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      Diversity, population genetics, and evolution of macrofungi associated with animals

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          Abstract

          Macrofungi refers to all fungi that produce visible fruiting bodies. These fungi are evolutionarily and ecologically very divergent. Evolutionarily, they belong to two main phyla, Ascomycota and Basidiomycota, and many of them have relatives that cannot form visible fruiting bodies. Ecologically, macrofungi can be associated with dead organic matter, plants, and animals. Here we review our current understanding of population structure and biogeography of macrofungi associated with animals. Their interactions, functions, and patterns of coevolution are described and discussed. Our focus is on studies using molecular markers. Our analyses suggest that the types of fungi–animal associations play an important role in the structure of these animal-associated fungal populations.

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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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            The evolution of fungus-growing termites and their mutualistic fungal symbionts.

            We have estimated phylogenies of fungus-growing termites and their associated mutualistic fungi of the genus Termitomyces using Bayesian analyses of DNA sequences. Our study shows that the symbiosis has a single African origin and that secondary domestication of other fungi or reversal of mutualistic fungi to a free-living state has not occurred. Host switching has been frequent, especially at the lower taxonomic levels, and nests of single termite species can have different symbionts. Data are consistent with horizontal transmission of fungal symbionts in both the ancestral state of the mutualism and most of the extant taxa. Clonal vertical transmission of fungi, previously shown to be common in the genus Microtermes (via females) and in the species Macrotermes bellicosus (via males) [Johnson, R. A., Thomas, R. J., Wood, T. G. & Swift, M. J. (1981) J. Nat. Hist. 15, 751-756], is derived with two independent origins. Despite repeated host switching, statistical tests taking phylogenetic uncertainty into account show a significant congruence between the termite and fungal phylogenies, because mutualistic interactions at higher taxonomic levels show considerable specificity. We identify common characteristics of fungus-farming evolution in termites and ants, which apply despite the major differences between these two insect agricultural systems. We hypothesize that biparental colony founding may have constrained the evolution of vertical symbiont transmission in termites but not in ants where males die after mating.
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              Phylogenetic relationships in Cortinarius, section Calochroi, inferred from nuclear DNA sequences

              Background Section Calochroi is one of the most species-rich lineages in the genus Cortinarius (Agaricales, Basidiomycota) and is widely distributed across boreo-nemoral areas, with some extensions into meridional zones. Previous phylogenetic studies of Calochroi (incl. section Fulvi) have been geographically restricted; therefore, phylogenetic and biogeographic relationships within this lineage at a global scale have been largely unknown. In this study, we obtained DNA sequences from a nearly complete taxon sampling of known species from Europe, Central America and North America. We inferred intra- and interspecific phylogenetic relationships as well as major morphological evolutionary trends within section Calochroi based on 576 ITS sequences, 230 ITS + 5.8S + D1/D2 sequences, and a combined dataset of ITS + 5.8S + D1/D2 and RPB1 sequences of a representative subsampling of 58 species. Results More than 100 species were identified by integrating DNA sequences with morphological, macrochemical and ecological data. Cortinarius section Calochroi was consistently resolved with high branch support into at least seven major lineages: Calochroi, Caroviolacei, Dibaphi, Elegantiores, Napi, Pseudoglaucopodes and Splendentes; whereas Rufoolivacei and Sulfurini appeared polyphyletic. A close relationship between Dibaphi, Elegantiores, Napi and Splendentes was consistently supported. Combinations of specific morphological, pigmentation and molecular characters appear useful in circumscribing clades. Conclusion Our analyses demonstrate that Calochroi is an exclusively northern hemispheric lineage, where species follow their host trees throughout their natural ranges within and across continents. Results of this study contribute substantially to defining European species in this group and will help to either identify or to name new species occurring across the northern hemisphere. Major groupings are in partial agreement with earlier morphology-based and molecular phylogenetic hypotheses, but some relationships were unexpected, based on external morphology. In such cases, their true affinities appear to have been obscured by the repeated appearance of similar features among distantly related species. Therefore, further taxonomic studies are needed to evaluate the consistency of species concepts and interpretations of morphological features in a more global context. Reconstruction of ancestral states yielded two major evolutionary trends within section Calochroi: (1) the development of bright pigments evolved independently multiple times, and (2) the evolution of abruptly marginate to flattened stipe bulbs represents an autapomorphy of the Calochroi clade.
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                Author and article information

                Journal
                Mycology
                Mycology
                TMYC
                tmyc20
                Mycology
                Taylor & Francis
                2150-1203
                2150-1211
                2015
                18 May 2015
                : 6
                : 2 , Diversity, Population Genetics, and Phylogeography of Selected Wild Mushrooms
                : 94-109
                Affiliations
                [a ]Laboratory for Conservation and Utilization of Bio-Resources, and Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University , Kunming650091, Yunnan, PR China
                [b ]Yunnan Institute for Tropical Crop Research , Jinghong, Yunnan, China
                [c ]Department of Biology, McMaster University , Hamilton, Ontario, CanadaL8S 4K1
                Author notes
                [* ]Corresponding author. Email: yzh_1210@ 123456hotmail.com
                Article
                1043968
                10.1080/21501203.2015.1043968
                6106070
                © 2015 Mycological Society of China

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Tables: 2, References: 127, Pages: 16
                Product
                Funding
                Funded by: National Natural Science Foundation Programs of PR China
                Award ID: 31100018
                Award ID: 31470147
                Funded by: Yunnan Province High-Profile Talents Program
                Award ID: 2010CI106
                This work was supported by the Yunnan Province High-Profile Talents Program [grant number 2010CI106]; National Natural Science Foundation Programs of PR China [grant numbers 31100018 and 31470147].
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                macrofungi, animals, interaction, population, coevolution

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