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Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon

Kess, Tony1; Lehnert, Sarah1; Bentzen, Paul2; Duffy, Steven1; Messmer, Amber1; Dempson, J. Brian1; Newport, Jason2; Whidden, Chris2; Robertson, Martha1; Chaput, Gerald1; Breau, Cindy1; April, Julien3; Gillis, Carole-Anne4; Kent, Matthew5; Nugent, Cameron1; Bradbury, Ian1

Published Jun 18, 2025 on Dryad. https://doi.org/10.5061/dryad.g1jwstqz3

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Abstract

Complex traits often exhibit complex underlying architectures by evolution from standing variation, hard and soft sweeps, and alleles of varying effect size. Increasingly, studies implicate large-effect loci and polygenic patterns underpinning adaptation, but the extent that common genetic architectures are utilized during adaptation is not understood. Sea age or age at maturation represents a significant life history trait in Atlantic Salmon (Salmo salar), studied extensively in European Atlantic populations, with repeated identification of large-effect loci. However, the genetic basis of sea age within North American populations remains unclear, as does potential for a parallel trans-Atlantic genomic basis to sea age. Here, we used a large SNP array and whole genome re-sequencing to explore the genomic basis of sea age in North American Atlantic Salmon. We found significant associations at the gene and SNP level with a known large-effect locus (vgll3), indicating genetic parallelism, but found that this pattern varied based by sex and location. We identified non-repeated highly predictive loci associated with sea age among populations and sexes within North America, indicating polygenicity and low parallelism. Despite low parallelism, we uncovered conserved molecular pathways associated with sea age that were consistently enriched among comparisons, including calcium signalling, MapK signalling, focal adhesion, and phosphatidylinositol signalling. Together, our results indicate parallelism of the molecular basis of sea age in North American Atlantic Salmon across large-effect genes and molecular pathways, despite polygenicity. These findings reveal roles for both contingency and repeated adaptation at the molecular level in the evolution of life history variation.