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The likelihood of a new migratory route emerging is presumably a function of 1) the associated fitness payoff and 2) the probability that the route arises in the first place. It has been suggested that diametrically opposed ‘reverse' migratory trajectories might be surprisingly common and, if such routes were heritable, it follows that they could underlie the rapid evolution of divergent migratory trajectories. Here, we used Eurasian blackcap (Sylvia atricapilla; ‘blackcap') ringing recoveries and geolocator trajectories to investigate whether a recently evolved northwards autumn migratory route – and accompanying rapid northerly wintering range expansion – could be explained by the reversal of each individual's population‐specific traditional southwards migratory direction. We found that northwards autumn migrants were recovered closer to the sites specified by an axis reversal than would be expected by chance, consistent with the rapid evolution of new migratory routes via bi‐axial variation in orientation. We suggest that the surprisingly high probability of axis reversal might explain why birds expand their wintering ranges rapidly and divergently, and propose that understanding how migratory direction is encoded is crucial when characterising the genetic component underlying migration. 

ABSTRACT 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, each of which was phenotyped for migratory behavior using radio‐telemetry tracking. These individuals were sampled 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 (F_ST) 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. 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, overlappingPER2, 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. 

Abstract Structural variants (SVs) are a major source of genetic variation; and descriptions in natural populations and connections with phenotypic traits are beginning to accumulate in the literature. We integrated advances in genomic sequencing and animal tracking to begin filling this knowledge gap in the Eurasian blackcap. Specifically, we (a) characterized the genome-wide distribution, frequency, and overall fitness effects of SVs using haplotype-resolved assemblies for 79 birds, and (b) used these SVs to study the genetics of seasonal migration. We detected >15 K SVs. Many SVs overlapped repetitive regions and exhibited evidence of purifying selection suggesting they have overall deleterious effects on fitness. We used estimates of genomic differentiation to identify SVs exhibiting evidence of selection in blackcaps with different migratory strategies. Insertions and deletions dominated the SVs we identified and were associated with genes that are either directly (e.g., regulatory motifs that maintain circadian rhythms) or indirectly (e.g., through immune response) related to migration. We also broke migration down into individual traits (direction, distance, and timing) using existing tracking data and tested if genetic variation at the SVs we identified could account for phenotypic variation at these traits. This was only the case for 1 trait—direction—and 1 specific SV (a deletion on chromosome 27) accounted for much of this variation. Our results highlight the evolutionary importance of SVs in natural populations and provide insight into the genetic basis of seasonal migration.