Progressive spread of chromosomal inversions blends the role of colonization and evolution in a parallel Galapagos beetle radiation

Archipelago island fauna include some of the most compelling examples of parallel adaptation to ecological gradients. However, despite the insuslar nature of these systems, the possibility that repeated instances of within-island divergence resulted from independent (in situ) evolutionary rather than repeated colonization events remains most often unclear. Here, we investigated the genomic underpinning of a progressive adaptive radiation of caterpillar-hunter beetles (Calosoma) in the low- and highland habitats from the Galapagos. These Calosoma beetles have evolved only partially reduced wings in the highland of the youngest islands but evolved to distinct short-winged species in the highland of the oldest islands. In support of independent evolutionary events, the extent of genome-wide divergence between long-winged lowland and short-winged highland populations decreased towards younger islands. However, in support of repeated colonization events, adaptation to highland habitats was driven by repeated selection of alleles that are shared across all highland species and populations. These alleles comprised extensive chromosomal inversions whose origin was traced back to an initial high-lowland divergence event on the oldest island. Moreover, we found evidence that after this initial divergence event, highland alleles spread to younger islands through dispersal of highland individuals as well as dispersal of lowland individuals that were polymorphic at adaptive loci, both providing the opportunity for the establishment of highland populations on the younger islands. These findings highlight the importance of an old divergence in driving repeated adaptation to ecological gradients. Complex histories of colonization and introgression may thus result in a mixed contribution of inter-island dispersal and within-island evolution in shaping parallel species communities on islands.