Heritability and age-dependent changes in genetic variation of telomere length in a wild house sparrow population

Telomeres are a popular biomarker of senescence, as telomere dynamics are linked with survival and lifespan. However, the evolutionary potential of telomere dynamics, and the selection pattern that gives rise to senescence, are not well known. To better understand this, it is necessary to quantify genetic variation in telomere length, and how such variation changes with age. Here, we analysed a longitudinal dataset (2,156 samples from 1,267 individuals across 15 years) from a wild, insular house sparrow (Passer domesticus) population with complete life-history and genetic relatedness data. Using a series of ‘animal’ models, we confirmed that telomere length (TL): (1) changes with age, reflecting senescence in this population. We then showed that (2) TL is repeatable (15.7%, 95% CrI: 10.2–21.0%) and heritable (14.0%, 95% CrI: 8.7–19.5%); and, for the first time in the wild, (3) that TL shows a genotype-by-age interaction, meaning that genotypes differ in their rate of TL change, where additive genetic variance increases at older ages. Our findings provide empirical evidence from a wild population that supports hypotheses explaining the evolution of senescence, and highlights the importance of telomere dynamics as a key biomarker of body physiology for the evolution of senescence.