Journal Article

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

Kess, Tony, Breau, Cindy, Lehnert, Sarah J., Newport, Jason, Whidden, Christopher, Robertson, Martha J., Dempson, J. Brian, Nugent, Cameron M., Chaput, Gerald, Bradbury, Ian R., Gillis, Carole‐Anne, April, Julien, Messmer, Amber, Kent, Matthew, Bentzen, Paul, Duffy, Steven

2024

Overview

Complex traits often exhibit complex underlying genetic architectures resulting from a combination of evolution from standing variation, hard and soft sweeps, and alleles of varying effect size. Increasingly, studies implicate both large‐effect loci and polygenic patterns underpinning adaptation, but the extent that common genetic architectures are utilized during repeated adaptation is not well understood. Sea age or age at maturation represents a significant life history trait in Atlantic Salmon (Salmo salar), the genetic basis of which has been studied extensively in European Atlantic populations, with repeated identification of large‐effect loci. However, the genetic basis of sea age within North American Atlantic Salmon populations remains unclear, as does the potential for a parallel trans‐Atlantic genomic basis to sea age. Here, we used a large single‐nucleotide polymorphism (SNP) array and low‐coverage whole‐genome resequencing to explore the genomic basis of sea age variation in North American Atlantic Salmon. We found significant associations at the gene and SNP level with a large‐effect locus (vgll3) previously identified in European populations, indicating genetic parallelism, but found that this pattern varied based on both sex and geographic region. We also identified nonrepeated sets of highly predictive loci associated with sea age among populations and sexes within North America, indicating polygenicity and low rates of genomic parallelism. Despite low genome‐wide parallelism, we uncovered a set of conserved molecular pathways associated with sea age that were consistently enriched among comparisons, including calcium signaling, MapK signaling, focal adhesion, and phosphatidylinositol signaling. 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 population‐specific patterns of polygenicity. These findings reveal roles for both contingency and repeated adaptation at the molecular level in the evolution of life history variation. Complex traits often exhibit complex underlying genetic architectures, and studies have begun to identify both large‐effect loci and polygenic patterns underpinning adaptation. Sea age represents a significant life history trait in Atlantic Salmon (Salmo salar), the genetic basis of which has been studied extensively in European populations, with repeated identification of large‐effect loci. In a survey of North American rivers, we found significant associations at the gene and SNP level with a large‐effect locus (vgll3) previously identified in European populations, but found that this pattern varied based on both sex and geographic region. Contrasting low genome‐wide parallelism, we uncovered a set of conserved molecular pathways associated with sea age that were consistently enriched among comparisons, indicating parallelism of the molecular basis of sea age in North American Atlantic Salmon across large‐effect genes and molecular pathways despite population‐specific patterns of polygenicity.

• Publisher: John Wiley & Sons, Inc,Wiley
• Subject: Adaptation / Age / Atlantic Salmon / Biological evolution / Calcium signalling / Contingency / Environmental conditions / Fish / Fish populations / Genes / genetic architecture / Genomes / Genomics / Life history / MAP kinase / Nucleotides / Phosphatidylinositol / Polygenic inheritance / Polymorphism / Population genetics / Populations / Rivers / Salmon / Signal transduction / Single-nucleotide polymorphism / Variation