Decoupling production from survival: longitudinal associations of genomic functional longevity with health, reproductive performance, and herd persistence in Holstein dairy cows

Extending functional longevity in high-producing dairy cows is important for improving economic efficiency, environmental sustainability, and animal welfare in modern dairy systems. This longitudinal controlled cohort study investigated the phenotypic expression of genomic functional longevity breeding values (GFLBV) in a stratified cohort of Holstein-Friesian F0 cows managed under uniform conditions for more than 10 yr. Pregnant heifers were genomically classified into High-GFLBV (n = 18) and Medium-GFLBV (n = 18) groups while being matched for genomic milk production breeding values (GMPBV), thereby minimizing confounding by production potential. Genomic stratification was distinct, with a large difference in GFLBV between groups (Hedges’ g = 24.7), whereas GMPBV did not differ significantly (Hedges’ g = −1.39). Lifetime phenotypes included milk yield and milk composition traits derived from monthly standard milk performance testing, as well as reproductive performance, survival time, herd retention, and detailed veterinary diagnoses. Outcomes were analyzed using linear mixed-effects models, Hedges’ g effect sizes with bootstrap 95% confidence intervals, and Kaplan–Meier survival analysis. Milk production trajectories were broadly comparable between groups across parities, indicating effective separation of functional longevity from production intensity. Across months in milk and parities 1 to 5, milk yield, energy-corrected milk, milk fat traits, lactose traits, and milk urea nitrogen showed no meaningful group differences. Milk protein percentage was modestly greater in High-GFLBV cows, whereas protein yield remained similar. In contrast, somatic cell count was greater in Medium-GFLBV cows, consistent with higher udder inflammatory burden despite similar overall lactation output. Age at first calving, lactation length, offspring birth body weight, and calf sex distribution were also comparable between groups, whereas High-GFLBV cows exhibited shorter calving intervals (Hedges’ g = −0.50), indicating more favorable reproductive efficiency under similar production demands. Despite similar milk output, Medium-GFLBV cows showed a consistently greater weighted disease burden beginning in lactation 1, characterized by mastitis clustering, transition-related disorders, and greater burdens of ketosis, digestive disorders, and infectious claw disease. This pattern progressed toward greater claw-related multimorbidity in lactation 2 and a more pronounced lameness-reproductive burden in lactation 3. Herd retention remained similar after lactation 1 (18 vs. 17 cows), but diverged thereafter; by lactations 2 to 6, the numbers of cows remaining were 18 versus 14, 17 versus 11, 14 versus 7, 10 versus 4, and 8 versus 2 for High- and Medium-GFLBV groups, respectively. No Medium-GFLBV cows remained beyond lactation 6, whereas High-GFLBV cows persisted into lactations 7 to 9. Survival analysis showed sustained separation of survival curves and longer median survival in High-GFLBV cows. Collectively, these findings provide long-term phenotypic evidence that GFLBV is associated with more favorable health, reproductive, and survival outcomes under comparable milk production potential, supporting its relevance in breeding programs targeting improved lifetime performance.