Explaining variation in life expectancy between individuals of the same age is fundamental to our understanding of population ecology and life history evolution. Variation in the length and rate of loss of the protective telomere chromosome caps has been linked to cellular lifespan. Yet, the extent to which telomere length and dynamics predict organismal lifespan in nature is still contentious. Using longitudinal samples taken from a closed population of Acrocephalus sechellensis (Seychelles warblers) studied for over 20 years, we describe the first study into life-long adult telomere dynamics (1-17 years) and their relationship to mortality under natural conditions (n = 204 individuals). We show that telomeres shorten with increasing age and body mass, and that shorter telomeres and greater rates of telomere shortening predicted future mortality. Our results provide the first clear and unambiguous evidence of a relationship between telomere length and mortality in the wild, and substantiate the prediction that telomere length and shortening rate can act as an indicator of biological age further to chronological age when exploring life history questions in natural conditions.

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.

Helping by group members is predicted to lead to delayed senescence by affecting the trade-off between current reproduction and future survival for dominant breeders. Here we investigate this prediction in the Seychelles warbler, Acrocephalus sechellensis, in which mainly female subordinate helpers (both co-breeders and non-breeding helpers) often help dominants raise offspring. We find that the late-life decline in survival usually observed in this species is greatly reduced in female dominants when a helper is present. Female dominants with a female helper show reduced telomere attrition, a measure that reflects biological ageing in this and other species. Finally, the probability of having female, but not male, helpers increases with dominant female age. Our results suggest that delayed senescence is a key benefit of cooperative breeding for elderly dominants and support the idea that sociality and delayed senescence are positively self-reinforcing. Such an effect may help explain why social species often have longer lifespans.

Several hypotheses have been put forward to explain the evolution of senescence. One of the leading hypotheses, the disposable soma hypothesis, predicts a trade-off, whereby early-life investment in reproduction leads to late-life declines in survival (survival senescence). Testing this hypothesis in natural populations is challenging, but important for understanding the evolution of senescence. We used the long-term data set from a contained, predator-free population of individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate how age-related declines in survival are affected by early-life investment in reproduction and early-life environmental conditions. The disposable soma hypothesis predicts that higher investment in reproduction, or experiencing harsh conditions during early life, will lead to an earlier onset, and an increased rate, of senescence. We found that both sexes showed similar age-related declines in late-life survival consistent with senescence. Individuals that started breeding at a later age showed a delay in survival senescence, but this later onset of breeding did not result in a less rapid decline in late-life survival. Although survival senescence was not directly related to early-life environmental conditions, age of first breeding increased with natal food availability. Therefore, earlylife food availability may affect senescence by influencing age of first breeding. The disposable soma hypothesis of senescence is supported by delayed senescence in individuals that started breeding at a later age and therefore invested less in reproduction.