Ana M. Millanes

Phylogeny and character evolution in the jelly fungi (Tremellomycetes, Basidiomycota, Fungi)

The Tremellomycetes (Agaricomycotina, Basidiomycota, Fungi) are a nutritionally heterogeneous group comprising saprotrophs, animal parasites, and fungicolous species (fungal-inhabiting, including lichen-inhabiting). The relationships of many species, particularly those with a lichenicolous habit, have never been investigated by molecular methods. We present a phylogeny of the Tremellomycetes based on three nuclear DNA ribosomal markers (nSSU, 5.8S and nLSU), representing all main taxonomic groups and life forms, including lichenicolous taxa. The Cystofilobasidiales, Filobasidiales, Holtermanniales, and Tremellales (including the Trichosporonales) are recovered as monophyletic, but this is not the case for the Tremellomycetes. We suggest, however, that the Cystofilobasidiales tentatively continue to be included in the Tremellomycetes. As currently circumscribed, the Filobasidiaceae, Sirobasidiaceae, Syzygosporaceae and Tremellaceae are non-monophyletic. Cuniculitremaceae, Sirobasidiaceae and Tetragoniomycetaceae are nested within Tremellaceae. The lichenicolous species currently included within the Tremellomycetes belong in this group, distributed across the Filobasidiales and Tremellales. Lichen-inhabiting taxa do not form a monophyletic group; they are distributed in several clades and sometimes intermixed with taxa of other nutritional habits. Character state reconstruction indicates that two morphological traits claimed to characterize groups in the Tremellomycetes (the basidium habit and basidium septation) are highly homoplastic. Comparative phylogenetic methods suggest that the transitions between single and catenulate basidia in the Tremellales are consistent with a punctuational model of evolution whereas basidium septation is likely to have evolved under a graduational model in the clade comprising the Holtermanniales, Filobasidiales, and Tremellales.

Host switching promotes diversity in host-specialized mycoparasitic fungi: uncoupled evolution in the Biatoropsis - Usnea system

Fungal mycoparasitism—fungi parasitizing other fungi—is a common lifestyle in some basal lineages of the basidiomycetes, particularly within the Tremellales. Relatively nonaggressive mycoparasitic fungi of this group are in general highly host specific, suggesting cospeciation as a plausible speciation mode in these associations. Species delimitation in the Tremellales is often challenging because morphological characters are scant. Host specificity is therefore a great aid to discriminate between species but appropriate species delimitation methods that account for actual diversity are needed to identify both specialist and generalist taxa and avoid inflating or underestimating diversity. We use the Biatoropsis‐Usnea system to study factors inducing parasite diversification. We employ morphological, ecological, and molecular data—methods including genealogical concordance phylogenetic species recognition (GCPSR) and the general mixed Yule‐coalescent (GMYC) model—to assess the diversity of fungi currently assigned to Biatoropsis usnearum. The degree of cospeciation in this association is assessed with two cophylogeny analysis tools (ParaFit and Jane 4.0). Biatoropsis constitutes a species complex formed by at least seven different independent lineages and host switching is a prominent force driving speciation, particularly in host specialists. Combining ITS and nLSU is recommended as barcode system in tremellalean fungi.

Parmelia sulcata (Ascomycota: Parmeliaceae), a sympatric monophyletic species complex

Recently, the number of cryptic species known has increased considerably, showing that species diversity has in many cases been underestimated in the past. Parmelia sulcata is a widely distributed species and one of the most common taxa in temperate Europe. The first intra-specific molecular studies on P. sulcata showed an unexpectedly high genetic variability. In the present work, we study the biodiversity of this taxon including specimens from four continents and using three molecular markers (nuITS, nuIGS rDNA, and partial β-tubulin gene). Two monophyletic groups of P. sulcata were encountered; one of these is epitypified as P. sulcata s. str and the other one is segregated as the new cryptic species P. encryptata sp. nov. Issues surrounding the lectotypification of Parmelia sulcata have also been elucidated.

Lichenicolous fungi show population subdivision by host species but do not share population history with their hosts

Lichenicolous fungi are a species-rich biological group growing on lichen thalli. Here, we analyze the genetic structure of the lichenicolous basidiomycete Tremella lobariacearum and three host species (Lobaria pulmonaria, Lobaria macaronesica, and Lobaria immixta) in Macaronesia. We used ordination and analysis of molecular variance to investigate the structuring of genetic variation, and a simulation test to investigate whether rDNA haplotypes of T. lobariacearum were significantly associated with host species. To investigate the evolutionary and demographic history of the lichenicolous fungus and its hosts, we used coalescent samplers to generate trees, and Bayesian skyline plots. We found that the hosts were most important in structuring populations of the lichenicolous species. Despite their wide geographic distribution, the same haplotypes of T. lobariacearum consistently associated with a given host species. Our results suggest that the Lobaria hosts create a selective environment for the lichenicolous fungus. Both the pathogen and the host populations exhibited substantial genetic structure. However, evolutionary and demographic histories differed between the parasite and its hosts, as evidenced by different divergence times and tree topologies.

Molecular phylogenetic studies on the lichenicolous Xanthoriicola physciae reveal Antarctic rock-inhabiting fungi and Piedraia species among closest relatives in the Teratosphaeriaceae

The phylogenetic placement of the monotypic dematiaceous hyphomycete genus Xanthoriicola was investigated. Sequences of the nLSU region were obtained from 11 specimens of X. physciae, which formed a single clade supported both by parsimony (91 %), and maximum likelihood (100 %) bootstraps, and Bayesian Posterior Probabilities (1.0). The closest relatives in the parsimony analysis were species of Piedraria, while in the Bayesian analysis they were those of Friedmanniomyces. These three genera, along with species of Elasticomyces, Recurvomyces, Teratosphaeria, and sequences from unnamed rock-inhabiting fungi (RIF), were all members of the same major clade within Capnodiales with strong support in both analyses, and for which the family name Teratosphaeriaceae can be used pending further studies on additional taxa.

