Significant Synteny and Colocalization of Ecologically Relevant Quantitative Trait Loci Within and Across Species of Salmonid Fishes

Abstract

Abstract The organization of functional regions within genomes has important implications for evolutionary potential. Considerable research effort has gone toward identifying the genomic basis of phenotypic traits of interest through quantitative trait loci (QTL) analyses. Less research has assessed the arrangement of QTL in the genome within and across species. To investigate the distribution, extent of colocalization, and the synteny of QTL for ecologically relevant traits, we used a comparative genomic mapping approach within and across a range of salmonid species. We compiled 943 QTL from all available species [lake whitefish (Coregonus clupeaformis), coho salmon (Oncorhynchus kisutch), rainbow trout (O. mykiss), Chinook salmon (O. tshawytscha), Atlantic salmon (Salmo salar), and Arctic charr (Salvelinus alpinus)]. We developed a novel analytical framework for mapping and testing the distribution of these QTL. We found no correlation between QTL density and gene density at the chromosome level but did at the fine-scale. Two chromosomes were significantly enriched for QTL. We found multiple synteny blocks for morphological, life history, and physiological traits across species, but only morphology and physiology had significantly more than expected. Two or three pairs of traits were significantly colocalized in three species (lake whitefish, coho salmon, and rainbow trout). Colocalization and fine-scale synteny suggest genetic linkage between traits within species and a conserved genetic basis across species. However, this pattern was weak overall, with colocalization and synteny being relatively rare. These findings advance our understanding of the role of genomic organization in the renowned ecological and phenotypic variability of salmonid fishes.