Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium.

Ophiocordycipitaceae is a diverse family comprising ecologically, economically, medicinally, and culturally important fungi. The family was recognized due to the polyphyly of the genus Cordyceps and the broad diversity of the mostly arthropod-pathogenic lineages of Hypocreales. The other two cordyceps-like families, Cordycipitaceae and Clavicipitaceae, will be revised taxonomically elsewhere. Historically, many species were placed in Cordyceps, but other genera have been described in this family as well, including several based on anamorphic features. Currently there are 24 generic names in use across both asexual and sexual life stages for species of Ophiocordycipitaceae. To reflect changes in Art. 59 in the International Code of Nomenclature for algae, fungi, and plants (ICN), we propose to protect and to suppress names within Ophiocordycipitaceae, and to present taxonomic revisions in the genus Tolypocladium, based on rigorous and extensively sampled molecular phylogenetic analyses. When approaching this task, we considered the principles of priority, monophyly, minimizing taxonomic revisions, and the practical utility of these fungi within the wider biological research community.

BACKGROUND

The revision of Art. 59 in the International Code of Nomenclature for algae, fungi, and plants (ICN; McNeill ) has created a major task for mycologists, who must now reconcile under one name various possible names existing for different morphs of the same species of fungus (Hibbett & Taylor 2013). Groups have already begun to propose names which should be protected or suppressed within Hypocreales in accordance with the ‘one fungus one name’ policy (Geiser , Rossman , Leuchtmann , Johnston et al. 2014, Kepler ) and others are in progress. Here, we seek to retain names in Ophiocordycipitaceae with the goal of harmonizing priority, monophyly, simplicity of taxonomic revisions, and minimization of disruption to the research community.

The family Ophiocordycipitaceae was described by Sung to accommodate species that were determined to be phylogenetically distinct from Cordycipitaceae and Clavicipitaceae s.str. Asexual morphologies in Ophiocordycipitaceae show a tremendous range of variation, some of which are restricted in their phylogenetic distribution while others are often found in disparate lineages. For example, Verticillium is a common asexual morph of many species in several hypocrealean families, including Ophiocordycipitaceae, Cordycipitaceae and Clavicipitaceae (see Zare , Sung , 2007, and Gams & Zare 2001).

Ophiocordyceps is the most speciose genus of the family, and was described originally by Petch (1931a) for species of Cordyceps that have septate ascospores that do not disarticulate into part-spores at maturity and asci with inconspicuous apical caps (Petch 1931a, 1933). Kobayasi (1941) later used Ophiocordyceps as a subgeneric classification of the genus Cordyceps, but Sung restored Ophiocordyceps to the rank of genus to include those Cordyceps species within Ophiocordycipitaceae forming a sister clade with the genus Elaphocordyceps (see below). The type of the genus is O. blattae, a rarely collected cockroach pathogen for which no culture or molecular data are available.

Asexual generic names associated with Ophiocordyceps include Sorosporella, the oldest name still in use for species in the clade, Hirsutella, Hymenostilbe, Stilbella, Syngliocladium, and Paraisaria. Hirsutella species typically produce one to several conidia in a limited mucus droplet borne on basally subulate phialides that taper into slender necks (Gams & Zare 2003). Hymenostilbe was proposed by Petch (1931b), and there is some evidence to support restricting its use within the genus Ophiocordyceps to the ‘O. sphecocephala clade’, most species of which sporulate from adult insects (Sung , Luangsa-ard ). These taxa produce conidia singly from multiple denticles on conidiogenous cells forming a palisade-like layer along the entire outer surface of synnemata (Mains 1950). The Stilbella morphology has been applied broadly among species associated with Ophiocordyceps, as well as to fungi later reclassified in other genera (Seifert 1985, Gräfenhan ). Stilbella species often produce aggregate synnemata with a fertile, terminal head of conidia. Syngliocladium spp. often have laterally arising conidiophores similar in morphology to the hypocreaceous asexual morph Gliocladium, and they may be either synnematous or mononematous on their arthropod hosts (Petch 1932, Hodge ). Sorosporella, a chlamydospore producing spore state, has been linked as a synasexual morph of Syngliocladium (Speare 1917, 1920), but the two morphologies are not always produced by all species (Hodge et al.1998, Evans & Shah 2002). Species of Paraisaria possess feathery synnemata which fruit from arthropod hosts, and several species have been linked via cultural and molecular data to the O. gracilis clade (Samson & Brady 1983, Sung , Evans ). Names of genera associated with Ophiocordyceps whose types are located outside of Hypocreales include Tilachlidiopsis and Podonectria, members of the Agaricomycetes and Dothideomycetes, respectively (Rossman 1978, Stalpers et al.1991, Hughes , Boonmee ). Despite the large number of taxa associated with Ophiocordyceps, a lack of support for internal nodes resulting in equivocal topologies has limited inferences about relationships within the genus in previous studies (Sung ).

The most notable species in the Ophiocordyceps clade is O. sinensis, which is nearly double the price of gold by weight (Stone 2008, Shrestha & Bawa 2013) and the subject of intense research, especially in China (Shrestha , Hu , Ren & Yao 2013, Bushley , etc.). Almost exclusively found parasitizing the larvae of ghost moths (Hepialidae: Thitarodes) in the alpine and sub-alpine pastures of the Tibetan plateau and the Himalayas, this species is undergoing heavy, possibly unsustainable, and destructive harvesting (Cannon , Shrestha & Bawa 2013).

