Island populations diverge from the mainland and from each other by both natural selection and neutral forces such as founder effects and genetic drift. In this work we aim to determine the relative roles of selection and drift in the diversification of chaffinches (Fringilla spp.) in Macaronesia. We tested the hypothesis that taxa inhabiting Macaronesian archipelagos, which exhibit significant differences in habitat and climate compared to the mainland, should experience distinct ecological pressures, leading to divergence at loci under selection related to environmental variables. To determine the role of local adaptation in the differentiation of these taxa, we performed genotype-environment association (GEA) analyses using ten environmental variables and 52,306 single-nucleotide polymorphism markers obtained from genotyping-by-sequencing (GBS) in 79 chaffinches. Redundancy analysis (RDA) revealed that genomic variation is associated with environmental variables, and identified candidate genes related to phenotypic traits and environmental variables. Variables associated with habitat type and precipitation, together with drift, played an important role in the genomic differentiation between chaffinches from Macaronesia and the mainland, as well as within the Canarian archipelago. Genetic drift was identified as the main factor in the differentiation of North African chaffinches from Macaronesia and mainland Europe, as well as Madeira chaffinches from those in the Canary Islands. Finally, chaffinches from the Canary Islands show an incipient diversification process at the genetic and phenotypic level driven by both selection and neutral processes. Our results suggest that both habitat-driven local adaptation and drift have played a role in the radiation of chaffinch taxa in Macaronesia.

Understanding the factors driving phenotypic and genomic differentiation of insular populations is of major interest to gain insight into the speciation process. Comparing patterns across different insular taxa subjected to similar selective pressures upon colonizing oceanic islands provides the opportunity to study parallel evolution and identify shared patterns in their genomic landscapes of differentiation. We selected four species of passerine birds (common chaffinch Fringilla coelebs/canariensis, red-billed chough Pyrrhocorax pyrrhocorax, house finch Haemorhous mexicanus and dark-eyed/island junco Junco hyemalis/insularis) that have both mainland and insular populations. For each species, we sequenced whole genomes from mainland and insular individuals to infer their demographic history, characterize their genomic differentiation, and identify the factors shaping them. We estimated the relative (FST) and absolute (dxy) differentiation, nucleotide diversity (π), Tajima’s D, gene density and recombination rate. We also searched for selective sweeps and chromosomal inversions along the genome. Changes in body size between island and mainland were consistent with the island rule. All species shared a marked reduction in effective population size (Ne) upon island colonization. We found highly differentiated genomic regions in all four species, suggesting the role of selection in island-mainland differentiation, yet the lack of congruence in the location of these regions indicates that each species adapted to insular environments differently. Our results suggest that the genomic mechanisms involved, which include selective sweeps, chromosomal inversions, and historical factors like recurrent selection, differ in each species despite the highly conserved structure of avian genomes and the similar selective factors involved.