Nagy, L. | bioRxiv Science

bioRxiv2017

Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

Complex multicellularity comprises the most advanced level of organization evolved on Earth. It has evolved only a few times in metazoans, green plants, brown and red algae and fungi. Compared to other lineages, the evolution of multicellularity in fungi follows different principles; both simple and complex multicellularity evolved via unique mechanisms not seen in other lineages. In this article we review ecological, paleontological, developmental and genomic aspects of complex multicellularity in fungi and discuss the general principles of the evolution of complex multicellularity in light of its fungal manifestations. Fungi represent the only lineage in which complex multicellularity shows signatures of convergent evolution: it appears 8-12 distinct fungal lineages, which show a patchy phylogenetic distribution, yet share some of the genetic mechanisms underlying complex multicellular development. To mechanistically explain the patchy distribution of complex multicellularity across the fungal tree of life we identify four key observations that need to be considered: the large number of apparently independent complex multicellular clades; the lack of documented phenotypic homology between these; the universal conservation of gene circuits regulating the onset of complex multicellular development; and the existence of clades in which the evolution of complex multicellularity is coupled with limited gene family diversification. We discuss how these patterns and known genetic aspects of fungal development can be reconciled with the genetic theory of convergent evolution to explain its pervasive occurrence in across the fungal tree of life.

evolutionary biology↗

bioRxiv2017

Multiple hidden processes complicate phylogenomic inference of deep Basidiomycota relationships

Resolving deep divergences in the fungal tree of life remains a challenging task even for analyses of genome-scale phylogenetic datasets. Relationships between Basidiomycota subphyla, the rusts (Pucciniomycotina), smuts (Ustilaginomycotina) and mushroom forming fungi (Agaricomycotina) represent a particularly challenging situation that posed problems to both traditional multigene and genome-scale phylogenetic studies. Here, we address basal Basidiomycota relationships using three different phylogenomic datasets, concatenated and gene tree-based analyses and examine the contribution of several potential sources of uncertainty, including fast-evolving sites, putative long-branch taxa, model violation and missing data. We inferred conflicting results with different datasets and under different models. 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 Astral analyses. The most conserved datasets grouped rusts with mushroom forming fungi, although this relationship proved labile, sensitive to model choice, different data subsets and missing data. Excluding putative long branch taxa, genes with the highest proportions of missing data and/or genes with strong signal failed to reveal a consistent trend toward one or the other topology, suggesting that additional sources of conflict are at play too. 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. While concatenated analyses yielded strong but conflicting support, individual gene trees mostly provided poor support for rusts, smuts and mushroom-forming fungi, suggesting that the true Basidiomycota tree might be in a part of the tree space that is difficult to access using both concatenation and gene tree based approaches. Thus, basal Basidiomycota relationships remain unresolved and might represent a phylogenetic problem that remains contentious even in the genomic era.

evolutionary biology↗