Demographic history and genomics of local adaptation in blue tit populations

Understanding the genomic processes underlying local adaptation is a central aim of modern evolutionary biology. This task requires identifying footprints of local selection but also estimating spatio-temporal variations in population demography and variations in recombination rate and in diversity along the genome. Here, we investigated these parameters in blue tit populations inhabiting deciduousversusevergreen forests, and insularversusmainland areas, in the context of a previously described strong phenotypic differentiation. Neighboring population pairs of deciduous and evergreen habitats were weakly genetically differentiated (F-ST = 0.003 on average), nevertheless with a statistically significant effect of habitat type on the overall genetic structure. This low differentiation was consistent with the strong and long-lasting gene flow between populations inferred by demographic modeling. In turn, insular and mainland populations were moderately differentiated (F-ST = 0.08 on average), in line with the inference of moderate ancestral migration, followed by isolation since the end of the last glaciation. Effective population sizes were large, yet smaller on the island than on the mainland. Weak and nonparallel footprints of divergent selection between deciduous and evergreen populations were consistent with their high connectivity and the probable polygenic nature of local adaptation in these habitats. In turn, stronger footprints of divergent selection were identified between long isolated insular versus mainland birds and were more often found in regions of low recombination, as expected from theory. Lastly, we identified a genomic inversion on the mainland, spanning 2.8 Mb. These results provide insights into the demographic history and genetic architecture of local adaptation in blue tit populations at multiple geographic scales.