The Ascomycota Tree of Life: A Phylum-wide Phylogeny Clarifies the Origin and Evolution of Fundamental Reproductive and Ecological Traits

Abstract

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.

Journey from the West: Did tropical Graphidaceae (lichenized Ascomycota: Ostropales) evolve from a saxicolous ancestor along the American Pacific coast?

“…Rivas Plata et al, unpublished manuscript ). This hypothesis is consistent with the fi nding that in several cases, saxicolous lichens or even nonlichenized rock fungi are basal or sister to the main lichenized lineages ( Miadlikowska et al, 2006 ;Hofstetter et al, 2007 ;Gueidan et al, 2008 ;Schoch et al, 2009 ). In many lichenized lineages, however, the immediate sister group is not known, which makes assumptions about their early evolution speculative.…”

“…GUIDANCE uses a MAFFT alignment and returns a colored MSA that allows to nonlichenized fungal lineages ( Tehler et al, 2003 ;Eriksson, 2005 ). However, for extant lichenized lineages such as Arthoniomycetes, Lecanoromycetes, Lichinomycetes, Eremithallales, Trypetheliales, and Verrucariales in Ascomycota and Dictyonema , Lepidostroma , Lichenomphalia , Marchandomphalina , and Multiclavula in Basidiomycota, evidence points to a more recent, multiple origin of these from nonlichenized ancestors between 300 and 200 Ma ( Gargas et al, 1995 ;Lawrey et al, 2009 ;Nelsen et al, 2009Nelsen et al, , 2011Schoch et al, 2009 ). In the absence of a good fossil record, molecular clock dating studies indicate that most lichenized lineages, at least in the Ascomycota, evolved in the relatively dry, warm Triassic, during which extended terrestrial forest vegetation was sparsely developed ( Amo de Paz et al, 2011 ;E.…”

Extended phylogeny and a revised generic classification of thePannariaceae(Peltigerales, Ascomycota)

“…Peltigerales is one out of nine named orders in the most species-rich class among the ascomycetes, the Lecanoromycetes (Schoch et al 2009), and incorporates the majority of lichen-forming fungi with cyanobacteria as their photosynthesizing symbiotic partner. The Peltigeralean lichens play an important role in the terrestrial nitrogen cycle of many ecosystems through the fixation of atmospheric nitrogen (Cleveland et al 1999;Belnap 2003).…”

Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi

“…For Ascomycota (including mold genera such as Aspergillus), they are generally superior to rRNA genes for resolving relationships at various taxonomic levels (29). Specialized identification databases use several markers [e.g., translation elongation factor 1-α for Fusarium (30) and β-tubulin for Penicillium (31)], but there is little standardization.…”