The recently described genus Elaphocordyceps is typified by E. ophioglossoides, one of the first Cordyceps species to be described. Species in Elaphocordyceps are mostly parasites of the ectomycorrhizal truffle genus Elaphomyces (Ascomycota, Eurotiales). The majority of Elaphocordyceps species have no known asexual morph, but where known they produce ones which are verticillium-like or Tolypocladium (Sung ). There are a few Elaphocordyceps species known to be entomopathogens, including three cicada pathogens (E. inegoensis, E. paradoxa, and E. toriharamontana), and one beetle pathogen, E. subsessilis (syn.Tolypocladium inflatum) (Hodge , Sung ). Tolypocladium inflatum (a name conserved by the rejection of Pachybasium niveum; Dreyfuss & Gams 1994), is a medicinally important fungus and the subject of much research due to its production of the immunosuppressant drug, cyclosporin A (Survase , Bushley ). The other species of Tolypocladium have no known sexual morphs and have mainly been isolated from soil (Gams 1971, Bissett 1983) or observed parasitizing rotifers or insects (Barron 1980, 1981, 1983, Samson & Soares 1984, Weiser ). The asexually typified genus Chaunopycnis is also related to this clade (Bills ) and has been isolated mainly from soil samples (Gams 1980, Bills ), although one species was isolated from epilithic Antarctic lichens (Möller & Gams 1993). The similarity of conidiogenesis between Chaunopycnis and Tolypocladium was noted in the original description of Chaunopycnis (Gams 1980), and its phialides often taper in a manner similar to those of Tolypocladium. Interestingly, these two genera have also been linked by their shared production of cyclosporin A (Traber & Dreyfuss 1996). Two of the described Chaunopycnis species produce loosely enclosed conidiomata, a morphology not seen in other members of the clade or within Ophiocordycipitaceae as a whole.

The relationships among the species of the Purpureocillium clade were recently reviewed by Luangsa-ard . The genus was proposed to encompass taxa closely related to Purpureocillium lilacinum (syn. Paecilomyces lilacinus) and consists of species with purple-hued conidia, including Nomuraea atypicola and Isaria takamizusanensis. The type of Nomuraea is N. rileyi (syn. N. prasina), which has recently been synonymized with Metarhizium (Kepler ). The type of Isaria is a member of Cordycipitaceae (Gams , Hodge , Luangsa-ard ). While N. atypicola and I. takamizusanensis have not been addressed taxonomically, other studies found close relationships between these taxa and Purpureocillium (Sung , Perdomo ). Nomuraea atypicola is the asexual morph of C. cylindrica (Hywel-Jones & Sivichai 1995), the only sexual morph described for this clade and one of the “residual” Cordyceps s. lat. left without reassignment to any phylogenetically redefined genus by Sung .

Nematode pathogens have been described in many genera throughout Hypocreales. The largest and oldest of these is the asexually typified genus Harposporium. Most Harposporium species produce crescent-shaped or helicoid conidia that are ingested by their hosts and become lodged in the upper portions of the digestive tract (Barron 1977). Conidia are produced on spherical conidiogenous cells, and several species are known to produce hirsutella-like synasexual morphs (Hodge , Chaverri , Li ). While the majority of Harposporium species are known from nematodes, these fungi are common in the soil and several studies have reported an entomopathogenic ecology as well (e.g., Shimazu & Glockling 1997, Evans & Whitehead 2005). In 2005, Chaverri et al. reported the asexual-sexual morph connection between Harposporium and Podocrella, an arthropod-pathogenic genus. Several researchers initially described nematophagous taxa in the originally plant-pathogenic genus Meria (Vuillemin 1896, Drechsler 1941), but this genus was found to be polyphyletic (Gams & Jansson 1985), and for this reason Drechmeria was erected for the nematophagous meria-like taxa in Hypocreales. The type of Drechmeria, D. coniospora, has cone-shaped conidia whose conidiogenous cells are not basally swollen as in Harposporium. One protozoan-infecting species of Drechmeria, D. harposporioides, produces crescent-shaped conidia similar to those of Harposporium (Barron & Szijarto 1982). Haptocillium was erected for asexual nematode pathogens bearing verticillate phialides and whose conidia are not ingested but adhere to the surface of their hosts (Zare & Gams 2001).

Polycephalomyces represents a diverse clade that is currently incertae sedis within Hypocreales, as its placement has lacked support in previous molecular studies (Kepler ). Of particular uncertainty was whether Polycephalomyces and its closest related taxon, C. pleuricapitata, formed a sister clade to Ophiocordycipitaceae, or if it was more closely related to Clavicipitaceae. Many morphological characters are shared between Ophiocordycipitaceae and Polycephalomyces. For example, numerous species in both clades produce hirsutella-like anamorphs with conidia often borne in a slimy mass (Seifert 1985). In addition, sexual sporing structures of Polycephalomyces often possess a wiry, tough, carbonaceous stipe which is a common morphology of Ophiocordyceps (Kepler ). Many species within this genus are known mycoparasites of other hypocrealean entomopathogens and myxomycetes, but there are also several species of entomopathogens. Cordyceps pleuricapitata was deemed a residual species of Cordyceps of uncertain placement by Kepler , due to a lack of statistical support joining that species and Polycephalomyces.

In this paper we expand the taxon sampling presented in Sung by 222 hypocrealean isolates. This includes sexual and asexual states which provide the framework for addressing the nomenclatural issues demanded by changes to the most recent ICN.

MATERIALS AND METHODS

Sequences from five nuclear loci, including the small and large subunits of the rDNA (SSU and LSU), the transcription elongation factor-1α (TEF), and the first and second largest subunits of RNA polymerase II (RPB1 and RPB2) were used for phylogenetic analyses. DNA extraction and PCR amplification were carried out as previously described (Kepler ). Sequencing reactions were performed at the University of Washington High-Throughput Genomics Center (Seattle, WA) with the primers used for the initial amplifications. All other sequences were collected from GenBank. Efforts were made for all specimens to have data for at least three of the five genes to be considered in our analyses. However, certain taxa for which only one or two genes were available were included due to the importance in addressing the taxonomic issues at hand (Table 1).

Table 1.

Specimen information and GenBank accession numbers for sequences used in this study.

