Identification of candidate genes for trait variation in diverging lineages and characterization of mechanistic underpinnings of genome differentiation are key steps towards understanding the processes underlying the formation of new species. Hybrid zones provide a valuable resource for such investigations since they allow for studying how genomes evolve as species exchange genetic material and for associating particular genetic regions with phenotypic traits of interest. Here we use whole-genome resequencing of both allopatric and hybridising populations of the European (Phylloscopus collybita abietinus) and the Siberian chiffchaff (P. tristis) - two recently diverged species which differ in morphology, plumage, song, habitat and migration - to quantify the regional variation in genome-wide genetic diversity and differentiation and to identify candidate regions for trait variation. We find that the levels of diversity, differentiation and divergence are highly heterogeneous with significantly reduced global differentiation and more pronounced differentiation peaks in sympatry than in allopatry. This pattern is consistent with regional differences in effective population size and recurrent background selection or selective sweeps reducing the genetic diversity in specific regions prior to lineage divergence, but the data also suggest that post-divergence selection has resulted in increased differentiation and fixed differences in specific regions. We find that hybridization and backcrossing is common in sympatry and that phenotype is a poor predictor of the genomic composition of sympatric birds. The combination of a differentiation scan approach with identification of fixed differences pinpoint a handful of candidate regions that might be important for trait variation between the two species.
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