Structural variants underlie parallel adaptation following global invasion

Abstract

Rapid adaptation during invasion has historically been considered limited and unpredictable. We leverage whole-genome sequencing of >2600 plants across six continents to investigate the relative roles of colonization history and adaptation during the worldwide invasion of Trifolium repens. Introduced populations contain high levels of genetic variation with independent colonization histories evident on different continents. Five large structural variants on three chromosomes exist as standing genetic variation within the native range, and exhibit strong signatures of parallel climate-associated adaptation across continents. Common gardens in the native and introduced ranges demonstrate that three structural variants exhibit patterns of selection consistent with local adaptation across each range. Our results provide strong evidence that rapid and parallel adaptation during invasion is caused by large-effect structural variants introduced throughout the world. Significance StatementBiological invasions occur over short timescales and introductions are often hypothesized to include limited genetic diversity, making the role of adaptation in invasion success controversial. We demonstrate that the invasion of a human-commensal species, Trifolium repens, likely stems from multiple, diverse introductions with significant evidence of climate-associated adaptation following introduction. The genetic basis of adaptation is most strongly linked to five chromosomal rearrangements that each span hundreds of genes - matching theoretical predictions that large-effect variants are key to the initial stages of adaptation to novel environments. Chromosomal rearrangements have remarkably parallel signatures of adaptation across different introductions despite initial colonization from different areas of Europe. Our study highlights the impact of globalization and rapid adaptation for the invasion success of human commensal species.