Demographic history and genomics of local adaptation in blue tit populations

Abstract

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 variation of populations’ demography and variation in recombination rate and diversity along the genome. Here, we investigated these parameters in blue tit populations inhabiting neighbouring deciduous and evergreen forests and populations in an insular versus a continental context. Close populations from deciduous and evergreen habitats were weakly genetically differentiated (FST = 0.004 on average), nevertheless with a significant effect of habitat type on the overall genetic structure. This low differentiation was consistent with the large effective population sizes (from 43,000 to 463,000) and the strong and long-lasting gene flow inferred by demographic modeling. In turn, insular and continental populations were moderately differentiated (FST = 0.08 on average), which was consistent with the inference of moderate ancestral migrations followed by isolation since the end of the last glaciation. Weak and non-parallel footprints of divergent selection among deciduous and evergreen populations were consistent with their demography and the probable polygenic nature of local adaptation in these habitats. This contrasted with stronger outlier regions, more often in regions of low recombination, found between insular and continental populations. Lastly, we identified a genomic inversion on the continent, spanning 2.8Mb. These results provide insights into the demographic history and genetic architecture of local adaptation in blue tit populations at multiple geographic scales.