conserved type. Taxon 54: 537.
Gams W, Zare R (2001). A revision of Verticillium sect. Prostrata. III. Generic classification. Nova Hedwigia 72:329 –337.
Gams W, Zare R (2003). A taxonomic review of the clavicipitaceous anamorphs parasitizing nematodes and other microinvertebrates. In: Clavicipitalean fungi: Evolutionary biology, Chemistry, Biocontrol and Cultural Impacts (White, JF Jr., Bacon CW, Hywel-Jones NL, Spatafora JW, eds.). Marcel Dekker Inc., New York: 17–73.
Hawksworth DL, Rossman AY (1997). Where are all the undescribed fungi? Phytopathology 87:888 –891.[CrossRef][Medline]
Hodge KT (1998). Revisionary studies in Hirsutella (Anamorphic Hypocreales: Clavicipitaceae). PhD Thesis, Cornell University, Ithaca, New York.
Hodge KT (2003). Clavicipitaceous anamorphs. In: Clavicipitalean fungi: Evolutionary biology, Chemistry, Biocontrol and Cultural Impacts (White, JF Jr., Bacon CW, Hywel-Jones NL, Spatafora JW, eds.). Marcel Dekker Inc., New York:75 –123.
Hodge KT, Krasnoff SB, Humber RA (1996). Tolypocladium inflatum is the anamorph of Cordyceps subsessilis.Mycologia 88:715 –719.[CrossRef]
Hoog GS de (1972). The genera Beauveria, Isaria, Tritirachium and Acrodontium gen. nov. Studies in Mycology 1:1 –44.
Huang B, Li C, Humber RA, Hodge KT, Fan M, Li Z (2005). Molecular evidence for the taxonomic status of Metarhizium taii and its teleomorph, Cordyceps taii (Hypocreales, Clavicipitaceae). Mycotaxon 94:137 –147.
Huelsenbeck JP, Ronquist F (2001). MrBAYES: Bayesian
inference of phylogenetic trees. Bioinformatics
17:754
–755.
Humber RA, Rombach MC (1987). Torrubiella ratticaudata sp. nov. (Pyrenomycetes: Clavicipitales) and other fungi from spiders on the Solomon Islands. Mycologia 79:375 –382.[CrossRef]
Hywel-Jones NL (1993). Torrubiella luteorostrata: a pathogen of scale insects and its association with Paecilomyces cinnamomeus, with a note on Torrubiella tenuis.Mycological Research 97:1126 –1130.
Hywel-Jones NL (1994). Cordyceps khaoyaiensis and C. pseudomilitaris, two new pathogens of lepidopteran larvae from Thailand. Mycological Research 98:939 –942.
Hywel-Jones NL (1995). Hymenostilbe ventricosa sp. nov., a pathogen of cockroaches in Thailand. Mycological Research 99:1201 –1204.
Hywel-Jones NL (1996). Cordyceps myrmecophila-like fungi infecting ants in the leaf litter of tropical forest in Thailand. Mycological Research 100:613 –619.
Hywel-Jones NL (2002). Multiples of eight in Cordyceps ascospores. Mycological Research 106:2 –3.[CrossRef]
Hywel-Jones NL, Evans HC (1993). Taxonomy and ecology of Hypocrella discoidea and its anamorph, Aschersonia samoënsis. Mycological Research 97:871 –876.
Hywel-Jones NL, Samuels GJ (1998). Three species of Hypocrella with large stromata pathogenic on scale insects. Mycologia 90:36 –46.[CrossRef]
Hywel–Jones NL, Sivichai S (1995). Cordyceps cylindrica and its association with Nomuraea atypicola in Thailand. Mycological Research 99:809 –812.
Kobayasi Y (1939). On the genus Cordyceps and its allies on cicadae from Japan. Bulletin of the Biogeographical Society of Japan 9:145 –176.
Kobayasi Y (1941). The genus Cordyceps and its allies. Science Reports of the Tokyo Bunrika Daigaku, (Section B, no. 84) 5:53 –260.
Kobayasi Y (1982). Keys to the taxa of the genera Cordyceps and Torrubiella. Transactions of the Mycological Society of Japan 23:329 –364.
Kobayasi Y, Shimizu D (1960). Monographic studies of Cordyceps 1. Group parasitic on Elaphomyces. Bulletin of the National Science Museum Tokyo 5:69 –85.