Phylogeny of the Acarosporaceae (Lecanoromycetes, Ascomycota, Fungi) and the evolution of carbonized ascomata

The phylogeny of the Acarosporaceae (Lecanoromycetes, Acarosporomycetidae, Acarosporales) is investigated using data from three molecular markers; nuclear ITS-LSU rDNA, mitochondrial SSU and β-tubulin. Acarosporaceae is shown to be constituted by six main clades; Myriospora, Timdalia, Pleopsidium, a clade composed by “Acarospora” rhizobola and “A.” terricola, the poorly supported Sarcogyne clade (including several Polysporina and Acarospora species) and the Acarospora clade (including the type of Polysporina, P. simplex, and several other Polysporina species). The common ancestor of the Acarosporaceae did not produce strongly black pigmented (carbonized or melanized) ascomata, but this trait has arisen secondarily and independently numerous times in the evolution of the group. The number of changes in character states of both carbonized epihymenium and carbonized exciple are considerably more than the minimum number. The genera Sarcogyne and Polysporina—largely circumscribed based on the presence of black pigmented ascomata—are shown to be distinctly non-monophyletic. The presence of green algae in the ascoma margin (lecanorine or lecideine ascomata) may vary even within single species.

Cyphobasidium gen. nov., a new lichen-inhabiting lineage in the Cystobasidiomycetes (Pucciniomycotina, Basidiomycota, Fungi)

Pucciniomycotina is a highly diverse group of fungi, showing a remarkably wide range of lifestyles and ecologies. However, lichen-inhabiting fungi are only represented by a few species included in the genera Chionosphaera and Cystobasidium, and their phylogenetic position has never been investigated. Phylogenetic analyses using the nuclear SSU, ITS, and LSU ribosomal DNA markers reveal that the lichenicolous members of Cystobasidium (C. hypogymniicola, C. usneicola) form a monophyletic group distinct from Cystobasidium and outside the Cystobasidiales. The new genus Cyphobasidium is consequently described to accommodate these lichen-inhabiting species. Cyphobasidium is characterized by producing conspicuous galls on the host lichen thalli, by having distinctive basidia that arise from a thick-walled, cup-like structure, the probasidium, that persists after the senescence of the actual basidium (meiosporangium), and by its lichenicolous occurrence on species of Hypogymnia and Usnea. Cyphobasidium is one of the few representatives of the Cystobasidiomycetes in which the sexual stage predominates in nature, whereas most species in the group are known only from an asexual yeast phase. This is the first time the position of lichen-inhabiting taxa within the Pucciniomycotina is investigated using molecular data.

Roselliniella revealed as an overlooked genus of Hypocreales, with the description of a second species on parmelioid lichens

Based on newly obtained 28S rDNA sequences from Roselliniella atlantica and R. euparmeliicola sp. nov., the genus Roselliniella has to be placed in Hypocreales and not in Sordariales; however, the family placement could not be resolved from the sequences obtained. The mature ascospores are single-celled and brown, but young ascospores are hyaline and sometimes have a median septum. The new species occurs on a Parmelia s.str. species in China, and differs in 24 nucleotide substitution positions in the nu-LSU rDNA region and ascospore size from R. atlantica. In this case, small variations in ascospore sizes and shape prove to be phylogenetically and taxonomically informative. The two species occur in the same clade with 95 % jack-knife support. Roselliniella atlantica occurs on Xanthoparmelia and Melanohalea species in Europe, whereas R. euparmeliicola was found on the species of Parmelia s.str. DNA was successfully recovered from a dried specimen of R. atlantica collected in 1992. Two unidentified fungi were also recovered from the Chinese specimen, and these belong to Sordariomycetidae and Dothideomycetes; whether these two are additional fungi living endolichenically in the lichen host, saprobes, or contaminants could not be ascertained.

Tremella cetrariellae (Tremellales, Basidiomycota, Fungi), a new lichenicolous fungus on Cetrariella delisei

Tremella cetrariellae (Tremellales, Basidiomycota, Fungi), a new lichenicolous species on Cetrariella delisei

Understanding lichenicolous heterobasidiomycetes: new taxa and reproductive innovations in Tremella s.l.

Four new lichenicolous Tremella species are described and characterized morphologically and molecularly. Tremella celata grows on Ramalina fraxinea, inducing the formation of inconspicuous galls, and having hyphae with incomplete clamps. Tremella endosporogena develops intrahymenially in the apothecia of Lecanora carpinea, having single-celled basidia and clampless hyphae. Tremella diederichiana is the name proposed for a species micromorphologically close to T. christiansenii but inducing the formation of small, pale galls on the thallus and apothecia of Lecidea aff. erythrophaea. Tremella variae grows on Lecanora varia thallus, instead of on the apothecia, as do the other known Tremella species parasitizing Lecanora s.l. Phylogenetic relationships and host specificity of these species are investigated and compared with other taxa that show morphological resemblances, phylogenetic affinities or similar hosts. The formation of mitotic conidia inside old basidia (endospores), which is a poorly known reproductive strategy in the Basidiomycota, is also a distinctive character of Tremella endosporogena. A discussion on the reproductive role and systematic implications of endospores is included.