Distinct patterns of genetic variation at low-recombining genomic regions represent haplotype structure

Genomic regions sometimes show patterns of genetic variation distinct from the genome-wide population structure. Such deviations have often been interpreted to represent effects of selection. However, systematic investigation of whether and how non-selective factors, such as recombination rates, can affect distinct patterns has been limited. Here, we associate distinct patterns of genetic variation with reduced recombination rates in a songbird, the Eurasian blackcap (Sylvia atricapilla), using a new reference genome assembly, whole-genome resequencing data and recombination maps. We find that distinct patterns of genetic variation reflect haplotype structure at genomic regions with different prevalence of reduced recombination rate across populations. At low-recombining regions shared in most populations, distinct patterns reflect conspicuous haplotypes segregating in multiple populations. At low-recombining regions found only in a few populations, distinct patterns represent variance among cryptic haplotypes within the low-recombining populations. With simulations, we confirm that these distinct patterns evolve neutrally by reduced recombination rate, on which the effects of selection can be overlaid. Our results highlight that distinct patterns of genetic variation can emerge through evolutionary reduction of local recombination rate. The recombination landscape as an evolvable trait therefore plays an important role determining the heterogeneous distribution of genetic variation along the genome.