Andrew W. Wilson

Reconstructing the early evolution of Fungi using a six-gene phylogeny

The ancestors of fungi are believed to be simple aquatic forms with flagellated spores, similar to members of the extant phylum Chytridiomycota (chytrids). Current classifications assume that chytrids form an early-diverging clade within the kingdom Fungi and imply a single loss of the spore flagellum, leading to the diversification of terrestrial fungi. Here we develop phylogenetic hypotheses for Fungi using data from six gene regions and nearly 200 species. Our results indicate that there may have been at least four independent losses of the flagellum in the kingdom Fungi. These losses of swimming spores coincided with the evolution of new mechanisms of spore dispersal, such as aerial dispersal in mycelial groups and polar tube eversion in the microsporidia (unicellular forms that lack mitochondria). The enigmatic microsporidia seem to be derived from an endoparasitic chytrid ancestor similar to Rozella allomycis, on the earliest diverging branch of the fungal phylogenetic tree.

Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota).

This study uses phylogenetic analysis of the Sclerodermatineae to reconstruct the evolution of ectomycorrhizal host associations in the group using divergence dating, ancestral range and ancestral state reconstructions. Supermatrix and supertree analysis were used to create the most inclusive phylogeny for the Sclerodermatineae. Divergence dates were estimated in BEAST. Lagrange was used to reconstruct ancestral ranges. BayesTraits was used to reconstruct ectomycorrhizal host associations using extant host associations with data derived from literature sources. The supermatrix data set was combined with internal transcribed spacer (ITS) data sets for Astraeus, Calostoma, and Pisolithus to produce a 168 operational taxonomic unit (OTU) supertree. The ensuing analysis estimated that basal Sclerodermatineae originated in the late Cretaceous while major genera diversified near the mid Cenozoic. Asia and North America are the most probable ancestral areas for all Sclerodermatineae, and angiosperms, primarily rosids, are the most probable ancestral hosts. Evolution in the Sclerodermatineae follows the biogeographic history of disjunct plant communities associated with early Cenozoic mesophytic forests and a boreotropical history. Broad geographic distributions are observed in the most promiscuous Sclerodermatineae (those with broad host ranges), while those with relatively limited distribution have fewer documented ectomycorrhizal associations. This suggests that ectomycorrhizal generalists have greater dispersal capabilities than specialists.

EFFECTS OF GASTEROID FRUITING BODY MORPHOLOGY ON DIVERSIFICATION RATES IN THREE INDEPENDENT CLADES OF FUNGI ESTIMATED USING BINARY STATE SPECIATION AND EXTINCTION ANALYSIS

Gasteroid fungi include puffballs, stinkhorns, and other forms that produce their spores inside the fruiting body. Gasteroid taxa comprise about 8.4% of the Agaricomycetes (mushroom‐forming fungi) and have evolved numerous times from nongasteroid ancestors, such as gilled mushrooms, polypores, and coral fungi, which produce spores on the surface of the fruiting body. Nongasteroid Agaricomycetes have a complex mechanism of forcible spore discharge that is lost in gasteroid lineages, making reversals to nongasteroid forms very unlikely. Our objective was to determine whether gasteromycetation affects the rate of diversification of lineages “trapped” in the gasteroid state. We assembled four datasets (the Sclerodermatineae, Boletales, Phallomycetidae, and Lycoperdaceae), representing unique origins of gasteroid fungi from nongasteroid ancestors and generated phylogenies using BEAST. Using the program Diversitree, we analyzed these phylogenies to estimate character‐state‐specific rates of speciation and extinction, and rates of transitions between nongasteroid and gasteroid forms. Most optimal models suggest that the net diversification rate of gasteroid forms exceeds that of nongasteroid forms, and that gasteroid forms will eventually come to predominate over nongasteroid forms in the clades in which they have arisen. The low frequency of gasteroid forms in the Agaricomycetes as a whole may reflect the recent origins of many gasteroid lineages.

