Ancient persistence and recurrent emergence of structural variants across divergent Atlantic salmon lineages

Abstract

Structural variants (SVs) are a major source of genomic diversity, yet the evolutionary origins of SVs shared across divergent populations remain difficult to resolve. Shared SVs may reflect ancient polymorphism, recurrent mutation, introgression, or subsequent lineage-specific frequency change, but the relative contribution of these processes often remains difficult to distinguish. Here, we investigated SV evolution across four Atlantic salmon (Salmo salar) lineages differing in geography, Europe versus North America, and domestication status, wild versus farmed. Using sensitive SV discovery, stringent genotyping, local PCA, haplotype-distance analyses, and forward simulations, we tested whether broadly shared SVs behave as a single class of variation or separate into distinct evolutionary categories. We generated a high-confidence SV map and found that SVs were enriched in repetitive regions, particularly segmental duplications and LTR retrotransposons, consistent with genome architecture shaping SV formation. Nearly half of high-confidence SVs were shared across all four lineages despite deep continental divergence, and simulations showed that this broad sharing is more consistent with ancient persistence than recurrent mutation alone. In contrast, a small subset of large SVs exhibited complex PCA clustering and multimodal haplotype-distance distributions, consistent with recurrent formation at structurally unstable loci. Large SVs also showed contrasting frequency trajectories between continents, and one immune gene-rich copy-number variable region showed a marked frequency increase in domesticated European salmon. Together, these results show that shared SVs comprise distinct evolutionary categories shaped by ancient persistence, recurrent mutation, and lineage-specific frequency change.