Current nomenclatural changes in Cordyceps sensu lato and its multidisciplinary impacts

ABSTRACT Innumerable name changes have occurred in Cordyceps and allied taxa, after the phylogenetic classification of Cordyceps, coupled by the application of one fungus one name after the amendment of ICN. Complying with one fungus one name, many generic names have been protected for monophyletic clades in Clavicipitaceae and Ophiocordycipitaceae that have made tremendous transfer of Cordyceps spp. to both sexual and asexual genera. Species compositions of the accepted genera Ophiocordyceps, Tolypocladium, Metarhizium, Perennicordyceps, Polycephalomyces and Purpureocillium are briefly discussed to update the readers with the current placements of Cordyceps spp. Some examples of frequent name changes of Cordyceps spp. are also mentioned, with reference to use of older scientific names in non-mycological publications.


Phylogenetic classification of Cordyceps
The genus Cordyceps, established by Fries (1818), was traditionally classified in Clavicipitaceae (Hypocreales, Ascomycota) to accommodate insect and fungal parasites, producing elongated, cylindrical or filamentous stromata with perithecioid type of ascocarp and filamentous, multi-septate ascospores. It is a big hypocrealean genus, comprising more than 400 spp. that parasitise numerous orders of insects, including spiders, in majority (Araújo and Hughes 2016;Shrestha et al. 2016). Cordyceps Fr. and allied species are very curious groups of fungi, with long botanical history starting in pre-Linnaean era (Shrestha et al. 2014). Recent molecular phylogenetic studies showed that Cordyceps sensu lato is not monophyletic and is intercepted by plant pathogenic genera Claviceps Tul., Balansia Speg., Epichloë (Fr.) Tul. and C. Tul. within Clavicipitaceae (Sung et al. 2007). Cordyceps sensu stricto was, hence, circumscribed to a clade that consisted of its type species C. militaris (L.) Fr., and new genera were proposed for other clades outside Cordyceps spp. (Sung et al. 2007;Kepler et al. 2012b) (Figure 1). Besides transfer of many Cordyceps spp. to new genera, many more Cordyceps spp. (~170 spp.) still remain incertae sedis (of uncertain placement) within Hypocreales, because of lack of molecular phylogenetic studies or inconclusive morphological and ecological assessment (Sung et al. 2007).
Among the new genera, Metacordyceps shared sister relationship with a clade of plant pathogenic genera (Claviceps, Balansia, Epichloë) and were all retained in the family Clavicipitaceae s.s. (Sung et al. 2007). Tyrannicordyceps is a small genus placed within a clade of Balansia, Claviceps and Epichloë, to which all five spp. were transferred from Cordyceps (Kepler et al. 2012b). All the members of Tyrannicordyceps are pathogens of Claviceps stromata. Elaphocordyceps, Ophiocordyceps and other allied genera formed a separate clade and were placed in a new family Ophiocordycipitaceae that formed a sister clade with Clavicipitaceae s.s. (Sung et al. 2007 (Sung et al. 2007).
As mentioned above, Cordyceps s.s. was circumscribed to a clade in Cordycipitaceae that consists of its type species C. militaris (Sung et al. 2007 (Sung et al. 2007;Shrestha et al. 2010).

Clavicipitaceae
Podocrella is linked to Harposporium, which is mainly known from nematodes (Chaverri et al. 2005b).  (Kepler et al. 2013Quandt et al. 2014;Spatafora et al. 2015;Humber 2016). Following one fungus one name, only a single generic name regardless of its state will be protected or accepted for a monophyletic clade against all other generic names available in that clade based on nomenclatural priority in principle, so that a single scientific name can be given to a single species. Recently, single generic names have been protected for monophyletic clades of invertebrate pathogens in Ophiocordycipitaceae and Clavicipitaceae. The protected names that accommodate former Cordyceps spp. are briefly discussed below ( Figure 2).

Ophiocordyceps
It is the largest genus in Ophiocordycipitaceae with 214 spp. Among them, 194 spp. are transferred from Cordyceps or are typified by cordyceps-like sexual states (Figure 2). Besides Cordyceps or cordycepslike spp., Ophiocordyceps includes other spp. transferred from sexual and asexual genera, based on their phylogenetic placement (Figure 3). Among sexual spp., two spp. from each Podonectria Petch and Torrubiella were transferred to Ophiocordyceps (Spatafora et al. 2015) (Figure 3). Similarly, many other asexually typified spp. were transferred to Ophiocordyceps such as nine Hymenostilbe spp., five Syngliocladium spp. and one sp. from each Paraisaria and Stilbella Lindau (Spatafora et al. 2015) (Figure 3).
Ophiocordyceps thus consists of both sexually and asexually typified spp. For such genera as Ophiocordyceps, Metarhizium, Tolypocladium, alternative or suppressed generic names retain the role of morphological descriptors as suggested by Gams (2016).

Clavicipitaceae
Metarhizium is a protected generic name in Clavicipitaceae that comprises spp. previously classified in Cordyceps. Metarhizium currently consists of 25 spp. Among them, 13 spp. were transferred from Cordyceps or Metacordyceps to Metarhizium, complying with one fungus one name (Figures 2 and 7). As shown in Figure 7, among 11 spp. transferred from Cordyceps, nine spp. were first transferred from Cordyceps to Metacordyceps prior to transfer to Metarhizium (Sung et al. 2007;Kepler et al. 2012aKepler et al. , 2014. Another sp. was first transferred from Cordyceps to Ophiocordyceps and then finally to Metarhizium (Sung et al. 2007;Kepler et al. 2014). The remaining sp. was first transferred from Cordyceps to Ophiocordyceps and then to Metacordyceps prior to transfer to Metarhizium (Sung et al. 2007;Kepler et al. 2012aKepler et al. , 2014. Two  more Metacordyceps spp. were transferred to Metarhizium, following one fungus one name ) (Figure 7).