Durianella, a new gasteroid genus of boletes from Malaysia

Hydnangium echinulatum, described originally from a single specimen collected in Malaysia, has been recollected, and based on morphological and molecular characters is recognized as representing a new gasteroid genus of boletes with affinities to the Boletineae, herein named Durianella. Diagnostic features include an epigeous, ovoid, pyramidal-warted, durian fruit-like basidiome with gelatinized glebal locules and a columella that turns indigo blue upon exposure, and subglobose basidiospores with long, curved, thin-walled and collapsible spines. A redescription, phylogenetic analysis and comparison with allied taxa are presented.

Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria

Summary A systematic and evolutionary ecology study of the model ectomycorrhizal (ECM) genus Laccaria was performed using herbarium material and field collections from over 30 countries covering its known geographic range. A four‐gene (nrITS, 28S, RPB2, EF1α) nucleotide sequence dataset consisting of 232 Laccaria specimens was analyzed phylogenetically. The resulting Global Laccaria dataset was used for molecular dating and estimating diversification rates in the genus. Stable isotope analysis of carbon and nitrogen was used to evaluate the origin of Laccarias ECM ecology. In all, 116 Laccaria molecular species were identified, resulting in a near 50% increase in its known diversity, including the new species described herein: Laccaria ambigua. Molecular dating indicates that the most recent common ancestor to Laccaria existed in the early Paleocene (56–66 million yr ago), probably in Australasia. At this time, Laccaria split into two lineages: one represented by the new species L. ambigua, and the other reflecting a large shift in diversification that resulted in the remainder of Laccaria. L. ambigua shows a different isotopic profile than all other Laccaria species. Isotopes and diversification results suggest that the evolution of the ECM ecology was a key innovation in the evolution of Laccaria. Diversification shifts associated with Laccarias dispersal to the northern hemisphere are attributed to adaptations to new ecological niches.

Cantharellaceae of Guyana I: new species, combinations and distribution records of Craterellus and a synopsis of known taxa

Members of the Cantharellaceae (Cantharellales, Basidiomycota) are common ectomycorrhizal associates of the leguminous genus Dicymbe in the Pakaraima Mountains of Guyana. Eight distinct species or morphospecies currently are recognized in Craterellus Pers. or Cantharellus Adans. ex Fr. from Guyanese Dicymbe-dominated forests. We evaluated the systematics of these taxa with phylogenetic analyses of DNA sequence data from the nuclear ribosomal regions of the internal transcribed spacer (ITS) and 28S large subunit (LSU). The results of these analyses along with careful assessment of morphology let us described two new species, Craterellus atratoides sp. nov. and Craterellus strigosus sp. nov., redescribe Craterellus atratus (Corner) Yomyart et al. based on new material from Guyana, and propose a new combination in Craterellus for Cantharellus pleurotoides T.W. Henkel, Aime & S.L. Mill. Macroscopic illustrations are provided for two additional cantharelloid morphospecies confirmed in Craterellus, as well as the regionally endemic Cantharellus guyanensis Mont. Macromorphological, micromorphological and habitat data are provided for C. atratoides, C. strigosus and C. atratus, and ITS and LSU sequence data are provided for each of the eight known Guyanese taxa.

Cantharellus chicagoensis sp. nov. is supported by molecular and morphological analysis as a new yellow chanterelle in midwestern United States

Recent molecular systematic studies of Cantharellus cibarius sensu lato have revealed previously unknown species in different regions of North America. This study investigates yellow chanterelles in the Midwest using phylogenetic analysis of three DNA regions: nuc rDNA internal transcribed spacer 2 (ITS2) and 28S sequences and translation elongation factor 1α gene (EF1α). This analysis reveals a locally common taxon Cantharellus chicagoensis sp. nov. as distinct from sympatric species present in northeastern Illinois, northwestern Indiana and Wisconsin. This chanterelle features a pileus that often has a greenish yellow margin when immature, a squamulose disk when mature, a yellow spore print and the absence of a fragrant odor. Multiple Cantharellus specimens group with C. flavus and C. phasmatis, expanding their known range, and others with C. roseocanus. Our observations highlight the diversity of Cantharellus in midwestern USA and further document the need for additional systematic focus on the region’s fungi.

