Glaciation history and geographic barriers shape genetic diversity of Lewis flax across North America

Factors shaping genetic variation at the continental scale include geographic barriers, glacial cycles, and genetic constraints like mating system. We examine how such factors combine to influence diversification in Linum lewisii (Lewis flax), a perennial forb native to North America. We used whole genome sequencing, spatial analyses, and demographic inference to quantify population diversity across space and time and to test expectations about mating system evolution during range expansion. We found that Lewis flax consists of four genetic clusters that diverged during the Last Glacial Period, with the Rocky Mountains acting as a dispersal barrier. These clusters aren’t reflected in current taxonomy. Genomic data also suggest Lewis flax is predominantly outcrossing, despite its self-compatibility. Although it is thought to have colonized North America via Beringia, we found no evidence of northern refugia. Current northern populations apparently derive from a post-glacial range expansion, and their genomic signatures may indicate a shift towards increased selfing. The mixed mating system of Lewis flax thus interacts with glacial history and geographical barriers in a way that differs from obligate outcrossing or selfing species. This study furthermore provides foundational knowledge for its use in ecological restoration and ongoing neodomestication as a perennial oilseed food crop.