Species	Voucher Information	SSU	LSU	TEF	RPB1	RPB2
Chaunopycnis alba	MRL GB5502		AF245297
	MRL MF6799		AF373284
Chaunopycnis pustulata	MRL GB6597		AF389190
	MRL MF5368LR		AF373282
Cordyceps cylindrica	CEM 1185	KJ878907	KJ878872	KJ878955
Cordyceps formosana	TNM F13893	KJ878908		KJ878956	KJ878988	KJ878943
Cordyceps gunnii	OSC 76404	AF339572	AF339522	AY489616	AY489650	DQ522426
Cordyceps irangiensis	OSC 128579	EF469123	EF469076	EF469060	EF469089	EF469107
Cordyceps nipponica	BCC 18108	KF049608	KF049626	KF049681	KF049644
Cordyceps pleuricapitata	NBRC 100745	KF049606	KF049624	KF049679	KF049642	KF049667
Cordyceps pleuricapitata	NBRC 100746	KF049607	KF049625	KF049680	KF049643	KF049668
Cordyceps sp.	EFCC 12075	KJ878909	KJ878873	KJ878957	KJ878989
Drechmeria coniospora	CBS 596.92	AF106012
Elaphocordyceps capitata	OSC 71233	AY489689	AY489721	AY489615	AY489649	DQ522421
Elaphocordyceps fracta	OSC 110990	DQ522545	DQ518759	DQ522328	DQ522373	DQ522425
Elaphocordyceps japonica	OSC 110991	DQ522547	DQ518761	DQ522330	DQ522375	DQ522428
Elaphocordyceps longisegmentis	OSC 110992		EF468816		EF468864	EF468919
Elaphocordyceps ophioglossoides	CBS 100239	KJ878910	KJ878874	KJ878958	KJ878990	KJ878944
	OSC 106405	AY489691	AY489723	AY489618	AY489652	DQ522429
Elaphocordyceps subsessilis	OSC 71235	EF469124	EF469077	EF469061	EF469090	EF469108
Haptocillium balanoides	CBS 250.82	AF339588	AF339539	DQ522342	DQ522388	DQ522442
Haptocillium sinense	CBS 567.95	AF339594	AF339545	DQ522343	DQ522389	DQ522443
Haptocillium zeosporum	CBS 335.8	AF339589	AF339540	EF469062	EF469091	EF469109
Harposporium anguillulae	ARSEF 5407		AY636080
	ARSEF 5593		AY636081
Harposporium helicoides	ARSEF 5354	AF339577	AF339527
Hirsutella crinalis	TNS F18550	KJ878911	KJ878875	KJ878959
Hirsutella sp.	OSC 128575	EF469126	EF469079	EF469064	EF469093	EF469110
Hirsutella sp.	NHJ 12525	EF469125	EF469078	EF469063	EF469092	EF469111
Hymenostilbe aurantiaca	OSC 128578	DQ522556	DQ518770	DQ522345	DQ522391	DQ522445
Hymenostilbe muscaria	OSC 151902	KJ878912	KJ878876		KJ878991	KJ878945
Hymenostilbe odonatae	TNS F18563		KJ878877		KJ878992
	TNS F27117		KJ878878
Isaria takamizuensis	NHJ 3582	EU369097	EU369034	EU369015
Isaria takamizusanensis	NHJ 3497	EU369096	EU369033	EU369014	EU369053	EU369074
Nomuraea atypicola	RCEF 3833	KJ878913	KJ878879	KJ878960	KJ878993
	OSC 151901	KJ878914	KJ878880	KJ878961	KJ878994
	CBS 744.73	EF468987	EF468841	EF468786	EF468892
Ophiocordyceps acicularis	OSC 110987	EF468950	EF468805	EF468744	EF468852
	OSC 110988	EF468951	EF468804	EF468745	EF468853
	OSC 128580	DQ522543	DQ518757	DQ522326	DQ522371	DQ522423
Ophiocordyceps agriotidis	ARSEF 5692	DQ522540	DQ518754	DQ522322	DQ522368	DQ522418
Ophiocordyceps annulata	CEM 303	KJ878915	KJ878881	KJ878962	KJ878995
Ophiocordyceps aphodii	ARSEF 5498	DQ522541	DQ518755	DQ522323		DQ522419
Ophiocordyceps brunneipunctata	OSC 128576	DQ522542	DQ518756	DQ522324	DQ522369	DQ522420
Ophiocordyceps clavata	CEM 1762	KJ878916	KJ878882	KJ878963	KJ878996
	CEM 1763		KJ878883	KJ878964	KJ878997
	NBRC 106961	JN941727	JN941414		JN992461
	NBRC 106962	JN941726	JN941415		JN992460
Ophiocordyceps communis	NHJ 12581	EF468973	EF468831	EF468775		EF468930
	NHJ 12582	EF468975	EF468830	EF468771		EF468926
Ophiocordyceps curculionum	OSC 151910	KJ878918	KJ878885		KJ878999
Ophiocordyceps dipterigena	OSC 151911	KJ878919	KJ878886	KJ878966	KJ879000
	OSC 151912	KJ878920	KJ878887	KJ878967	KJ879001
Ophiocordyceps elongata	OSC 110989		EF468808	EF468748	EF468856
Ophiocordyceps entomorrhiza	KEW 53484	EF468954	EF468809	EF468749	EF468857	EF468911
Ophiocordyceps formicarum	TNS F18565	KJ878921	KJ878888	KJ878968	KJ879002	KJ878946
Ophiocordyceps forquignonii	OSC 151908	KJ878922	KJ878889		KJ879003	KJ878947
Ophiocordyceps gracilis	EFCC 3101	EF468955	EF468810	EF468750	EF468858	EF468913
	EFCC 8572	EF468956	EF468811	EF468751	EF468859	EF468912
	OSC 151906	KJ878923	KJ878890	KJ878969
Ophiocordyceps heteropoda	EFCC 10125	EF468957	EF468812	EF468752	EF468860	EF468914
	OSC 106404	AY489690	AY489722	AY489617	AY489651
Ophiocordyceps irangiensis	OSC 128577	DQ522546	DQ518760	DQ522329	DQ522374	DQ522427
Ophiocordyceps konnoana	EFCC 7295	EF468958			EF468862	EF468915
