Model Choice, Missing Data, and Taxon Sampling Impact Phylogenomic Inference of Deep Basidiomycota Relationships

Abstract

Resolving deep divergences in the tree of life is challenging even for analyses of genome-scale phylogenetic data sets. Relationships between Basidiomycota subphyla, the rusts and allies (Pucciniomycotina), smuts and allies (Ustilaginomycotina), and mushroom-forming fungi and allies (Agaricomycotina) were found particularly recalcitrant both to traditional multigene and genome-scale phylogenetics. Here, we address basal Basidiomycota relationships using concatenated and gene tree-based analyses of various phylogenomic data sets to examine the contribution of several potential sources of bias. We evaluate the contribution of biological causes (hard polytomy, incomplete lineage sorting) versus unmodeled evolutionary processes and factors that exacerbate their effects (e.g., fast-evolving sites and long-branch taxa) to inferences of basal Basidiomycota relationships. Bayesian Markov Chain Monte Carlo and likelihood mapping analyses reject the hard polytomy with confidence. In concatenated analyses, fast-evolving sites and oversimplified models of amino acid substitution favored the grouping of smuts with mushroom-forming fungi, often leading to maximal bootstrap support in both concatenation and coalescent analyses. On the contrary, the most conserved data subsets grouped rusts and allies with mushroom-forming fungi, although this relationship proved labile, sensitive to model choice, to different data subsets and to missing data. Excluding putative long-branch taxa, genes with high proportions of missing data and/or with strong signal failed to reveal a consistent trend toward one or the other topology, suggesting that additional sources of conflict are at play. While concatenated analyses yielded strong but conflicting support, individual gene trees mostly provided poor support for any resolution of rusts, smuts, and mushroom-forming fungi, suggesting that the true Basidiomycota tree might be in a part of tree space that is difficult to access using both concatenation and gene tree-based approaches. Inference-based assessments of absolute model fit strongly reject best-fit models for the vast majority of genes, indicating a poor fit of even the most commonly used models. While this is consistent with previous assessments of site-homogenous models of amino acid evolution, this does not appear to be the sole source of confounding signal. Our analyses suggest that topologies uniting smuts with mushroom-forming fungi can arise as a result of inappropriate modeling of amino acid sites that might be prone to systematic bias. We speculate that improved models of sequence evolution could shed more light on basal splits in the Basidiomycota, which, for now, remain unresolved despite the use of whole genome data.

Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi

“…Using the pipeline PifCoSm (Pipeline for Construction of Supermatrices, available through https://github.com/RybergGroup/ PifCoSm), we created an alignment of 8,472 nuclear ribosomal large subunit (nLSU) sequences, 1,872 nuclear ribosomal small subunit (nSSU) sequences, 784 largest subunit of RNA polymerase II (rpb1) sequences, 1,683 second-largest subunit of RNA polymerase II (rpb2) sequences, and 856 translation elongation factor 1-alpha (tef-1-α) sequences (SI Appendix, Table S1). The resulting phylogeny recovered the 21 monophyletic orders accepted in the Agaricomycetes, with a topology that is in general agreement with previous phylogenies (18)(19)(20). The Russulales was placed as a sister group of a large clade containing the Polyporales, Thelephorales, Gloeophyllales, Jaapiales, and Agaricomycetidae, as shown in previous studies (19,20), although in other studies, it has also been recovered as sister to Jaapiales and Gloeophyllales (17).…”

Fungal evolution: diversity, taxonomy and phylogeny of the Fungi

“…Most phylogenies recover Ustilaginomycotina as sister to Agaricomycotina, with Pucciniomycotina as the earliest diverging branch. This relationship remains debated as it seems to be greatly influenced by methodological biases (Prasanna et al ., ). Wallemiomycotina is a recently recognized subphylum that includes a few genera ( Wallemia , Basidioascus , Geminibasidium ) of thermoresistant and xerotolerant moulds or yeast‐like fungi (Zalar et al ., ; Padamsee et al ., ; Zajc et al ., ; Nasr et al ., ).…”

A genome-scale phylogeny of Fungi; insights into early evolution, radiations, and the relationship between taxonomy and phylogeny

“…Agaricomycotina + Wallemiomycotina has proven challenging 37,39,55,56 . We too found discordant topologies between concatenation-and coalescent-based analyses (Fig.…”