Kobayasi Y, Shimizu D (1963). Monographic studies of Cordyceps 2. Group parasitic on Cicadae. Bulletin of the National Science Museum Tokyo 6:286 –314.
Kobayasi Y, Shimizu D (1976). The genus Cordyceps and its allies from New Guinea. Bulletin of the National Science Museum, Tokyo, Ser. B. 2:133 –151.
Kobayasi Y, Shimizu D (1978). Cordyceps species from Japan. Bulletin of the National Science Museum, Tokyo, Ser. B. 4:44 –62.
Kobayasi Y, Shimizu D (1982). Monograph of the genus Torrubiella. Bulletin of the National Science Museum, Tokyo, Ser. B. 8:43 –78.
Li Z-Z, Li C-R, Huang B, Fan M-Z (2001). Discovery and demonstration of the teleomorph of Beauveria bassiana (Bals.) Vuill., an important entomopathogenic fungus. Chinese Science Bulletin 9:751 –753.
Liang Z-Q (1991). Determination and identification of anamorph of Cordyceps pruinosa. Acta Mycologica Sinica 10:72 –80.
Liang Z-Q, Liu A-Y, Liu J-L (1991). A new species of the genus Cordyceps and its Metarhizium anamorph. Acta Mycologica Sinica 10:257 –262.
Liu Z-Y, Liang Z-Q, Whalley AJS, Yao Y-J, Liu A-Y (2001). Cordyceps brittlebankisoides, a new pathogen of grubs and its anamorph, Metarhizium anisopliae var. majus.Journal of Invertebrate Pathology 78:178 –182.[CrossRef][Medline]
Luangsa-ard JJ, Hywel-Jones NL, Manoch L, Samson RA (2005). On the relationships of Paecilomyces sect. Isarioidea species. Mycological Research 109:581 –589.[CrossRef][Medline]
Luangsa-ard JJ, Hywel-Jones NL, Samson RA (2004). The
polyphyletic nature of Paecilomyces sensu lato based on 18S-generated
rDNA phylogeny. Mycologia
96:773
–780.
Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B,
Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V,
Schoch C, Arnold AE, Miadlikowska J, Spatafora JW, Johnson D, Hambleton S,
Crockett M, Shoemaker R, Sung G-H, Lucking R, Lumbsch T, O'Donnell K, Binder
M, Diederich P, Ertz D, Gueidan C, Hansen K, Harris RC, Hosaka K, Lim Y-W,
Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H,
Stone J, Sugiyama J, Yahr R, Vilgalys R (2004). Assembling the
fungal tree of life: progress, classification, and evolution of subcellular
traits. American Journal of Botany
91:1446
–1480.
MacLeod DM (1954). Investigations on the genera Beauveria Vuill. and Tritirachium Limber. Canadian Journal of Botany 32:818 –890.
McNeill JF, Barrie F, Burdet HM, Demoulin V, Hawksworth DL, Marhold K, Nicolson DH, Prado J, Silva PC, Skog JE, Wiersema J, Turland NJ, eds (2006). International Code of Botanical Nomenclature (Vienna Code). Regnum Vegetabile 146. Koeltz Scientific Books, Königstein.
Maddison DR, Maddison WP (2000). MacClade 4: Analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, Massachusetts.
Mains EB (1950). Entomogenous species of Akanthomyces, Hymenostilbe and Insecticola in North America. Mycologia 42:566 –589.[CrossRef]
Mains EB (1957). Species of Cordyceps parasitic on Elaphomyces. Bulletin of the Torrey Botanical Club 84:243 –251.[CrossRef]
Mains EB (1958). North American entomogenous species of Cordyceps. Mycologia 50:169 –222.[CrossRef]
Mains EB (1959). North American species of Aschersonia parasitic on Aleyrodidae. Journal of Insect Pathology 1:43 –47.
Mason-Gamer RJ, Kellogg EA (1996). Testing for
phylogenetic conflict among molecular data sets in the tribe Triticeae
(Gramineae). Systematic Biology
45:524
–545.
Massee G (1895). A revision of the genus Cordyceps. Annals of Botany 9:1 –44.
Mugnai L, Bridge PD, Evans HC (1989). A chemotaxonomic evaluation of the genus Beauveria. Mycological Research 92:199 –209.[CrossRef]
Nannfeldt JA (1932). Studien über die Morphologie und Systematik der nicht-lichenisierten, inoperculaten Discomyceten. Nova Acta R. Societatis Scientiarum Upsaliensis, Ser. 6, 8:1 –368.