Incertae sedis within hypocreales
Besides nearly 170 Cordyceps spp. incertae sedis within Hypocreales, Sphaerocordyceps Kobayasi also belongs to this group (Kobayasi 1981;Sung et al. 2007) (Figure 2 Impact of one fungus one name on nomenclature of Cordyceps spp. The use of entomopathogenic fungi is getting wider due to their economic and environmental importance. Several species of Cordyceps are highly regarded as medicinal herbs in oriental medicine in Asia and have been successfully cultivated for commercial application. Other entomopathogenic fungi, asexual spp. in particular, have been successfully used for biological control of insects and pests. Professionals such as biochemists, pharmacologists, alternative (traditional) medicine practitioners, drug researchers, biocontrol researchers, insect pathologists, forest pathologists and entomologists are widely involved in the research and use of entomopathogenic fungi, besides mycologists.
To cope with name changes of fungal spp., different authors have suggested for the smooth application of one fungus one name for the benefit of their user groups, such as plant pathogenic fungi and medically important fungi (Wingfield et al. 2012;Zhang et al. 2013;De Hoog et al. 2015). De Hoog et al. (2015 have cautioned that nomenclatural changes of medically important fungi may take decades to gain wide acceptance and have suggested some delay in following name changes. With respect to hypocrealean invertebrate-parasitic fungi, Kepler et al. (2013Kepler et al. ( , 2014, Quandt et al. (2014) and Spatafora et al. (2015) have vastly contributed to the application of one fungus one name.
The name changes have been two-fold for hypocrealean invertebrate-parasitic fungi in recent years that have caused multiple name changes within a short duration in some cases: the first one based on the phylogenetic arrangement of Cordyceps spp. and the second one based on the application of one fungus one name. The phylogenetic arrangement of Cordyceps spp. has been discussed above. The name changes following one fungus one name are more diverse. They are briefly discussed here with reference to multiple name changes from Cordyceps to Perennicordyceps, for instance ( Figure 8). Cordyceps cuboidea and C. ryogamiensis were transferred to Ophiocordyceps following the phylogenetic split of genus Cordyceps and were renamed as Ophiocordyceps cuboidea and O. ryogamiensis, respectively (Sung et al. 2007). After the application of one fungus one name, they were again named as Polycephalomyces cuboideus and Po. ryogamiensis as Polycephalomyces was protected for a clade where O. cuboidea and O. ryogamiensis were placed (Kepler et al. 2013). However, the clade that included Polycephalomyces cuboideus and Po. ryogamiensis was again delineated as a separate genus Perennicordyceps and consequently the spp. were renamed as Perennicordyceps cuboidea and Pe. Ryogamiensis, respectively (Matočec et al. 2014). De Hoog et al. (2015 recently opined that when clade system is used for naming, there is no delimitation criterion and that when a genus becomes nearly congruent to species, then it becomes a redundant rank. Perennicordyceps cuboidea (Kobayasi & Shimizu) Matočec et al. (2014) Basionym: Cordyceps cuboidea Kobayasi & Shimizu (1980) Synonyms: Ophiocordyceps cuboidea (Kobayasi & Shimizu) S. Ban et al. (2009).
Polycephalomyces cuboideus (Kobayasi & Shimizu) Kepler et al. (2013) Perennicordyceps ryogamiensis (Kobayasi & Shimizu) Matočec et al. (2014) Basionym: Cordyceps ryogamiensis Kobayasi & Shimizu (1983) Synonyms: Ophiocordyceps ryogamiensis (Kobayasi & Shimizu) G.H. Sung et al. (2007) Polycephalomyces ryogamiensis (Kobayasi & Shimizu) Kepler et al. (2013) Minnis (2015) has rightly pointed out that due to frequent name changes, the users of fungal names get frustrated. Few examples are shown here where older names of Cordyceps spp. are being used in nonmycological publications despite nomenclatural changes. Cordyceps sinensis was established by Saccardo (1883) during the taxonomic revision of Cordyceps that was recently transferred to Ophiocordyceps resulting in O. sinensis as its currently accepted name, after the phylogenetic classification of Cordyceps (Sung et al. 2007) and is now widely accepted by the mycological community. However, the older name C. sinensis is still in frequent use in non-mycological publications Yu et al. 2016), despite its recent nomenclatural change. Similarly, C. ophioglossoides (Sun et al. 2014) and C. sobolifera (Yang and Zhang 2016) are used in publications, in spite of their recent nomenclatural changes. Though non-mycologists know the name changes, they may ignore in publications. Editors or reviewers of non-mycological journals may also simply not be aware of current nomenclatural changes of fungal species or may not put much emphasis on names changes. It is also true that nonmycologists may not be aware of worldwide online databases of fungi such as MycoBank, IndexFungorum and Fungal Names to be update with the fungal name changes. The more rapidly the name changes take place, other professionals will simply feel safe by using older names.