Abstract
Uncovering the genetic basis of species diversification is a central goal in evolutionary biology. Yet, the link between the accumulation of genomic changes during population divergence and the evolutionary forces promoting reproductive isolation is poorly understood. Here, we analysed 124 genomes of crow populations with various degrees of genome-wide differentiation, with parallelism of a sexually selected plumage phenotype, and ongoing hybridization. Overall, heterogeneity in genetic differentiation along the genome was best explained by linked selection exposed on a shared genome architecture. Superimposed on this common background, we identified genomic regions with signatures of selection specific to independent phenotypic contact zones. Candidate pigmentation genes with evidence for divergent selection were only partly shared, suggesting context-dependent selection on a multigenic trait architecture and parallelism by pathway rather than by repeated single-gene effects. This study provides insight into how various forms of selection shape genome-wide patterns of genomic differentiation as populations diverge.
Highlights
Uncovering the genetic basis of species diversification is a central goal in evolutionary biology
The isolation of few loci specific to each contact zone contrasts with studies implicating a high number of prominent outlier regions hosting candidates under divergent selection associated with the contrast in question[37,38]
Selection on traits encoded by many genes, should in principle not be detectable in genome scans, which are effectively blind to selection on small-effect polygenes, or when epistasis is involved[39]
Summary
Uncovering the genetic basis of species diversification is a central goal in evolutionary biology. Heterogeneity in genetic differentiation along the genome was best explained by linked selection exposed on a shared genome architecture Superimposed on this common background, we identified genomic regions with signatures of selection specific to independent phenotypic contact zones. Exploiting variation in population connectivity ranging from allopatry to ongoing gene flow across multiple contact zones, in combination with the contrast in phenotype, allowed us to characterize the evolutionary processes underlying genomic differentiation during incipient speciation. Genomic regions of elevated differentiation were best explained by selection pressures common to all populations Superimposed on this background, divergent selection against gene flow was specific to each contact zone and linked to phenotype by metabolic pathway rather than by repeated selection on individual genes
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