Microbial diversity emerges from evolutionary processes shaping genomic and phenotypic traits. Here, we use the yeast Yarrowia lipolytica to examine these dynamics across diverse environments and demonstrate how population-level data can inform targeted bioprospecting for industrial traits. Whole-genome and phenotypic analyses of 126 isolates reveal a complex population structure shaped by ecological specialization and gene flow. Some lineages show ecological filtering, reduced genetic diversity, and distinct gene content, reflecting specialization to substrates such as dairy or hydrocarbons, while others maintain higher genetic diversity and broader phenotypic capacity, including stress tolerance and metabolic flexibility. Trait assays link phenotypic variation to underlying genetic differences. For example, improved growth on acetate is linked to regulatory variation in hydrocarbon-adapted strains. Together, our results indicate that Y. lipolytica diversity reflects a gradient of ecological specialization and gene flow, highlighting how varying evolutionary trajectories shape ecological success and can be leveraged for microbial bioprospecting

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