Cantharellaceae of Guyana II: New species of Craterellus, new South American distribution records for Cantharellus guyanensis and Craterellus excelsus, and a key to the Neotropical taxa

Craterellus olivaceoluteus sp. nov. and Craterellus cinereofimbriatus sp. nov. are described as new to science. These fungi were collected from Guyana in association with ectomycorrhizal host trees in the genera Dicymbe (Fabaceae subfam. Caesalpinioideae) and Pakaraimaea (Dipterocarpaceae). Cantharellus guyanensis Mont., originally described from French Guiana, is redescribed from recent collections from Guyana, with additional range extensions for the species provided based on material examined from French Guiana, Venezuela, and north central, northeastern and southern Brazil, circumscribing nearly the entire Guiana Shield region and beyond. A new distribution record from French Guiana is provided for Craterellus excelsus T.W. Henkel & Aime. Macromorphological, micromorphological and habitat data are provided for the new species and C. guyanensis as well as DNA sequence data from the nuclear ribosomal regions of the internal transcribed spacer (ITS) and 28S large subunit (LSU); additional sequence data is provided for C. guyanensis and C. excelsus specimens collected outside Guyana. The relationships of these taxa within the Cantharellaceae were evaluated with phylogenetic analyses of ITS and LSU sequence data. This work brings the total number of Cantharellaceae species known from Guyana to eight. A key to the Cantharellus and Craterellus species known from the lowland Neotropics and extralimital montane Central and South America is provided.

Examining the efficacy of a genotyping-by-sequencing technique for population genetic analysis of the mushroom Laccaria bicolor and evaluating whether a reference genome is necessary to assess homology

Given the diversity and ecological importance of Fungi, there is a lack of population genetic research on these organisms. The reason for this can be explained in part by their cryptic nature and difficulty in identifying genets. In addition the difficulty (relative to plants and animals) in developing molecular markers for fungal population genetics contributes to the lack of research in this area. This study examines the ability of restriction-site associated DNA (RAD) sequencing to generate SNPs in Laccaria bicolor. Eighteen samples of morphologically identified L. bicolor from the United States and Europe were selected for this project. The RAD sequencing method produced anywhere from 290 000 to more than 3 000 000 reads. Mapping these reads to the genome of L. bicolor resulted in 84 000–940 000 unique reads from individual samples. Results indicate that incorporation of non-L. bicolor taxa into the analysis resulted in a precipitous drop in shared loci among samples, suggests the potential of these methods to identify cryptic species. F-statistics were easily calculated, although an observable “noise” was detected when using the “All Loci” treatment versus filtering loci to those present in at least 50% of the individuals. The data were analyzed with tests of Hardy-Weinburg equilibrium, population genetic statistics (FIS and FST), and population structure analysis using the program Structure. The results provide encouraging feedback regarding the potential utility of these methods and their data for population genetic analysis. We were unable to draw conclusions of life history of L. bicolor populations from this dataset, given the small sample size. The results of this study indicate the potential of these methods to address population genetics and general life history questions in the Agaricales. Further research is necessary to explore the specific application of these methods in the Agaricales or other fungal groups.

Biogeography of the Ectomycorrhizal Mushroom Genus Laccaria

The mushroom genus Laccaria is one of the very few ectomycorrhizal lineages whose diversity has been explored from the phylogenetic, population genetic, genomic, and ecological perspectives. The genus serves as a model for understanding the biology of ectomycorrhizal fungi. This chapter provides an in-depth overview of the systematic diversity, ecology, host associations, and phylogenetic relationships that helped shape the current distribution of Laccaria species. This chapter discusses the challenges in identifying and delimiting species of Laccaria, along with the potential influence of life-history strategy and ecological role on the speciation and dispersal of Laccaria. The biogeographic histories of several well-documented and important ectomycorrhizal hosts of Laccaria are reviewed. These histories provide a backdrop to examine potential migration and dispersal routes during the diversification of Laccaria. They reveal historical distribution patterns that explain how ectomycorrhizal symbioses likely shaped the biogeography of Laccaria. The phylogenetic history and global systematic diversity of Laccaria is reviewed in the final sections, which include discussions of the Southern Hemisphere origins of the genus, a hypothesis for dispersal to the Northern Hemisphere, and the challenges of correlating diversity and distribution patterns in the Northern Hemisphere. Altogether, Laccaria represents a genus that is rich with opportunities to explore the ecological and evolutionary forces shaping the biogeography of ectomycorrhizal fungi.