Rapid phenotypic changes in traits of adaptive significance are crucial for organisms to thrive in changing environments. How such phenotypic variation is achieved rapidly, despite limited genetic variation in species that experience a genetic bottleneck is unknown.Capsella rubella, an annual and inbreeding forb (Brassicaceae), is a great system for studying this basic question. Its distribution is wider than those of its congeneric species, despite an extreme genetic bottleneck event that severely diminished its genetic variation. Here, we demonstrate that transposable elements (TEs) are an important source of genetic variation that could account for its high phenotypic diversity. TEs are (i) highly enriched inC. rubellacompared with its outcrossing sister speciesCapsella grandiflora, and (ii) 4.2% of polymorphic TEs inC. rubellaare associated with variation in the expression levels of their adjacent genes. Furthermore, we show that frequent TE insertions atFLOWERING LOCUS C (FLC)in natural populations ofC. rubellacould explain 12.5% of the natural variation in flowering time, a key life history trait correlated with fitness and adaptation. In particular, we show that a recent TE insertion at the 3′ UTR ofFLCaffects mRNA stability, which results in reducing its steady-state expression levels, to promote the onset of flowering. Our results highlight that TE insertions can drive rapid phenotypic variation, which could potentially help with adaptation to changing environments in a species with limited standing genetic variation.

Flowering time is an adaptive life history trait. , a close relative of and a young species, displays extensive variation for flowering time but low standing genetic variation due to an extreme bottleneck event, providing an excellent opportunity to understand how phenotypic diversity can occur with a limited initial gene pool. Here, we demonstrate that common allelic variation and parallel evolution at the locus confer variation in flowering time in We show that two overlapping deletions in the 5' untranslated region (UTR) of , which are associated with local changes in chromatin conformation and histone modifications, reduce its expression levels and promote flowering. We further show that these two pervasive variants originated independently in natural populations after speciation and spread to an intermediate frequency, suggesting a role of this parallel -regulatory change in adaptive evolution. Our results provide an example of how parallel mutations in the same 5' UTR region can shape phenotypic evolution in plants.