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      Phylogeny- and morphology-based recognition of new species in the spider-parasitic genus Gibellula (Hypocreales, Cordycipitaceae) from Thailand

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          Abstract

          Thailand is known to be a part of what is called the Indo-Burma biodiversity hotspot, hosting a vast array of organisms across its diverse ecosystems. This is reflected by the increasing number of new species described over time, especially fungi. However, a very few fungal species from the specialized spider-parasitic genus Gibellula have ever been reported from this region. A survey of invertebrate-pathogenic fungi in Thailand over several decades has led to the discovery of a number of fungal specimens with affinities to this genus. Integration of morphological traits into multi-locus phylogenetic analysis uncovered four new species: G. cebrennini , G. fusiformispora , G. pigmentosinum , and G. scorpioides . All these appear to be exclusively linked with torrubiella-like sexual morphs with the presence of granulomanus-like asexual morph in G. pigmentosinum and G. cebrennini . A remarkably high host specificity of these new species towards their spider hosts was revealed, and for the first time, evidence is presented for manipulation of host behavior in G. scorpioides .

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          Phylogenetic classification of Cordyceps and the clavicipitaceous fungi

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

            Grass-associated fungi (grass symbionts) in the family Clavicipitaceae (Ascomycota, Hypocreales) are species whose host range is restricted to the plant family Poaceae and rarely Cyperaceae. The best-characterized species include Claviceps purpurea (ergot of rye) and Neotyphodium coenophialum (endophyte of tall fescue). They have been the focus of considerable research due to their importance in agricultural and grassland ecosystems and the diversity of their bioactive secondary metabolites. Here we show through multigene phylogenetic analyses and ancestral character state reconstruction that the grass symbionts in Clavicipitaceae are a derived group that originated from an animal pathogen through a dynamic process of interkingdom host jumping. The closest relatives of the grass symbionts include the genera Hypocrella, a pathogen of scale insects and white flies, and Metarhizium, a generalist arthropod pathogen. These data do not support the monophyly of Clavicipitaceae, but place it as part of a larger clade that includes Hypocreaceae, a family that contains mainly parasites of other fungi. A minimum of 5-8 independent and unidirectional interkingdom host jumps has occurred among clavicipitaceous fungi, including 3-5 to fungi, 1-2 to animals, and 1 to plants. These findings provide a new evolutionary context for studying the biology of the grass symbionts, their role in plant ecology, and the evolution of host affiliation in fungal symbioses.
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              Comparative biology ofPortia africana, P. albimana, P. fimbriata, P. labiata, andP. shultzi, araneophagic, web-building jumping spiders (Araneae: Salticidae): Utilisation of webs, predatory versatility, and intraspecific interactions

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                Author and article information

                Contributors
                Journal
                MycoKeys
                MycoKeys
                11
                urn:lsid:arphahub.com:pub:C004A564-9D6A-5F9F-B058-6A3815DFE9C3
                MycoKeys
                Pensoft Publishers
                1314-4057
                1314-4049
                2020
                02 September 2020
                : 72
                : 17-42
                Affiliations
                [1 ] National Center for Genetic Engineering and Biotechnology (BIOTEC), 113 Thailand Science Park, Phahonyothin Road, Khlong Nueng, Khlong Luang, Pathum Thani 12120 Thailand National Center for Genetic Engineering and Biotechnology (BIOTEC) Pathum Thani Thailand
                [2 ] Department of Biotechnology, Faculty of Science and Technology, Thammasat University, Pathumthani 12120 Thailand Thammasat University Pathumthani Thailand
                [3 ] Department of Microbial Drugs, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany Helmholtz Centre for Infection Research Braunschweig Germany
                Author notes
                Corresponding author: J. Jennifer Luangsa-ard ( jajen@ 123456biotec.or.th )

                Academic editor: T. Lumbsch

                Article
                55088
                10.3897/mycokeys.72.55088
                7481265
                Wilawan Kuephadungphan, Kanoksri Tasanathai, Booppa Petcharad, Artit Khonsanit, Marc Stadler, J. Jennifer Luangsa-ard

                This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Funding
                National Center for Genetic Engineering and Biotechnology (BIOTEC) Platform Technology Management (Grant no. P19-50231) European Union’s Horizon 2020 Research Innovation and Staff Exchange programme (RISE) under the Marie Skłodowska-Curie grant agreement No 645701, Project acronym “GoMyTri”
                Categories
                Research Article
                Hypocreales
                Sordariomycetes
                Habitats
                Ecosystems & Natural Spaces
                Molecular Systematics
                Nomenclature
                Phylogeny
                Taxonomy
                Asia

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