Ophiocordyceps konnoana	EFCC 7315	EF468959		EF468753	EF468861	EF468916
Ophiocordyceps lloydii	OSC 151913	KJ878924	KJ878891	KJ878970	KJ879004	KJ878948
Ophiocordyceps longissima	EFCC 6814		EF468817	EF468757	EF468865
	TNS F18448	KJ878925	KJ878892	KJ878971	KJ879005
Ophiocordyceps longissima	HMAS_199600	KJ878926		KJ878972	KJ879006	KJ878949
Ophiocordyceps melolonthae	OSC 110993	DQ522548	DQ518762	DQ522331	DQ522376
Ophiocordyceps myrmecophila	HMAS_199620	KJ878929	KJ878895	KJ878975	KJ879009
	CEM 1710	KJ878927	KJ878893	KJ878973	KJ879007
	TNS 27120	KJ878928	KJ878894	KJ878974	KJ879008
Ophiocordyceps neovolkiana	OSC 151903	KJ878930	KJ878896	KJ878976	KJ879010
Ophiocordyceps nigrella	EFCC 9247	EF468963	EF468818	EF468758	EF468866	EF468920
Ophiocordyceps nutans	OSC 110994	DQ522549	DQ518763	DQ522333	DQ522378
Ophiocordyceps pruinosa	NHJ 12994	EU369106	EU369041	EU369024	EU369063	EU369084
Ophiocordyceps pulvinata	TNS-F 30044	GU904208		GU904209	GU904210
Ophiocordyceps purpureostromata	TNS F18430	KJ878931	KJ878897	KJ878977	KJ879011
Ophiocordyceps ravenelii	OSC 110995	DQ522550	DQ518764	DQ522334	DQ522379	DQ522430
	OSC 151914	KJ878932		KJ878978	KJ879012	KJ878950
Ophiocordyceps rhizoidea	NHJ 12522	EF468970	EF468825	EF468764	EF468873	EF468923
	NHJ 12529	EF468969	EF468824	EF468765	EF468872	EF468922
Ophiocordyceps ryogamiensis	NBRC 101751	KF049614	KF049633	KF049688	KF049650
Ophiocordyceps sinensis	EFCC 7287	EF468971	EF468827	EF468767	EF468874	EF468924
Ophiocordyceps sobolifera	KEW 78842	EF468972	EF468828		EF468875	EF468925
	TNS F18521	KJ878933	KJ878898	KJ878979	KJ879013
Ophiocordyceps sp.	TNS F18495	KJ878937	KJ878901		KJ879017
Ophiocordyceps sp.	OSC 110997	EF468976		EF468774	EF468879	EF468929
Ophiocordyceps sp.	OSC 151904	KJ878934	KJ878899	KJ878980	KJ879014
Ophiocordyceps sp.	OSC 151905	KJ878935		KJ878981	KJ879015	KJ878951
Ophiocordyceps sp.	OSC 151909	KJ878936	KJ878900	KJ878982	KJ879016	KJ878952
Ophiocordyceps sphecocephala	OSC 110998	DQ522551	DQ518765	DQ522336	DQ522381	DQ522432
Ophiocordyceps stylophora	OSC 110999	EF468982	EF468837	EF468777	EF468882	EF468931
	OSC 111000	DQ522552	DQ518766	DQ522337	DQ522382	DQ522433
Ophiocordyceps tricentri	CEM 160	AB027330	AB027376
Ophiocordyceps unilateralis	OSC 128574	DQ522554	DQ518768	DQ522339	DQ522385	DQ522436
Ophiocordyceps variabilis	OSC 111003	EF468985	EF468839	EF468779	EF468885	EF468933
	ARSEF 5365	DQ522555	DQ518769	DQ522340	DQ522386	DQ522437
Ophiocordyceps yakusimensis	HMAS_199604	KJ878938	KJ878902		KJ879018	KJ878953
Paecilomyces lilacinus	ARSEF 2181	AF339583	AF339534	EF468790	EF468896
	CBS 431.87	AY624188	EF468844	EF468791	EF468897	EF468940
	CBS 284.36	AY624189	AY624227	EF468792	EF468898	EF468941
Podocrella harposporifera	ARSEF 5472	AF339569	AF339519	DQ118747	DQ127238
Podonectria citrina	TNS F18537		KJ878903	KJ878983		KJ878954
Polycephalomyces cuboideus	TNS F18487	KF049609	KF049628	KF049683
Polycephalomyces cuboideus	NBRC 101740	KF049610	KF049629	KF049684	KF049646
Polycephalomyces formosus	ARSEF 1424	KF049615	AY259544	DQ118754	DQ127245	KF049671
Polycephalomyces nipponicus	BCC 1881	KF049618	KF049636	KF049692		KF049674
	BCC 1682	KF049620	KF049638	KF049694
	NHJ4286	KF049621	KF049639	KF049695	KF049654	KF049676
	BCC2325	KF049622	KF049640	KF049696	KF049655	KF049677
Polycephalomyces paracuboideus	NBRC 101742	KF049611	KF049630	KF049685	KF049647	KF049669
Polycephalomyces prolificus	TNS F18481	KF049612	KF049631	KF049686	KF049648
	TNS F18547	KF0496613	KF049632	KF049687	KF049649	KF049670
Polycephalomyces ramosopulvinatus	SU-65		DQ118742	DQ118753	DQ127244
	EFCC 5566		KF049627	KF049682	KF049645
Polycephalomyces sp.	JB07.08.16_08	KF049616	KF049635	KF049690	KF049652	KF049672
Polycephalomyces sp.	JB07.08.17_07b	KF049617		KF049691	KF049653	KF049673
Polycephalomyces sp.	BBC 2637	KF049619	KF049637	KF049693		KF049675
Polycephalomyces tomentosus	BL4	KF049623	AY259545	KF049697	KF049656	KF049678
Stilbella buquetii	HMAS_199613	KJ878939	KJ878904	KJ878984	KJ879019
	HMAS_199617	KJ878940	KJ878905	KJ878985	KJ879020
Tilachlidiopsis nigra	TNS 16252	KJ878941	KJ878906	KJ878986
	TNS 16250	KJ878942		KJ878987	KJ879021
Tolypocladium cylindrosporum	NRRL 28025	AF049153	AF049173

