Evolution at two time frames: polymorphisms from an ancient singular divergence event fuel contemporary parallel evolution

When species occur in repeated ecologically distinct habitats across their range, adaptation may proceed surprisingly fast and result in parallel evolution. There is increasing evidence that such cases of rapid parallel evolution are fueled by standing genetic variation, but the origin of this genetic variation remains poorly understood. In Pogonus chalceus beetles, short- and long-winged ecotypes have diverged in response to contrasting hydrological regimes and can be repeatedly found along the Atlantic European coast. By analyzing genomic variation across the beetles distribution, we reveal that genomically widespread short-wing selected alleles evolved during a singular divergence event, estimated at ~0.19 Mya. The ancient and differentially selected alleles are currently polymorphic in all populations across the range, allowing for the fast evolution of one ecotype from a small number of random individuals, as low as 5 to 15, of the populations of the other ecotype. Our results suggest that cases of fast parallel ecological divergence might be the result of evolution at two different time frames: divergence in the past, followed by repeated selection on the divergently evolved alleles after admixture. We suggest that this mechanism may be common and potentially further driven by periods of geographic isolation imposed by large-scale environmental changes such as glacial cycles.