Temporal Comparison Reveals Weakened Genotype-Phenotype Association at a Major-Effect Locus in Dworshak National Fish...

Life history diversity in salmonids contributes to population resilience, yet the mechanisms driving contemporary life history change remain difficult to disentangle from demographic and environmental processes. We evaluated long-term changes in neutral genetic variation, adaptive haplotypes near the six6 gene, and life history traits in the Dworshak National Fish Hatchery steelhead (Oncorhynchus mykiss) broodstock by comparing archived scale samples from the founding broodstock and subsequent returns (1969-1976) with contemporary samples (2014-2016; 2019-2022). Neutral genetic diversity and population structure remained stable through time, consistent with prior evidence that observed life history shifts were not associated with erosion of neutral genetic diversity. In contrast, we detected pronounced temporal shifts in adaptive variation near the six6 gene on chromosome 25, including a decline in the long haplotype historically associated with extended years in the ocean and larger body size. Ocean age composition also shifted over time, with an increased proportion of 2-ocean fish and altered age distributions within six6 genotype classes. Although six6 remained significantly associated with length-at-age, the magnitude of phenotypic differences among genotypes was substantially reduced in contemporary samples, indicating a weakening of the genotype-phenotype relationship. These results suggest that environmental conditions increasingly constrain, or otherwise alter, the expression of genetically based life history variation. Our findings demonstrate that life history change can occur without loss of neutral genetic diversity and highlight the importance of integrating genetic and demographic data to understand eco-evolutionary responses of salmonids under changing ocean conditions.