CAUSES AND CONSEQUENCES OF TELOMERE LENGTH VARIATION IN TWO WILD BIRD POPULATIONS

Understanding the physiological and molecular mechanisms that generate interindividual variation in survival and reproductive success is a central goal in evolutionary ecology. In this context, telomeres may be particularly relevant, as their length (TL) and attrition rate (ΔTL) may reflect somatic state and maintenance, and thus individual conditions/quality, while also capturing environmentally driven variation that may play a key role in life-history evolution. However, studies from wild populations are still limited and have yielded mixed results, especially those integrating multiple environmental, physiological and parental sources of interindividual variation in early-life TL/ΔTL, and those examining whether this variation translates into different performance over the entire lifespan. Therefore, the present thesis investigated the potential environmental, physiological and parental sources of interindividual variation in early-life TL and ΔTL, as well as the possible fitness consequences of such variation, on two wild bird species, the lesser kestrel (Falco naumanni) and the barn swallow (Hirundo rustica). Chapter 1 tested the effects of thermal stress and growth on ΔTL in lesser kestrel nestlings. ΔTL was slower in nestlings experiencing experimentally decreased nest temperature, while was faster under heatwaves and in faster-growing nestlings, indicating that both thermal stress and growth may accelerate telomere loss during development. Chapter 2 investigated, in barn swallow nestlings, the possible link between hypothalamus-pituitary-adrenal (HPA) axis activity (i.e. corticosterone release), stimulated through a handling-induced stress, and TL/ΔTL, while also testing the influence of developmental conditions and growth. TL and ΔTL were negatively associated with body mass and mass gain in males but not in females, pointing to sex-specific telomeric costs of growth. Moreover, higher corticosterone levels at the end of handling-induced stress were associated with faster ΔTL in smaller broods, but the opposite pattern emerged as brood size increased, suggesting HPA axis activity as a possible proximate mechanism through which stressful developmental conditions may influence telomere dynamics. In barn swallows, Chapter 3 examined environmental and parental sources of interindividual variation in early-life TL and whether this translated into differences in long-term survival. Nestling TL was negatively associated with brood size and paternal age, indicating that both competitive family environment and parental aging may contribute to nestlings’ TL variability. Notably, nestlings with longer telomeres showed higher probability of surviving beyond the first reproduction, suggesting that interindividual variation in TL established early in life can translate into differences in long-term survival, and longer telomeres at this stage may be favored by natural selection even in a species characterized by high annual mortality. The possible association between TL and fitness was further investigated by Chapter 4 in adult barn swallows. Consistent with TL measured during development, longer telomeres at recruitment (i.e. 1-year old) were associated with both longer lifespan and higher lifetime reproductive success, indicating that TL at the onset of adulthood may capture variation in individual quality, and be therefore still exposed to selection at the beginning of adult life. Furthermore, TL and ΔTL covaried with secondary sexual traits in a sex- and trait-specific manner, pointing to a potential role of telomere dynamics in sexual selection processes. Therefore, the thesis identifies multiple environmental, physiological and parental sources of interindividual variation in TL/ΔTL early in life, and shows that such variation can persist across life stages and be associated with survival, reproduction and ornament expression. Moreover, the presence of sex-specific relationships highlights the importance of considering species-specific traits when investigating both the possible causes and consequences of telomere variation. Overall, these results support the idea that telomeres may contribute to linking developmental conditions with later-life performance and suggest that telomere dynamics may represent one of the molecular mechanisms underlying life-history variation in wild populations.