Unique trajectory of gene family evolution from genomic analysis of nearly all known species in an ancient yeast lineage

Abstract

Gene gains and losses are a major driver of genome evolution; their precise characterization can provide insights into the origin and diversification of major lineages. Here, we examined gene family evolution of 1,154 genomes from nearly all known species in the medically and technologically important yeast subphylum Saccharomycotina. We found that yeast gene family and genome evolution are distinct from plants, animals, and filamentous ascomycetes and are characterized by small genome sizes and smaller gene numbers but larger gene family sizes. Faster-evolving lineages (FELs) in yeasts experienced significantly higher rates of gene losses—commensurate with a narrowing of metabolic niche breadth—but higher speciation rates than their slower-evolving sister lineages (SELs). Gene families most often lost are those involved in mRNA splicing, carbohydrate metabolism, and cell division and are likely associated with intron loss, metabolic breadth, and non-canonical cell cycle processes. Our results highlight the significant role of gene family contractions in the evolution of yeast metabolism, genome function, and speciation, and suggest that gene family evolutionary trajectories have differed markedly across major eukaryotic lineages.

Convergent expansions of keystone gene families drive metabolic innovation in a major eukaryotic clade

“…Additional information, as well as all genomes, alignments, and phylogenies can be found at the original publication 21 . OrthoFinder 41 v3.0 was run under default parameters on the 1,154 genomes, resulting in 72,381 gene families 18 which were then filtered to 14,710 to include only gene families with at least 10 species represented. Following Opulente et al 2024 21 , gene models were annotated with KEGG orthologs 42 using KofamScan 43 .…”

“…Gene family evolutionary events such as gene duplication, gene loss, and horizontal gene transfer are often invoked in trait evolution and innovation 17 , 18 . However, support for causal relationships is often weak, as evolutionary innovations often evolve only once 19 , leaving no degrees of freedom to statistically test gene family – trait evolution associations 20 .…”