Early-life telomere length (TL) is associated with fitness in a range of organisms. Little is known about the genetic basis of variation in TL in wild animal populations, but to understand the evolutionary and ecological significance of TL it is important to quantify the relative importance of genetic and environmental variation in TL. In this study, we measured TL in 2746 house sparrow nestlings sampled across 20 years and used an animal model to show that there is a small heritable component of early-life TL (h2=0.04), but with a strong component of maternal inheritance. Variation in TL among individuals was mainly driven by environmental (year) variance, but also brood and parental effects. We did not find evidence for a negative genetic correlation underlying the observed negative phenotypic correlation between TL and structural body size. Thus, TL may evolve independently of body size and the negative phenotypic correlation is likely to be caused by non-genetic environmental effects. We further used genome‐wide association analysis to identify genomic regions associated with TL variation. We identified several putative genes underlying TL variation; these have been inferred to be involved in oxidative stress, cellular growth, skeletal development, cell differentiation and tumorigenesis in other species. Together, our results show that TL is a lowly heritable, polygenic trait which is strongly affected by environmental conditions in a free-living bird.
Telomere length and DNA methylation (DNAm) are two promising biomarkers of biological age. Environmental factors and life history traits are known to affect variation in both these biomarkers, especially during early life, yet surprisingly little is known about their reciprocal association. Here, we present the first study on a natural population to explore how variation in DNAm, growth rate and early-life conditions are associated with telomere length changes during development. We tested these associations by collecting data from wild, nestling zebra finches in the Australian desert. We found that increases in the level of DNAm were negatively correlated with telomere length changes across early life. We also confirm previously documented effects of post hatch growth rate and clutch size on telomere length in a natural ecological context for a species that has been extensively studied in the laboratory. However, we did not detect any effect of ambient temperature during developmental on telomere dynamics. We also found that the absolute telomere length of wild zebra finches, measured using the in-gel TRF method, was similar to that of captive birds. Our findings highlight exciting new opportunities to link and disentangle potential relationships between environmental, epigenetic and telomere length dynamics during early life.
Changes in telomere dynamics could underlie life-history trade-offs among growth, size and longevity, but our ability to quantify such mechanistic processes in natural, unmanipulated populations is limited. We investigated how 4 years of artificial selection for either larger or smaller body size affected early-life telomere length in two insular populations of wild house sparrows. A negative correlation between telomere length and structural size was evident under both selection regimes. The study also revealed that male sparrows had longer telomeres than females, after controlling for size, and there was a significant negative effect of harsh weather conditions on telomere length. The long-term fitness consequences of these changes in early-life telomere length induced by the artificial size selection were explored over a period of 11 years. These analyses indicated disruptive selection on telomere length because both short and long early-life telomere length tended to be associated with the lowest mortality rates and highest life expectancy. There was also weak evidence for a negative association between telomere length and annual reproductive success, but only in the population where body size was increased experimentally. Our results suggest that natural selection for optimal body size in wild animals will affect early-life telomere length during growth, which is known to be linked to longevity in birds, but also that the importance of telomeres for long-term somatic maintenance and fitness is complex in a wild bird species.