Nikoh N, Fukatsu T (2000). Interkingdom host jumping
underground: Phylogenetic analysis of entomopathogenic fungi of the genus
Cordyceps. Molecular Biology and Evolution
17:629
–638.
Oborník M, Jirku M, Dolezel D (2001). Phylogeny of mitosporic entomopathogenic fungi: Is the genus Paecilomyces polyphyletic? Canadian Journal of Microbiology 47:813 –819.[CrossRef][Medline]
Ochiel GS, Evans HC, Eilenberg J (1997). Cordycepioideus, a pathogen of termites in Kenya. Mycologist 11:7 –9
Pacioni G, Frizzi G (1978). Paecilomyces farinosus, the conidial state of Cordyceps memorabilis.Canadian Journal of Botany 56:391 –394.
Penzig O, Saccardo PA (1904). Icones fungorum Javanicorum. Buchhandlung and Druckerei E.J. Brill, Leiden.
Petch T (1921). Studies in entomogenous fungi. II. The genera of Hypocrella and Aschersonia. Annals of the Royal Botanic Garden Peradeniya 7:167 –278.
Petch T (1924). Studies in entomogenous fungus. IV. Some Ceylon Cordyceps. Transactions of the British Mycological Soceity 10:28 –45.
Petch T (1931). Notes on entomogenous fungi. Transactions of the British Mycological Society 16:55 –75.
Petch T (1932). Notes on entomogenous fungi. Transactions of the British Mycological Society 16:209 –245.
Petch T (1933). Notes on entomogenous fungi. Transactions of the British Mycological Society 18:48 –75.
Petch T (1936). Cordyceps militaris and Isaria farinosa. Transactions of the British Mycological Society 20:216 –224.
Petch T (1937). Notes on entomogenous fungi. Transactions of the British Mycological Society 21:34 –67.
Philippe H, Snell EA, Bapteste E, Lopez P, Holland PWH, Casane D
(2004). Phylogenomics of eukaryotes: impact of missing data on
large alignments. Molecular Biology and Evolution
21:1740
–1752.
Reeb V, Lutzoni F, Roux C (2004). Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycota, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Molecular Phylogenetics and Evolution 32:1036 –1060.[CrossRef][Web of Science][Medline]
Rehner SA, Buckley E (2005). A Beauveria
phylogeny inferred from nuclear ITS and EF1-
sequences:
evidence for cryptic diversification and links to Cordyceps
teleomorphs. Mycologia
97:84
–98.
Reynolds DR, Taylor JW (eds) (1993). The fungal holomorph: Mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford UK.
Rogerson CT (1970). The hypocrealean fungi (Ascomycetes, Hypocreales). Mycologia 62:865 –910.[Web of Science][Medline]
Rombach MC, Humber RA, Roberts DW (1986). Metarhizium flavoviride var. minus, var. nov., a pathogen of plant- and leafhoppers on rice in the Philippines and Solomon Islands. Mycotaxon 27:87 –92.
Rossman AY, Samuels GJ, Rogers JS, Lowen R (1999). Genera of Bionectriaceae, Nectriaceae and Hypocreaceae (Hypocreales, Ascomycetes). Studies in Mycology 42:1 –248.
Samson RA (1974). Paecilomyces and some allied hyphomycetes. Studies in Mycology 6:1 –119.
Samson RA, Evans HC (1975). Notes on entomogenous fungi from Ghana III. The genus Hymenostilbe. Proceedings, Koninklijke Nederlandse Akademie van Wetenschappen C 78:73 –79.
Samson RA, Evans HC, Latgé J-P (1988). Atlas of entomopathogenic fungi. Springer-Verlag, Berlin, Heidelberg, New York.
Samson RA, van Reenen-Hoekstra ES, Evans HC (1989). New species of Torrubiella (Ascomycotina: Clavicipitales) on insects from Ghana. Studies in Mycology 31:123 –132.
Shimazu M, Mitsuhashi W, Hashimoto H (1988). Cordyceps brongniartii sp. nov., the teleomorph of Beauveria brongniartii. Transactions of the Mycological Society of Japan 29:323 –330.
