Abstract
Most Atlantic salmon (Salmo salar L.) populations follow an anadromous life cycle, spending early life in freshwater, migrating to the sea for feeding, and returning to rivers to spawn. At the end of the last ice age ~10,000 years ago, several populations of Atlantic salmon became landlocked. Comparing their genomes to their anadromous counterparts can help identify genetic variation related to either freshwater residency or anadromy. The objective of this study was to identify consistently divergent loci between anadromous and landlocked Atlantic salmon strains throughout their geographical distribution, with the long‐term aim of identifying traits relevant for salmon aquaculture, including fresh and seawater growth, omega‐3 metabolism, smoltification, and disease resistance. We used a Pool‐seq approach (n = 10–40 individuals per population) to sequence the genomes of twelve anadromous and six landlocked Atlantic salmon populations covering a large part of the Northern Hemisphere and conducted a genomewide association study to identify genomic regions having been under different selection pressure in landlocked and anadromous strains. A total of 28 genomic regions were identified and included cadm1 on Chr 13 and ppargc1a on Chr 18. Seven of the regions additionally displayed consistently reduced heterozygosity in fish obtained from landlocked populations, including the genes gpr132, cdca4, and sertad2 on Chr 15. We also found 16 regions, including igf1 on Chr 17, which consistently display reduced heterozygosity in the anadromous populations compared to the freshwater populations, indicating relaxed selection on traits associated with anadromy in landlocked salmon. In conclusion, we have identified 37 regions which may harbor genetic variation relevant for improving fish welfare and quality in the salmon farming industry and for understanding life‐history traits in fish.
Highlights
One of the most extreme adaptations in Atlantic salmon (Salmo salar) occurred during land rise following the most recent ice age ~10,000 years ago, when numerous salmon strains became landlocked throughout the geographical distribution in the Northern Hemisphere (Hutchings et al, 2019; Tonteri et al, 2005)
Sequence reads mapped to the Atlantic salmon reference genome were used to identify a total of 43,329,247 single nucleotide polymorphisms (SNPs) in the genomes of landlocked and anadromous salmon
We identified a selective sweep on Chr 5 which contains a SNP previously found to explain 5.83% of phenotype variation in resistance to infectious salmon anemia (ISA) in commercial Saint John River Atlantic salmon (Holborn et al, 2020)
Summary
One of the most extreme adaptations in Atlantic salmon (Salmo salar) occurred during land rise following the most recent ice age ~10,000 years ago, when numerous salmon strains became landlocked throughout the geographical distribution in the Northern Hemisphere (Hutchings et al, 2019; Tonteri et al, 2005). It is likely that different landlocked populations of salmon have been exposed to similar selection pressures and relaxed selection on seawater traits and gone through similar genetic adaptation, sometimes independently of each other. Such populations present a unique opportunity to identify genomic regions under selection for different important traits, as successfully demonstrated in salmon for the age at maturity (Ayllon et al, 2015; Barson et al, 2015) and on genes associated with disease resistance (Kjaerner-Semb et al, 2016; Zueva et al, 2018). Comparisons between landlocked and anadromous salmon may provide an excellent model for identifying genetic mechanisms underlying evolution of important phenotypic traits during seawater adaptation such as smoltification, resistance to seaborne diseases, and omega-3 synthesis
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