Chromosomal fusion and life history-associated genomic variation contribute to within-river local adaptation of Atlantic salmon

Chromosomal inversions have been implicated in facilitating adaptation in the face of high levels of gene flow, but whether chromosomal fusions also have similar potential remains poorly understood. Atlantic salmon are usually characterized by population structure at multiple spatial scales; however, this is not the case for tributaries of the Miramichi River in North America. To resolve genetic relationships between populations in this system and the potential for known chromosomal fusions to contribute to adaptation, we genotyped 728 juvenile salmon using a 50 K SNP array. Consistent with previous work, we report extremely weak overall population structuring (Global F-ST = 0.004) and failed to support hierarchical structure between the river's two main branches. We provide the first genomic characterization of a previously described polymorphic fusion between chromosomes 8 and 29. Fusion genomic characteristics included high LD, reduced heterozygosity in the fused homokaryotes, and strong divergence between the fused and the unfused rearrangement. Population structure based on fusion karyotype was five times stronger than neutral variation (F-ST = 0.019), and the frequency of the fusion was associated with summer precipitation supporting a hypothesis that this rearrangement may contribute local adaptation despite weak neutral differentiation. Additionally, both outlier variation among populations and a polygenic framework for characterizing adaptive variation in relation to climate identified a 250-Kb region of chromosome 9, including the gene six6 that has previously been linked to age-at-maturity and run-timing for this species. Overall, our results indicate that adaptive processes, independent of major river branching, are more important than neutral processes for structuring these populations.