Evolutionary history of a dispersal-associated locus across sympatric and allopatric divergent populations of a wing-polymorphic beetle across Atlantic Europe.

Studying the evolutionary history of trait divergence, in particular those related to dispersal capacity, is of major interest for the process of local adaptation and metapopulation dynamics. Here, we reconstruct the evolution of different alleles at the nuclear-encoded mitochondrial NADP(+)-dependent isocitrate dehydrogenase (mtIdh) locus of the ground beetle Pogonus chalceus that are differentially and repeatedly selected in short- and long-winged populations in response to different hydrological regimes at both allopatric and sympatric scales along the Atlantic European coasts. We sequenced 2788 bp of the mtIdh locus spanning a ~7-kb genome region and compared its variation with that of two supposedly neutral genes. mtIdh sequences show (i) monophyletic clustering of the short-winged associated mtIDH-DE haplotypes within the long-winged associated mtIDH-AB haplotypes, (ii) a more than tenfold lower haplotype diversity associated with the mtIDH-DE alleles compared to the mtIDH-AB alleles and (iii) a high number of fixed nucleotide differences between both mtIDH haplotype clusters. Coalescent simulations suggest that this observed sequence variation in the mtIdh locus is most consistent with a singular origin in a partially isolated subpopulation, followed by a relatively recent spread of the mtIDH-DE allele in short-winged populations along the Atlantic coast. These results demonstrate that even traits associated with decreased dispersal capacity can rapidly spread and that reuse of adaptive alleles plays an important role in the adaptive potential within this sympatric mosaic of P. chalceus populations.