The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits.

We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.

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.

A multigene phylogeny of the Dothideomycetes using four nuclear loci.

We present an expanded multigene phylogeny of the Dothideomycetes. The final data matrix consisted of four loci (nuc SSU rDNA, nuc LSU rDNA, TEF1, RPB2) for 96 taxa, representing five of the seven orders in the current classification of Dothideomycetes and several outgroup taxa representative of the major clades in the Pezizomycotina. The resulting phylogeny differentiated two main dothideomycete lineages comprising the pseudoparaphysate Pleosporales and aparaphysate Dothideales. We propose the subclasses Pleosporomycetidae (order Pleosporales) and Dothideomycetidae (orders Dothideales, Capnodiales and Myriangiales). Furthermore we provide strong molecular support for the placement of Mycosphaerellaceae and Piedraiaceae within the Capnodiales and introduce Davidiellaceae as a new family to accommodate species of Davidiella with Cladosporium anamorphs. Some taxa could not be placed with certainty (e.g. Hysteriales), but there was strong support for new groupings. The clade containing members of the genera Botryosphaeria and Guignardia resolved well but without support for any relationship to any other described orders and we hereby propose the new order Botryosphaeriales. These data also are consistent with the removal of Chaetothyriales and Coryneliales from the Dothideomycetes and strongly support their placement in the Eurotiomycetes.