Raw sequences were processed, aligned, and gaps excluded as in Kepler , using the programs MAFFT v. 6 (Katoh , Katoh & Toh 2008), Geneious v. 7.0.6 (Biomatters, available http://www.geneious.com), and Gblocks (Talavera & Castresana 2007). The final alignment length was 4570 nucleotides - 1023 for SSU, 879 for LSU, 987 for TEF, 646 for RPB1, and 1035 for RPB2. RAxML v. 7.6.6 (Stamatakis 2006) was used to perform Maximum likelihood (ML) estimation of the phylogeny with 500 bootstrap replicates on the concatenated dataset using eleven data partitions. These included one each for SSU and LSU, and three for each of the three codon positions of the protein coding genes, TEF, RPB1, and RPB2. The GTR-GAMMA model of nucleotide substitution was used.

RESULTS AND DISCUSSION

Our results are in agreement with the overall phylogenetic structure of the order Hypocreales put forth by Sung . Nomenclatural issues for taxa in the other two families of cordyceps-like organisms, Cordycipitaceae and Clavicipitaceae, will be presented elsewhere or have already been published (Leuchtmann , Kepler ). Based on this exhaustive phylogenetic reconstruction (Fig. 1), we recognize six genera within Ophiocordycipitaceae Ophiocordyceps, Tolypocladium, Purpureocillium, Harposporium, Drechmeria, and Polycephalomyces (Table 2). This framework will provide clarity for researchers, ease of communication for instructors, and phylogenetic taxonomy around which to investigate the evolution of life histories (e.g. morphology, ecology).

Fig. 1.

ML tree of Ophiocordycipitaceae obtained using RAxML to analyze the concatenated five gene dataset (SSU, LSU, TEF, RPB1, and RPB2). Proposed genus level names to protect are delimited, but names of individual species have not been changed on the leaves of the tree, to demonstrate the diversity of taxa sampled. Values above branches represent MLBP proportions greater than or equal to 70 % from 500 replicates. Inset tree shows the larger phylogeny of Hypocreales.

Table 2.

Proposed list of generic names in Ophiocordycipitaceae to be protected and their competing synonyms. Names to be protected are in bold type, and names previously synonymized are in blue.

Proposed to protect	Proposed to suppress
Ophiocordyceps Petch, Trans. Br. Mycol. Soc. 16: 74 (1931).	Sorosporella Sorokin Zentbl. Bakt. ParasitKde., Abt. II 4: 644 (1888).
Type: O. blattae Petch 1931.	Type: S. agrotidis Sorokin 1888.
	Hirsutella Pat., Revue Mycol. 14: 67 (1892).
	Type: H. entomophila Pat. 1892.
	Didymobotryopsis Henn., Hedwigia 41: 149 (1902).
	Type: D. parasitica Henn. 1902.
	Mahevia Lagarde, Archs Zool. Exp. Gen. 56: 292 (1917).
	Type: M. guignardii (Maheu) Lagarde 1917.
	Synnematium Speare, Mycologia 12: 74 (1920).
	Type: S. jonesii Speare 1920.
	Trichosterigma Petch, Trans. Br. Mycol. Soc. 8: 215 (1923).
	Type: T. clavisporum Petch 1923.
	Didymobotrys Clem. & Shear, Gen. Fungi: 228 (1931).
	Type: D. parasitica (Henn.) Clem. & Shear 1931.
	Troglobiomyces Pacioni, Trans. Br. Mycol. Soc. 74: 244 (1980).
	Type: T. guignardii (Maheu) Pacioni 1980.
	Hymenostilbe Petch, Naturalist (Hull), ser. 3, 1931: 101 (1931).
	Type: H. muscaria Petch 1931.
	Syngliocladium Petch, Trans. Br. Mycol. Soc. 17: 177 (1932).
	Type: S. aranearum Petch 1932.
	Cordycepioideus Stifler, Mycologia 33: 83 (1941).
	Type: C. bisporus Stifler 1941.
	Paraisaria Samson & B.L. Brady, Trans. Br. Mycol. Soc. 81: 285 (1983).
	Type: P. dubia (Delacr.) Samson & B.L. Brady 1983.
Purpureocillium Luangsa-ard et al., FEMS Microbiol Lett 321: 144 (2011).
Type: P. lilacinum (Thom) Luangsa-ard et al. 2011 (syn. Penicillium lilacinum Thom 1920).
Tolypocladium W. Gams, Persoonia 6: 185 (1971).	Chaunopycnis W. Gams, Persoonia 11: 75 (1980).
Type: T. inflatum W. Gams 1971.	Type: C. alba W. Gams 1980.
	Elaphocordyceps G.H. Sung & Spatafora, Stud. Mycol. 57: 36 (2007).
	Type: E. ophioglossoides (Ehrh. ex J.F. Gmel.: Fr.) G.H. Sung et al. 2007.
Harposporium Lohde, Tagbl. Versamml. Ges. Deutsch. Naturf. 47: 206 (1874).	Polyrhina Sorokin, Annls Sci. Nat., Bot., sér 6, 4: 65 (1876).
Type: H. anguillulae Lohde 1874.	Type: P. multiformis Sorokin 1876.
	Podocrella Seaver, Mycologia 20: 57 (1928).
	Type: P. poronioides Seaver 1928.
	Atricordyceps Samuels, N.Z. Jl. Bot. 21: 174 (1983).
	Type A. harposporifera Samuels 1983.
Drechmeria W. Gams & H.-B. Jansson, Mycotaxon 22: 36 (1985).	Haptocillium W. Gams & Zare, Nova Hedwigia 73: 334 (2001).
Type: D. coniospora (Drechsler) W. Gams & H.-B. Jansson 1985 (syn. Meria coniospora Drechsler 1941).	Type: H. balanoides (Drechsler) Zare & W. Gams 2001.
Polycephalomyces Kobayasi, Sci. Rep. Tokyo Bunrika Daig., sect. B 5: 245 (1941).	Blistum B. Sutton, Mycol. Pap. 132: 16 (1973).
Type: P. formosus Kobayasi 1941.	Type: B. tomentosum (Schrad.) B. Sutton 1973.

TAXONOMY

Ophiocordyceps Petch 1931

Ophiocordyceps sensu Sung is resolved as a well-supported (MLBP=77) clade (Fig. 1, Node 3). This clade is speciose, diverse, and almost exclusively comprises insect pathogens. In spite of increased taxon sampling, current reconstructions fail to find strong statistical support at the internal nodes, and therefore we refrain from defining infrageneric groupings (Fig. 1). While Sorosporella is the oldest name for any members in this clade, there are only two described species, and Evans & Shah (2002) argued Sorosporella should be synonymized with Syngliocladium instead of being recognized as a an asexual morph, as Synnematium was previously treated with respect to Hirsutella (Evans & Samson 1982). We propose, therefore, to suppress the use of Sorosporella for this clade. Hirsutella is the next oldest name, but the type, H. entomophila, which was described growing from adult Coleoptera, has not been sampled and no culture of this species is available. Sung argued that the Hirsutella morphology was phylogenetically informative for the ‘O. unilateralis group’ which they resolved as paraphyletic, a topology recovered in the current analyses as well (Fig 1, Nodes 4 and 5). However, the Hirsutella morphology is observed in other clades (e.g. Harposporium, Polycephalomyces, Clavicipitaceae), and while it is difficult to place the type species based on morphology alone, it appears from its original description to be morphologically and ecologically (as a parasite of adults) similar to species of Hymenostilbe found in the ‘O. sphecocephala’ clade and not Hirsutella of the ‘O. unilateralis group’ (Patouillard 1892). Another reason for suppressing the use of Hirsutella for this clade is the larger number of new combinations that would have to be made – 178 for Ophiocordyceps vs. 77 for Hirsutella – as the vast majority of species encompassed here are currently described as Ophiocordyceps. Also, preservation of the name “cordyceps” within the name of O. sinensis is considered paramount given its economic, medicinal, and cultural importance in addition to being the most widely known and researched species in the clade (Shrestha ).

