Understanding individual‐level variation in response to the environment is fundamental to understanding life‐history evolution and population dynamics. Telomeres, the protective caps at the ends of chromosomes, shorten in response to oxidative stress, and telomere shortening is correlated with reduced survival and life span. Investigating telomere dynamics may help us quantify individual variation in the costs experienced from social and ecological factors, and enhance our understanding of the dynamics of natural populations.Here, we study spatio‐temporal variation in lifelong telomere dynamics in the Seychelles warbler, Acrocephalus sechellensis. We combine long‐term life history and ecological data with a large longitudinal dataset of mean telomere lengths, consisting of 1,808 samples from 22 cohorts born between 1993 and 2014. We provide a detailed analysis of how telomere dynamics vary over individual life spans and cohorts, and with spatio‐temporal variation in the social and ecological environment.We found that telomere length decreases with cross‐sectional and longitudinal measures of age, and most rapidly very early in life. However, both cross‐sectional and longitudinal data suggested that against this overall pattern of shortening, bouts of telomere length increase occur in some individuals. Using a large number of repeated measurements we show statistically that these increases are unlikely to be explained solely by qPCR measurement error.Telomere length varied markedly among cohorts. Telomere length was positively associated with temporal variation in island‐wide insect abundance—a key resource for the insectivorous Seychelles warbler—suggesting that the costs associated with living in harsher environments can be studied by investigating telomere dynamics. We also found evidence for sex‐specific relationships between telomeres and tarsus length, potentially reflecting differential costs of growth.Our long‐term data show that in a natural population, telomere dynamics vary in a complex manner over individual life spans, and across space and time. Variance in telomere dynamics among individuals is the product of a wide array of genetic, parental and environmental factors. Explaining this variation more fully will require the integration of comprehensive long‐term ecological and genetic data from multiple populations and species.

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