Population genomics reveals gene flow and positive selection patterns in the wine-related yeast Hanseniaspora uvarum

Hanseniaspora uvarum is a representative non-Saccharomyces species that plays a significant role in fermentation processes such as winemaking. In recent years, this species has gained attention in food engineering and evolutionary biology. However, the population genomic signatures in this species remain poorly understood. In this study, a population genomics analysis was conducted on 151 H. uvarum strains (45 from Ningxia, China; 21 from other regions of China; 67 from Australia; and 18 from other regions or of unspecified origin), and a pangenome analysis was performed on 159 strains, incorporating eight additional genome assemblies. Phylogenetic analysis, ancestry coefficient analysis, and principal component analysis generally distinguished Chinese strains from those sampled on other continents. However, substantial post-divergence gene flow and introgression were inferred between intercontinentally paired clades. Positively selected candidate genes exhibited region-specific patterns: GO terms related to the positive regulation of filamentous growth in response to external stimuli were significantly enriched in the Ningxia strains; the stress-related GO term "cytoplasmic stress granule" was significantly enriched in both the Ningxia and Australian strains, but with distinct sets of associated genes. Although the samples were primarily isolated from anthropogenic environments, H. uvarum exhibited an open pangenome, indicating substantial adaptive potential to diverse stresses. This study advances our understanding of the evolutionary dynamics of H. uvarum and establishes a genomic foundation for future ecological and industrial research on this yeast.