Structural genomic variation and migratory behavior in a wild songbird

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.

How structural variants shape avian phenotypes: Lessons from model systems

“…These studies show an improved understanding of the genetic bases of phenotypes when SVs, which involve a larger portion of the genome, are included (e.g. Delmore et al 2023;Knief et al, 2019). Lundberg et al, 2023).…”

“…Lundberg et al, 2023). The same trait can be modified in multiple ways, as a 710-bp deletion on chromosome 27 in the Eurasian Blackcap (Sylvia atricapilla) also shapes migratory phenotypes (Delmore et al, 2023). Other complex behavioural traits are mediated by supergenes in the Ruff (Philomachus pugnax; Küpper et al, 2016) and the White-throated sparrow (Zonotrichia albicollis; Tuttle et al, 2016).…”

Fitness consequences of structural variation inferred from a House Finch pangenome

“…They differ from the more common and simpler 'single nucleotide polymorphisms' (SNPs), which involve only single DNA base changes. SVs are important for adaptation in natural populations (1)(2)(3)(4)(5)(6)(7)(8)(9), influencing morphology (10)(11)(12)(13), behavior (14)(15)(16)(17), and other physiological traits, such as disease resistance in humans (18), animals (8,19), and plants (20). However, compared to SNPs, we know little about the fitness effects of SVs due to their underrepresentation in short-read sequencing data and the understudied links to phenotypes (4,(21)(22)(23)(24).…”