Patterns of natural selection acting on the mitochondrial genome of a locally adapted fish species

Abstract

Background: Mitochondrial DNA (mtDNA) is frequently used in population genetic studies and is usually considered as a neutral marker. However, given the functional importance of the proteins encoded by the mitochondrial genome, and the prominent role of mitochondria in cellular energy production, the assumption of neutrality is increasingly being questioned. Results: We tested for evidence of selection on the mitochondrial genome of the Atlantic salmon, which is a locally adapted and widely farmed species and is distributed across a large latitudinal cline. We analysed 20 independent regions of the salmon mtDNA that represented nine genes (ND1, ND2, ND3, COX1, COX2, ATP6, ND4, ND5, and CYTB). These 20 mtDNA regions were sequenced using a 454 approach from samples collected across the entire European range of this species. We found evidence of positive selection at the ND1, ND3 and ND4 genes, which is supported by at least two different codon-based methods and also by differences in the chemical properties of the amino acids involved. The geographical distribution of some of the mutations indicated to be under selection was not random, and some mutations were private to artic populations. We discuss the possibility that selection acting on the Atlantic salmon mtDNA genome might be related to the need for increased metabolic efficiency at low temperatures. Conclusions: The analysis of sequences representing nine mitochondrial genes that are involved in the OXPHOS pathway revealed signatures of positive selection in the mitochondrial genome of the Atlantic salmon. The properties of the amino acids involved suggest that some of the mutations that were identified to be under positive selection might have functional implications, possibly in relation to metabolic efficiency. Experimental evidence, and better understanding of regional phylogeographic structuring, are needed to clarify the potential role of selection acting on the mitochondrial genome of Atlantic salmon and other locally adapted fishes.