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

Abstract

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 50K SNP array. Consistent with previous work, we report extremely weak overall population structuring (Global FST = 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 (FST = 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. Conservation and management of species benefit from an understanding of fine-scale demographic and evolutionary processes, which aid in delimitating appropriate population-scale

Genome of an iconic Australian bird: High‐quality assembly and linkage map of the superb fairy‐wren (Malurus cyaneus)

“…More points of comparison would help to show whether certain chromosomes or particular motifs found in chromosomes might be more prone to rearrangements than others. Furthermore, the dynamic fission and fusion of the gene‐rich microchromosomes may have implications regarding species or clade‐specific adaptation (Guerrero & Kirkpatrick, ; Hansmann et al, ; Wellband et al, ). Physically creating or breaking linkages between sets of genes will change the local recombination rates.…”

Chromosome polymorphisms track trans‐Atlantic divergence and secondary contact in Atlantic salmon

“…However, without information on individual phenotype and ecological data, our conclusions regarding the adaptive nature of the rearrangements remain speculative. Nevertheless, recent work from a river system in North America (Miramichi River, New Brunswick, Canada) also identified variation in the Ssa08/29 chromosomal fusion and found that the frequency of the fusion was associated with precipitation, suggesting a potential role in local adaptation (Wellband et al, ). Many salmonid species show differences in karyotypes (Phillips, ) and although limited studies suggest that some identified rearrangements may not be involved in adaptive differences between individuals (Thorgaard, ), the identification of rearrangements coupled with advances in genomic technologies will allow better characterization of the adaptive or neutral role of rearrangements in salmonids.…”

Consequences of Single-Locus and Tightly Linked Genomic Architectures for Evolutionary Responses to Environmental Change

“…In recent years, linked genomic architectures have been associated with a variety of adaptive traits in natural populations ( Table 1 ). Although inversions appear to be the most commonly studied ( Wellenreuther and Bernatchez 2018 ; Wellenreuther et al 2019 ), chromosomal fusions ( Wellband et al 2019 ) and complex architectures involving multiple rearrangements ( Tigano et al 2018 ; Pearse et al 2019 ) are also associated, directly or indirectly, with traits relevant for adaptation. In some cases, SNPs located in proximity to one another are found to be in LD and the structural architecture is yet to be determined (e.g., Micheletti et al 2018 ).…”

“…Chromosomal translocations and fusions are common among salmonids ( Phillips 2005 ). Their adaptive significance, if any, is not generally known, although a fusion in Atlantic salmon (Ssa08/Ssa29) is associated with summer precipitation in a Canadian river system ( Wellband et al 2019 ).…”