Climate-induced range shifts drive adaptive response via spatio-temporal sorting of alleles

Quaternary climate fluctuations drove many species to shift their geographic ranges, in turn shaping their genetic structures. Recently, it has been argued that adaptation may have accompanied species range shifts via the “sieving” of genotypes during colonisation and establishment. However, this has not been directly demonstrated, and knowledge remains limited on how different evolutionary forces, that are typically investigated separately, interacted to jointly mediate species responses to past climatic change. Here, through whole-genome resequencing of over 1200 individuals of the carnation Dianthus sylvestris coupled with integrated population genomic and gene-environment models, we reconstruct the past neutral and adaptive landscape of this species as it was shaped by the Quaternary glacial cycles. We show that adaptive responses emerged concomitantly with the post-glacial range shifts and expansions of this species in the last 20 thousand years. This was due to the spatial sorting of adaptive alleles through time, as populations expanded out of restrictive glacial refugia into the broader and more heterogeneous range of habitats available in the present-day inter-glacial. Our results reveal a tightly-linked interplay of migration and adaptation under past climate-induced range shifts that has acted to shape the spatial patterns of adaptive genetic variation we see in the species today.