Partial migration is a phenomenon where migratory and resident individuals of the same species co-exist within a population, and has been linked to both intrinsic (e.g., genetic) as well as environmental factors. Here we investigated the genomic architecture of partial migration in the Common blackbird, a songbird that comprises resident populations in the southern distribution range, partial migratory populations in central Europe and exclusively migratory populations in northern and eastern Europe. We generated whole-genome sequencing data for 60 individuals across the species’ distribution range, including resident populations (Spain and France), obligate migrants (Russia), and a partial migratory population with equal numbers of migratory and resident individuals in Germany. We estimated genetic differentiation (FST) of single-nucleotide variants (SNVs) in 2.5 kb windows between all possible population and migratory phenotype combinations, and focused our characterization on birds from the partial migratory population in Germany that have been individually phenotyped with radio-telemetry tracking. Despite overall low differentiation within the partial migratory German population, we identified several outlier regions with elevated differentiation on four distinct chromosomes. The region with the highest relative and absolute differentiation was located on chromosome 9, overlapping PER2, which has previously been shown to be involved in the control of the circadian rhythm across vertebrates. While this region showed high levels of differentiation, no fixed variant could be identified, supporting the notion that a complex phenotype such as migratory behavior is likely controlled by a large number of genetic loci.
Recombination generates new combination of alleles, whereby it maintains haplotype diversity and enhances the efficacy of selection. Despite the apparent stasis in positioning recombination events in birds, recombination rates differ widely across the genome and within species. The causes of recombination rate variation and its evolutionary impact on natural populations remain poorly understood. We used whole-genome resequencing data of 167 individuals of the Eurasian blackcap (Sylvia atricapilla) to characterise the historical recombination landscape variation at broad and fine scales among populations with distinct migratory phenotypes. We additionally evaluated the interplay between recombination rates with patterns of genetic diversity, population divergence (based on Fst and dxy), and potential signs of selection. Our comparative analyses revealed: i) Lower divergence of recombination maps at the broad scale and higher variability at fine scales. Resident island populations showed higher variability in recombination patterns among them and with continental populations. Recombination rates were more conserved in continental populations regardless of the migratory phenotype. ii) The degree of divergence between recombination maps correlated with population differentiation. It could also recapitulate population-specific demographic history and genetic structure. iii) Recombination rates correlated negatively with Fst and positively with nucleotide diversity and dxy, suggesting that recombination may reduce the effect of linked selection over the loss of neutral diversity. We identified chromosomal regions with potential signs of linked selection. This study evidences that recombination is a variable trait that shapes the diversity and evolution of population differentiation in the blackcap.
Recombination is responsible for breaking up haplotypes, influencing genetic variability, and the efficacy of selection. Bird genomes lack the protein PRDM9, a key determinant of recombination dynamics in most metazoans. The historical recombination maps in birds show an apparent stasis in the positioning of recombination events. This highly conserved recombination pattern over long timescales should constrain the evolution of recombination in birds, but extensive variation in recombination rate across the genome and between different species has been reported. Here, we characterise a fine-scale historical recombination map of an iconic migratory songbird, the European blackcap (Sylvia atricapilla) using a LD-based approach which accounts for population demography. We found variable recombination rates among and within chromosomes, which associate positively with nucleotide diversity and GC content, and a negatively with chromosome size. The recombination rates increased significantly at regulatory regions and not necessarily at high-dense gene regions. CpG islands associated strongly with recombination rates; however, their specific position and local DNA methylation patterns likely influenced this relationship. The association with retrotransposons varied according to specific family and location. Our results also provide evidence of a heterogeneous conservation of recombination maps between the blackcap and its closest sister taxon, the garden warbler at the intra-chromosomal level. These findings highlight the considerable variability of recombination rates at different scales and the role of specific genomic features at shaping this variation. This study opens the possibility of further investigating the impact of recombination in specific population-genomic features.