The Macroevolution of Filamentation Morphology Across the Saccharomycotina Yeast Subphylum

Saccharomycotina yeasts are a highly diverse and widely distributed subphylum of ascomycete fungi that exhibit diversity in their asexual growth morphologies; the human commensal yeast Candida albicans exhibits both unicellular and filamentous growth, whereas the baker’s yeast Saccharomyces cerevisiae grows unicellularly by budding. Filamentous growth (and the production of hyphae) can comprise linear and branched budding cells that do not undergo cell separation, termed pseudohyphae, or of tubular filaments with septa that perforate allowing movement of organelles, termed true hyphae. We integrated phenotypic, genomic, metabolic, and isolation environment data from 1,154 strains from 1,051 Saccharomycotina species to examine the variation and evolutionary history of filamentation across Saccharomycotina and determine the extent to which genes, metabolic traits, and environments can predict filamentation types. We found that 63.37% of strains can form filaments; 6.56% can form true hyphae, 42.40% can form pseudohyphae, and 14.39% can form both true hyphae and pseudohyphae. We found that the distributions of species that can produce true hyphae or that can filament were more strongly correlated with the yeast phylogeny than the distribution of species with pseudohyphae. Ancestral state reconstruction suggested that the ability to form true hyphae and/or pseudohyphae evolved several times in yeast evolution. We infer that most yeast ancestors likely produced pseudohyphae or lacked filaments, while the Saccharomycotina last common ancestor likely produced pseudohyphae but not true hyphae. Machine learning models trained on genomic and metabolic features predicted filament morphologies with about 70% accuracy. Connecting the evolution of Saccharomycotina morphologies to their genomic, metabolic, and ecological characteristics will enrich our understanding of the evolution of the diversity of lifestyles observed in this lineage.