Telomere dynamics in relation to sexual selection, longevity and fitness: a case study on a small migratory passerine

Understanding molecular mechanisms underlying interindividual differences in lifespan, lifetime fitness, and sexually selected traits, is crucial to understand life-history evolution. Although telomere length (TL) and its attrition rate (ΔTL) has been suggested to be potential biomarkers of somatic state and maintenance, most studies in the wild were focused on short-term links between telomeres, survival, and fitness, while their long-term implications and role in sexual selection remain little explored. Here, we aimed at investigating TL and ΔTL in nestling and adult barn swallows (Hirundo rustica) to assess: 1) environmental and parental factors influencing early-life TL; 2) annual and long-term survival as well as seasonal and lifetime reproductive success in relation to both nestling TL, and adult TL and ΔTL; 3) the association between TL and the expression of a sexually selected traits (i.e. outermost tail feathers length). Nestling TL decreased with brood size and paternal age, indicating potential effects of developmental conditions and paternal aging. Furthermore, longer early-life TL predicted higher long-term survival, supporting the possibility of natural selection on TL in early life. In adults, TL longitudinally declined with age, but neither TL nor ΔTL predicted annual survival and fitness. Similarly, TL at one year was unrelated to lifespan or lifetime fitness (i.e. total number of fledglings). However, in females, shorter TL was associated with longer tails, suggesting a sex-dependent reproductive cost on telomeres. Our results indicate that TL may predict survival early in life but not in adulthood, where it may instead reflect trade-offs between reproduction and physiological maintenance.