At this time, we also propose to suppress the use of the other names proposed for taxa in this clade, including Hymenostilbe, Syngliocladium, and Paraisaria, because these names are younger, and they contain fewer associated taxa than either Ophiocordyceps or Hirsutella. Our results suggest the restriction of Hymenostilbe to the ‘O. sphecocephala clade’ (Fig. 1, Node 6) which occupies a long branch and has strong support (MLBP=100), however, because the other internal nodes of the clade do not receive support, we refrain from making this distinction now as it would result in a paraphyletic Ophiocordyceps. These analyses place one species of Stilbella, S. buquetii, in this clade, while other studies (Seifert 1985, Gräfenhan ) have placed other Stilbella species in Nectriaceae, Bionectriaceae, or Polycephalomyces, and the current placement of Stilbella remains Hypocreales incertae sedis (Kirk ). The type of Stilbella, a coprophile, has yet to be considered in a phylogenetic context, and for these reasons we do not address that name here, but reject the use of that name for this clade. Therefore, we propose to protect Ophiocordyceps as the genus name for the entire clade, while acknowledging that future studies including more data and taxonomic sampling may provide better resolution of the relationships within the genus and a narrower concept of Ophiocordyceps.

Tolypocladium W. Gams 1971

Tolypocladium is proposed for protection over the other two generic names in the clade, Elaphocordyceps and Chaunopycnis. The clade itself is well supported (MLBP=97) in this and other published analyses (Sung , Kepler ). However, relationships between species in this clade are very sensitive to taxon sampling, and there is little bootstrap support for internal branches from the current data to justify more than one name for this clade. The asexual-sexual morph connection between Tolypocladium and some Elaphocordyceps species has been known for several years (Hodge ), although where known most Elaphocordyceps spp. do not possess the morphology associated with Tolypocladium (Sung ). While this may cause some short-term confusion, the alternative would be to name the clade Elaphocordyceps (which would cause the fewest name changes, 12 vs. 26 for Tolypocladium) and suppress Tolypocladium, a much more widely known, medicinally important, and older name, and therefore we find this a poor option. In this analysis the Chaunopycnis species sampled form a monophyletic clade which is the most divergent group within the clade. However, this may be the result of limited taxon and genetic sampling; only small subunit rDNA data for the sampled Chaunopycnis species was available for these analyses.

Here, we present a list of 26 new combinations within the genus Tolypocladium, which we emend to include species whose anamorphic forms do not possess inflated phialide bases, but that do form a single monophyletic clade encompassing a large number of truffle parasites, several insect pathogens, rotifer pathogens, and several fungi isolated to date only from soil.

Tolypocladium W. Gams, Persoonia 6: 185 (1971).

Synonyms: Chaunopycnis W. Gams, Persoonia 11: 75 (1980).

Elaphocordyceps G.H. Sung & Spatafora, Stud. Mycol. 57: 36 (2007).

Circumscription: The genus Tolypocladium is emended here to apply to all descendants of the node defined in the reference phylogeny (Fig. 1) as the terminal Tolypocladium clade. It is the least inclusive clade containing T. album, T. capitatum, T. cylindrosporum, T. fractum, T. inflatum, T. japonicum, T. longisegmentum, T. ophioglossoides, and T. pustulatum. No definitive synapomorphies are known for the clade. Morphologies associated with sexual reproductive states include robust stipitate stroma with clavate to capitate clava (e.g.T. capitatum) to highly reduced stroma comprising rhizomorphs and aggregated perithecia (e.g. T. inflatum); perithecia may be immersed and ordinal to the long axis of the stroma or superficial and produced on a highly reduced stromatic pad; asci are single-walled, long and cylindrical with a pronounced apical cap; ascospores are filiform, approximately as long as asci, septate and typically disarticulate into part-spores. Where known, asexual states include morphologies described as Tolypocladium sensu Gams (1970), Chaunopycnis sensu Gams (1979), or verticillium-like. Ecologies include parasites and pathogens of insects, rotifers and fungi, as well as, soil-inhabiting.

Type: Tolypocladium inflatum W. Gams 1971.

Tolypocladium inflatum W. Gams, Persoonia 6: 185 (1971), nom. cons.

Synonyms: Cordyceps subsessilis Petch, Trans. Brit. Mycol. Soc. 21: 39 (1937).

Elaphocordyceps subsessilis (Petch) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Cordyceps facis Kobayasi & Shimizu, Trans. Mycol. Soc. Japan 23: 361 (1982); as ‘Codyceps’.

Tolypocladium album (W. Gams) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808698

Basionym: Chaunopycnis alba W. Gams, Persoonia 11: 75 (1979).

Tolypocladium capitatum (Holmsk.: Fr.) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808699

Basionym: Clavaria capitata Holmsk., Beata Ruris Otia Fung. Dan. 1: 38 (1790).

Synonyms: Sphaeria capitata (Holmsk.: Fr.) Pers., Comm. Fung. Clav.: 13 (1797): Fr., Syst. Mycol. 2: 324 (1822).

Cordyceps capitata (Holmsk.: Fr.) Link, Handb. Erk. Gew. 3: 347 (1833).

Torrubia capitata (Holmsk.: Fr.) Tul. & C. Tul., Sel. Fung. Carpol. 3: 22 (1865).