Spatafora JW, Sung G-H, Sung J-M, Hywel-Jones NL, White JF Jr. (2007). Phylogenetic evidence for an animal pathogen origin for ergot and the grass endophytes. Molecular Ecology 16:1701 –1711.[CrossRef][Medline]
Stamatakis A, Ludwig T, Meier H (2005). RAxML-III: a
fast program for maximum likelihood-based inference of large phylogenetic
trees. Bioinformatics
21:456
–463.
Stensrud Ø, Hywel-Jones NL, Schumacher T (2005). Towards a phylogenetic classification of Cordyceps: ITS nrDNA sequence data confirm divergent lineages and paraphyly. Mycological Research 109:41 –56.[CrossRef][Medline]
Su C-H, Wang H-H (1986). Phytocordyceps, a new genus of the Clavicipitaceae. Mycotaxon 26:337 –344.
Suh S-O, Spatafora JW, Ochiel GRS, Evans HC, Blackwell M (1998). Molecular phylogenetic study of a termite pathogen Cordycepioideus bisporus. Mycologia 90:611 –617.[CrossRef]
Sullivan RF, Bergen MS, Patel R, Bills GF, Alderman SC, Spatafora JW, White JF Jr. (2001). Neoclaviceps monostipa: features of an enigmatic clavicipitalean fungus and the phyletic status of the anamorphic genus Ephelis. Mycologia 93:90 –99.[CrossRef]
Sullivan RF, Bills GF, Hywel-Jones NL, White JF Jr. (2000). Hyperdermium: a new clavicipitalean genus for some tropical epibionts of dicotyledonous plants. Mycologia 92:908 –918.[CrossRef]
Sung G-H, Spatafora JW (2004). Cordyceps
cardinalis sp. nov., a new species of Cordyceps with an east
Asian-eastern North American distribution. Mycologia
96:658
–666.
Sung G-H, Spatafora JW, Zare R, Hodge KT, Gams W (2001). A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae.Nova Hedwigia 72:311 –328.
Sung G-H, Sung J-M, Hywel-Jones NL, Spatafora JW (2007). A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Molecular Phylogenetics and Evolution, in press.
Sung J-M (1996). The insects-born fungus of Korea in color. Kyohak Publ. Co., Seoul.
Swofford DL (2002). PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, Massachusetts.
Tanaka E, Tanaka C, Gafur A, Tsuda M (2002). Heteroepichloë, gen. nov. (Clavicipitaceae; Ascomycotina) on bamboo plants in East Asia. Mycoscience 43:87 –93.[CrossRef]
Thompson JD, Higgins DG, Gibson TJ (1994). CLUSTAL W:
Improving the sensitivity of progressive multiple sequence alignment through
sequence weighting, positions-specific gap penalties and weight matrix choice.
Nucleic Acids Research
22:4673
–4680.
White JF Jr., Reddy PV (1998). Examination of structure and molecular phylogenetic relationships of some graminicolous symbionts in genera Epichloë and Parepichloë.Mycologia 90:226 –234.[CrossRef]
Wiens JJ (1998). Combining data sets with different phylogenetic histories. Systematic Biology 47:568 –581.[CrossRef][Web of Science][Medline]
Wiens JJ (2003). Missing data, incomplete taxa, and
phylogenetic accuracy. Systematic Biology
52:528
–538.
Zang M, Daoqing L, Ruoying H (1982). Notes concerning the subdivisions of Cordyceps and a new species from China. Acta Botanica Yunnanica 4:173 –176.
Zang M, Kinjo N (1998). Notes on the alpine Cordyceps of China and nearby nations. Mycotaxon 66:215 –229.
Zare R, Gams W (2001a). A revision of Verticillium sect. Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia 73:1 –50.
Zare R, Gams W (2001b). A revision of Verticillium sect. Prostrata. VI. The genus Haptocillium. Nova Hedwigia 73:271 –292.
Zare R, Gams W, Evans HC (2001). A revision of Verticillium sect. Prostrata. V. The genus Pochonia, with notes on Rotiferophthora. Nova Hedwigia 73:51 –86.
Zare R, Gams W, Starink-Willemse M, Summerbell RC (2007) Gibellulopsis, a suitable genus for Verticillium nigrescens, and Musicillium, a new genus for V. theobromae. Nova Hedwigia, in press.
Zhang WM, Li TH, Chen YQ, Qu LH (2004). Cordyceps
campsosterna, a new pathogen of Campsosternus auratus. Fungal
Diversity 17:239
–242.
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