Telomeres are emerging as correlates of fitness‐related traits and may be important mediators of ecologically relevant variation in life history strategies. Growing evidence suggests that telomere dynamics can be more predictive of performance than length itself, but very little work considers how telomere regulatory mechanisms respond to environmental challenges or influence performance in nature. Here, we combine observational and experimental data sets from free‐living tree swallows (Tachycineta bicolor) to assess how performance is predicted by the telomere regulatory gene POT1, which encodes a shelterin protein that sterically blocks telomerase from repairing the telomere. First, we show that lower POT1 gene expression in the blood was associated with higher female quality, that is, earlier breeding and heavier body mass. We next challenged mothers with an immune stressor (lipopolysaccharide injection) that led to “sickness” in mothers and 24 h of food restriction in their offspring. While POT1 did not respond to maternal injection, females with lower constitutive POT1 gene expression were better able to maintain feeding rates following treatment. Maternal injection also generated a 1‐day stressor for chicks, which responded with lower POT1 gene expression and elongated telomeres. Other putatively stress‐responsive mechanisms (i.e., glucocorticoids, antioxidants) showed marginal responses in stress‐exposed chicks. Model comparisons indicated that POT1 mRNA abundance was a largely better predictor of performance than telomere dynamics, indicating that telomere regulators may be powerful modulators of variation in life history strategies.

Long telomeres have become nearly synonymous with a variety of fitness-related traits and may be mediators of ecologically relevant variation in life history strategies. Growing evidence suggests that telomere dynamics are more predictive of performance than length itself, but very little work considers how telomere regulatory mechanisms respond to environmental challenges or influence performance in nature. Here, we combine observational and experimental datasets from free-living tree swallows (Tachycineta bicolor) to assess how performance is predicted by the telomere regulatory gene POT1, which encodes a shelterin protein that sterically blocks telomerase from repairing the telomere. First, we show that lower POT1 gene expression was associated with higher female quality, i.e. earlier breeding, and heavier body mass. We next challenged mothers with an immune stressor (lipopolysaccharide injection) that led to ‘sickness’ in mothers and 24h of food restriction in their offspring. While POT1 did not respond to maternal injection, females with lower constitutive gene expression were better able to maintain feeding rates following treatment. Maternal injection also generated a one-day stressor for chicks, who responded with decreased POT1 gene expression and elongated telomeres. Other putatively stress-responsive mechanisms (i.e. glucocorticoids, antioxidants) were not significantly different between control and stress-exposed chicks. Model comparisons indicated that POT1 mRNA abundance was a largely better predictor of performance than telomere dynamics, indicating that telomere regulators may be powerful modulators of variation in life history strategies.