Genomic variation across Chinook salmon populations reveals effects of a duplication on migration alleles and supports fine scale structure

Abstract

The distribution of ecotypic variation in natural populations is influenced by neutral and adaptive evolutionary forces that are challenging to disentangle. This study provides a high-resolution portrait of genomic variation in Chinook salmon (Oncorhynchus tshawytscha) with emphasis on a region of major effect for ecotypic variation in migration timing. With a filtered data set of ~13 million single nucleotide polymorphisms (SNPs) from low-coverage whole genome resequencing of 53 populations (3566 barcoded individuals), we contrasted patterns of genomic structure within and among major lineages and examined the extent of a selective sweep at a major effect region underlying migration timing (GREB1L/ROCK1). Neutral variation provided support for fine-scale structure of populations, while allele frequency variation in GREB1L/ROCK1 was highly correlated with mean return timing for early and late migrating populations within each of the lineages (r² = .58-.95; p < .001). However, the extent of selection within the genomic region controlling migration timing was much narrower in one lineage (interior stream-type) compared to the other two major lineages, which corresponded to the breadth of phenotypic variation in migration timing observed among lineages. Evidence of a duplicated block within GREB1L/ROCK1 may be responsible for reduced recombination in this portion of the genome and contributes to phenotypic variation within and across lineages. Lastly, SNP positions across GREB1L/ROCK1 were assessed for their utility in discriminating migration timing among lineages, and we recommend multiple markers nearest the duplication to provide highest accuracy in conservation applications such as those that aim to protect early migrating Chinook salmon. These results highlight the need to investigate variation throughout the genome and the effects of structural variants on ecologically relevant phenotypic variation in natural species.

Keywords: Chinook salmon; adaptive variation; low-coverage sequencing; migration timing; structural variants.