Selective breeding programs improve target traits but can also unintentionally change genetically correlated traits in the selected strain. The U.S. Department of Agriculture–Agricultural Research Service National Cold Water Marine Aquaculture Center (NCWMAC) in Franklin, Maine maintains a North American Atlantic salmon selective breeding program focused on improving commercially important traits (e.g., carcass weight). However, the program has experienced a significant decline in the percent of eyed embryos over its 14 years of operation, leading to concerns that reproductive performance was being unintentionally changed by selection for the target traits. The aims of this study were to 1) model eye up success as a potentially heritable trait utilizing the recorded pedigree and 2) assess the relationship between eye-up rate and environmental conditions experienced by the broodstock. Over 14 years of data encompassing 1537 full-sib families produced by 1537 dams and 885 sires was analyzed. Counts of eyed embryos and carcass weight were analyzed with a linear multi-trait trait model that included maternal genetic effects and a spawn year effect to determine the strength of genetic and environmental influences on the eyed embryo rate. To investigate the environmental influences in more detail, we assessed the correlation between water quality parameters in the broodstock rearing system observed over the same 14-year time period and the estimated spawn year effects. There was small heritability of the direct genetic effect (0.059 ± 0.009) and the maternal genetic effect (0.039 ± 0.013). Comparatively, the proportion of phenotypic variance explained by the maternal environmental effect was moderate (0.165 ± 0.012). The genetic correlations between carcass weight and eye up rate were very small and had a large amount of uncertainty. The correlation between the direct genetic effects on eye-up and carcass weight was −0.0528 ± 0.1469 while the correlation between the maternal genetic effect on eye-up and the direct genetic effect on carcass weight was 0.2030 ± 0.1791. The correlation between maternal common environmental effects on the two traits was also low at 0.0676 ± −0.0804. The effect of spawn year was statistically significant (p < 0.01), and the values were negatively correlated with mean un-ionized ammonia (mg/L, −0.56, p = 0.04,), nitrate concentrations (mg/L r = −0.65, p = 0.01) and temperature (°C, r = −0.61, p = 0.02) experienced by the broodstock prior to spawning. Overall, the results suggest that the decrease in eyed embryos over time was not caused by inadvertent selection but instead due to increases in water temperature and/or nitrogenous waste concentrations in the broodstock rearing system. Further investigation of the mechanisms behind these apparent environmentally induced declines and potential mitigation measures to prevent decreases in eye-up rates are needed.
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