Variation in corticosterone and telomere dynamics according to sex and rearing environment in barn swallow nestlings

Telomeres are the chromosome ends that shorten at each cell division and are widely recognized as biomarkers of individual quality and environmental stress exposure. By controlling the stress response through corticosterone release, which in turn can damage telomeres, the hypothalamus-pituitary-adrenal (HPA) axis may mediate environmental influence on telomere dynamics. However, these links remain poorly investigated in wild vertebrates, especially during development. Here, in barn swallow (Hirundo rustica) nestlings, we investigated environmental, growth and sex influences on baseline corticosterone level, after acute handling-induced stress, and during recovery of homeostasis, as well as on telomere length (TL) and attrition (ΔTL) during growth. Moreover, we tested whether corticosterone levels/changes predicted TL/ΔTL. Baseline corticosterone declined with increasing body mass, suggesting condition-dependent variation in baseline HPA-axis activity. In addition, corticosterone at the end of handling increased with brood size, highlighting higher corticosterone in more competitive and energy-demanding rearing environments. Recovery was faster in heavier and faster-growing nestlings, indicating that individuals in better condition returned to homeostasis more efficiently. Heavier and faster-growing males, but not females, had shorter TL and faster ΔTL, suggesting male-specific growth costs. Moreover, among males, the relationship between corticosterone variation during acute stress response and ΔTL shifted from negative in smaller broods to positive in larger broods, suggesting increased telomere maintenance in competitive family environments. Overall, we revealed that early-life TL/ΔTL are jointly shaped by rearing conditions, HPA-axis activity, and growth in different ways among male and female offspring, possibly contributing to shape sex-specific life trajectories during adulthood through carry-over effects.