Elaphocordyceps capitata (Holmsk.: Fr.) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Sphaeria agariciformis Bolton, Hist. Fung. Halifax: 130 (1789).

Cordyceps agariciformis (Bolton) Seaver, N. Amer. Fl. 3: 53 (1910).

Cordyceps canadensis Ellis & Everh., Bull. Torrey Bot. Club 25: 501 (1898).

Cordyceps capitata var. canadensis (Ellis & Everh.) Lloyd, Mycol. Writ. 5: 609 (1916).

Cordyceps nigriceps Peck, Bull. Torrey Bot. Club 27: 21 (1900).

Tolypocladium delicatistipitatum (Kobayasi) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808700

Basionym: Cordyceps delicatistipitata Kobayasi,Bull. Natn. Sci. Mus., Tokyo 5 (2, no. 47): 79 (1960); as ‘delicatostipitata’.

Synonym: Elaphocordyceps delicatistipitata (Kobayasi) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium fractum (Mains) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808701

Basionym: Cordyceps fracta Mains, Bull. Torrey. Bot. Club 84: 250 (1957).

Synonym: Elaphocordyceps fracta (Mains) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium inegoense (Kobayasi) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808702

Basionym: Cordyceps inegoensis Kobayasi, Bull. Natn. Sci. Mus., Tokyo 6: 292 (1963

Synonyms: Elaphocordyceps inegoensis (Kobayasi) G.H. Sung et al., Stud. Mycol. 57: 37 (2007); as ‘inegoënsis’.

Tolypocladium intermedium (S. Imai) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808703

Basionym: Cordyceps intermedia S. Imai, Proc. Imp. Acad. Japan 10: 677 (1934).

Synonyms: Elaphocordyceps intermedia (S. Imai) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium intermedium f. michinokuense (Kobayasi & Shimizu) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808704

Basionym: Cordyceps intermedia f. michinokuensis Kobayasi & Shimizu, Bull. Natn. Sci. Mus., Tokyo, B 8: 116 (1982).

Synonym: Elaphocordyceps intermedia f. michinokuensis (Kobayasi & Shimizu) G.H. Sung et al., Stud. Mycol. 57: 37 (2007); as ‘michinokuënsis’.

Tolypocladium japonicum (Lloyd) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808705

Basionym: Cordyceps japonica Lloyd, Mycol. Writ. 6 (Letter 62): 913 (1920).

Synonyms: Elaphocordyceps japonica (Lloyd) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Cordyceps umemurae S. Imai, Trans. Sapporo Nat. Hist. Soc. 11: 32 (1930) [1929]; as ‘umemurai’.

Tolypocladium jezoense (S. Imai) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808706

Basionym: Cordyceps jezoensis S. Imai, Trans. Sapporo Nat. Hist. Soc. 11: 33 (1930) [1929]. Synonym: Elaphocordyceps jezoensis (S. Imai) G.H. Sung et al., Stud. Mycol. 57: 37 (2007); as ‘jezoënsis’.

Tolypocladium longisegmentum (Ginns) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808856

Basionym: Cordyceps longisegmentis Ginns, Mycologia 80: 219 (1988).

Synonym: Elaphocordyceps longisegmentis (Ginns) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium minazukiense (Kobayasi & Shimizu) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808857

Basionym: Cordyceps minazukiensis Kobayasi & Shimizu, Bull. Natn. Sci. Mus., Tokyo, B 8: 117 (1982).

Synonym: Elaphocordyceps minazukiensis (Kobayasi & Shimizu) G.H. Sung et al., Stud. Mycol. 57: 37 (1982).

Tolypocladium miomoteanum (Kobayasi & Shimizu) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808858

Basionym: Cordyceps miomoteana Kobayasi & Shimizu, Bull. Natn. Sci. Mus., Tokyo, B 8: 118 (1982).

Synonym: Elaphocordyceps miomoteana (Kobayasi & Shimizu) G.H. Sung et al., Stud. Mycol. 57: 37 (1982).

Tolypocladium ophioglossoides (Ehrh. ex J.F. Gmel.) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808859

Basionym: Sphaeria ophioglossoides Ehrh. ex J.F. Gmel., Syst. Na., 13th edn 2: 1474 (1792).

Synonyms: Sphaeria ophioglossoides Ehrh., Pl. Crypt. Exs. fasc. 16 no. 160 (1789); nom. inval. (Art. 38.1).

Cordyceps ophioglossoides (Ehrh. ex G.F. Gmel.) Link, Handb. Erk. Gew. 3: 347 (1833): Fr., Syst. Mycol. 2: 324 (1822).

Torrubia ophioglossoides (Ehrh. ex G.F. Gmel.) Tul. & C. Tul., Sel. Fung. Carp. 3: 20 (1865).

Elaphocordyceps ophioglossoides (Ehrh. ex G.F. Gmel.) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Clavaria parasitica Willd., Fl. Berol. Prodr.: 405 (1787).

Cordyceps parasitica (Willd.) Henn., Nerthus 6: 4 (1904).

Tolypocladium ophioglossoides f. album (Kobayasi & Shimizu ex Y.J. Yao) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808860

Basionym: Cordyceps ophioglossoides f. alba Kobayasi & Shimizu ex Y.J. Yao, Acta Mycol. Sin. 14: 257 (1995).

Synonym: Elaphocordyceps ophioglossoides f. alba (Koba-yasi & Shimizu ex Y.J. Yao) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium ophioglossoides f. cuboides (Kobayasi) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808861

Basionym: Cordyceps ophioglossoides f. cuboides Kobayasi, Bull. Natn. Sci. Mus., Tokyo 5 (2, no. 47): 77 (1960).

Synonym: Elaphocordyceps ophioglossoides f. cuboides (Kobayasi) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium ovalisporum (C. Möller & W. Gams) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808862

Basionym: Chaunopycnis ovalispora C. Möller & W. Gams, Mycotaxon 48: 442 (1993).

Tolypocladium paradoxum (Kobayasi) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808863

Basionym:Cordyceps paradoxa Kobayasi, Bulletin of the Biogeogr. Soc. Jap. 9: 156 (1939).

Synonym: Elaphocordyceps paradoxa (Kobayasi) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium pustulatum (Bills et al.) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808864

Basionym:Chaunopycnis pustulata Bills et al., Mycol. Progr. 1: 8 (2002).

