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.

The patterns of genetic relatedness among individuals vary along the genome, representing fluctuation of local ancestry. The factors responsible for this variation have not been well studied in wild animals with ecological and behavioural relevance. Here, we characterise the genomic architecture of genetic relatedness in the Eurasian blackcap, an iconic songbird species in ecology and quantitative genetics of migratory behaviour. We identify 23 genomic regions with deviated local relatedness patterns, using a chromosome-level de novo assembly of the blackcap genome and whole-genome resequencing data of 179 individuals from nine populations with diverse migratory phenotypes. Five genomic regions show local relatedness patterns of polymorphic inversions, three of which are syntenic to polymorphic inversions known in the zebra finch. Phylogenetic analysis reveals these three polymorphic inversions evolved independently in the blackcap and zebra finch indicating convergence of polymorphic inversions. Population genetic analyses in these three inversions in the blackcap suggest balancing selection between two haplotypes in one locus and background selection in the other two loci. One genomic region with deviated local relatedness is under selection against gene flow by population-specific reduction in recombination rate. Other genomic islands including 11 pericentromeric regions consist of evolutionarily conserved and non-conserved recombination cold-spots under background selection. Two of these regions with non-conserved recombination suppression are known to be associated with population-specific migratory phenotypes, where local relatedness patterns support additional effects of population-specific selection. These results highlight how different forms of recombination suppression and selection jointly affect heterogeneous genomic landscape of local ancestries.

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.

Transposable elements are mobile genetic elements that have the ability to move around the genome, and as such can be a source of genome variability. Transposable elements (TEs) are ubiquitous and many are found within a wide variety of life. Based on their characteristics we can annotate TEs within the host genome and classify them into specific TE types and families. The increasing number of available high-quality genome references in recent years provides an excellent resource that will enhance the understanding of the role of recently active TEs on genetic variation and phenotypic evolution. Here we showcase this through a high-quality TE annotation of the Eurasian blackcap (Sylvia atricapilla), as our chromosome resolution reference genome allowed the reconstruction of difficult-to-assemble regions. We have the ability to distinguish species-specific and non-specific TEs. We investigate how these TE categories are distributed along the genome and evaluate their correlation with four genomic features: recombination rate, gene coverage, CpG island coverage and GC coverage. We found a marked difference between species-specific and non-specific TEs. While species-specific TEs were negatively correlated with both GC content and recombination rate, the correlation with recombination rate disappeared and turned positive for GC content when considering non-specific TEs.