Genotypic and Phenotypic Diversity of Maudiozyma humilis: The Multiple Evolutionary Trajectories of a Domesticated Yeast.

Maudiozyma humilis is the second most frequently encountered yeast species in sourdough bread. Despite its ecological and food relevance, little is known about its evolutionary trajectories and phenotype traits of interest. Here we investigated the genomic and phenotypic diversity of a worldwide collection of 55 M. humilis strains by combining genomic analyses and high-throughput phenotyping of fermentation kinetics and fitness. Population genomic analysis revealed six distinct clades, three diploid and three triploid, with no geographical or substrate-specific structuring. Phylogenetic, loss of heterozygosity (LOH), and allele specific analyses indicated that triploid strains originated from both recent and more ancient hybridization events involving multiple lineages. The absence of the HO gene and mating-type silent cassettes revealed the inability of M. humilis to carry mating-type switching. In addition, high linkage disequilibrium and variable LOH accumulation were observed consistent with a predominantly clonal reproduction. Last, an exceptionally high level of heterozygosity was detected, suggesting that occasional hybridization is the major driver of genetic diversity. Phenotypic characterization in a synthetic sourdough medium revealed variation in fermentation kinetics and fitness statistically associated with the genetic clades. Interestingly, genetic distance between clades and strains better explains the phenotypic variation than difference in ploidy. Altogether, our findings highlight the complex evolutionary history of M. humilis, shaped by hybridization and ploidy variation, and reveal that historical contingency shapes the phenotypic landscape of this species. Beyond providing the first analysis of M. humilis evolution, our result challenges the hypothesis that increases in ploidy are necessarily beneficial in domesticated species.