Tolypocladium ramosum (Teng) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808865

Basionym: Cordyceps ramosa Teng, Sinensia 7: 810 (1936).

Synonym: Elaphocordyceps ramosa (Teng) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium rouxii (Cand.) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808866

Basionym: Cordyceps rouxii Cand., Mycotaxon 4: 544 (1976).

Synonym: Elaphocordyceps rouxii (Cand.) G.H. Sung et al., Stud. Mycol. 57: 37 (2007).

Tolypocladium szemaoense (M. Zang) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808867

Basionym:Cordyceps szemaoensis M. Zang, Acta Bot. Yunn. 23: 295 (2001).

Synonym: Elaphocordyceps szemaoensis (M. Zang) G.H. Sung et al., Stud. Mycol. 57: 38 (2007); as ‘szemaoënsis’.

Tolypocladium tenuisporum (Mains) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808868

Basionym: Cordyceps tenuispora Mains, Bull. Torrey Bot. Club 84: 247 (1957).

Synonym: Elaphocordyceps tenuispora (Mains) G.H. Sung et al., Stud. Mycol. 57: 38 (2007).

Tolypocladium toriharamontanum (Kobayasi) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808869

Basionym: Cordyceps toriharamontana Kobayasi, Bull. Natn. Sci. Mus., Tokyo 6: 305 (1963).

Synonym: Elaphocordyceps toriharamontana (Kobayasi) G.H. Sung et al., Stud. Mycol. 57: 38 (2007).

Tolypocladium valliforme (Mains) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808870

Basionym: Cordyceps valliformis Mains, Bull. Torrey Bot. Club 84: 250 (1957).

Synonym: Elaphocordyceps valliformis (Mains) G.H. Sung et al., Stud. Mycol. 57: 38 (2007).

Tolypocladium valvatistipitatum (Kobayasi) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808871

Basionym: Cordyceps valvatistipitata Kobayasi, Bull. Natn. Sci. Mus., Tokyo 5(2, no. 47): 81 (1960); as ‘valvatostipitata’.

Synonym: Elaphocordyceps valvatistipitata (Kobayasi) G.H. Sung et al., Stud. Mycol. 57: 38 (2007).

Tolypocladium virens (Kobayasi) Quandt, Kepler & Spatafora, comb. nov.

MycoBank MB808872

Basionym: Cordyceps virens Kobayasi, J. Jap. Bot. 58: 222 (1983).

Synonym: Elaphocordyceps virens (Kobayasi) G.H. Sung et al., Stud. Mycol. 57: 38 (2007).

Purpureocillium Luangsa-ard et al. 2011

Our findings support those reported by Luangsa-ard for the Purpureocillium clade, and the change in Art. 59 allows for the inclusion of N. atypicola (syn. Cordyceps cylindrica) and Isaria takamizusanensis within this genus. Shared characters for this clade include purple-hued conidia and pathogenesis of arthropods, although P. lilacinum and P. lavendulum have been cultured from various substrates (Perdomo ), and P. lilacinum can cause keratitis and other mycoses in humans and other vertebrates (Pastor & Guarro 2006, Rodríguez ). Because this genus is well supported (MLBP=76) as sister to the nematode pathogen clade (Fig. 1), it is important to mention that P. lilacinum is frequently collected from nematodes (Luangsa-ard ), and has been used in the biocontrol of plant pathogenic nematodes (Kalele , Castillo ).

Harposporium Lohde 1874 and Drechmeria W. Gams & H.-B. Jansson 1985

Our analyses reconstruct a well-supported (MLBP=76) monophyletic origin of the mostly nematophagous clade of Ophiocordycipitaceae (Fig. 1 Node 2). Within this clade, there is strong phylogenetic support for two clades: one containing Harposporium and Podocrella, and the other consisting of Drechmeria, Haptocillium, and Cordyceps gunnii. The relationship between Harposporium and Podocrella has already been described (Chaverri ), but the revision of Art. 59 requires that one name be chosen for this genus. Harposporium is an older name, and the morphology of at least somewhat crescent-shaped conidia is a shared character for this clade. Suppression of Podocrella also requires the fewest taxonomic revisions (3 vs 30). For these reasons, we propose to protect Harposporium over Podocrella (Table 2).

Within the other nematophagous subclade, Drechmeria is an older name than Haptocillium, and the isolate included in these analyses is nested within the Haptocillium isolates sampled. For this reason, we propose to protect Drechmeria over Haptocillium. The inclusion of C. gunnii in this clade also provides a name for this residual taxon of Cordyceps. Most species however, are nematophagous (C. gunnii being the exception), and conidia may be cone-shaped, formed on conidiogenous cells in rosettes or verticils, or in the case of C. gunnii, paecilomyces-like. We did not have access to molecular data from D. harposporioides, but given our finding that the two nematophagous clades in Ophiocordycipitaceae are monophyletic in origin, it will be interesting to see if this species, a protozoan pathogen with helical conidia, is truly a member of the Drechmeria clade or in fact a species within Harposporium that simply lacks the basally swollen conidiogenous cells.

Polycephalomyces Kobayasi 1941

This study is the first to have definitive ML support (MLBP=82) for the sister relationship between the Polycephalomyces clade and Ophiocordycipitaceae (Fig. 1 Node 1). Support for this relationship remains even with the exclusion of C. pleuricapitata, which is on an early-diverging, long branch within the clade. Two options remain to deal with this finding. Either a new family must be erected to account for this clade, or Polycephalomyces and related taxa must be moved into Ophiocordycipitaceae. We propose to accept Polycephalomyces and C. pleuricapitata in Ophiocordycipitaceae, where it will be the earliest diverging lineage of the family. The taxonomy of C. pleuricapitata will be addressed elsewhere.

CONCLUSIONS

We present a concise, thorough, phylogenetically relevant, and taxonomically accurate revision of the family Ophiocordycipitaceae with the aim of complying with the changes to Art. 59 of the ICN. With the criteria of naming monophyletic taxa, and where possible, of adhering to priority while avoiding changes that would be disruptive to the wider community of researchers, we have proposed to protect six genera within Ophiocordycipitaceae, including incorporation of the genus Polycephalomyces within the family. We have also formally revised the genus Tolypocladium, to reflect the nomenclature suggested by our results.