Telomere length at recruitment predicts lifespan and lifetime reproductive success in the barn swallow (Hirundo rustica)

Identifying molecular mechanisms linked to variation in lifespan, reproductive output and sexually selected traits is key to understanding life-history evolution in wild populations. Telomere length (TL) and attrition (ΔTL) have been proposed as biomarkers of somatic state and maintenance (survival). Yet evidence linking telomeres to lifetime fitness and ornament expression remains limited. We quantified age-related variation in TL and annual ΔTL between the year of recruitment (1-year-old) and death, as well as tested whether TL at recruitment predicts realized lifespan and lifetime reproductive success in a short-lived migratory passerine, the barn swallow (Hirundo rustica). We also examined associations between TL/ΔTL and two sexual ornaments (outermost tail feathers length and ventral plumage colouration). TL constantly declined with age, and longer TL as yearling was linked to increased lifespan and higher number of fledglings during the entire life, indicating that TL captures considerable variation in individual quality. Moreover, longer tail feathers and a larger increase in tail length between consecutive years were associated, respectively, with shorter TL and faster ΔTL among females. Additionally, plumage darkening between consecutive years was associated with reduced ΔTL in both sexes, indicating that telomeres covary with secondary sexual traits in a sex- and trait-specific manner and may be involved in sexual selection processes. Overall, even in a species with high annual mortality, TL positively predicted major fitness components, supporting TL as a biomarker of individual quality and suggesting that longer telomeres at the onset of adulthood may be favoured by natural selection in wild populations.