Telomeres are chromosome protectors that shorten during cell replication and in stressful conditions. Developing individuals are susceptible to telomere erosion when their growth is fast and resources limited. This is critical because the rate of telomere attrition in early life is linked to health and life span of adults. The metabolic telomere attrition hypothesis (MeTA) suggests that telomere dynamics can respond to biochemical signals conveying information about the organism’s energetic state. Among these signals are glucocorticoids (hormones that promote catabolic processes, potentially impairing costly telomere maintenance) and nucleotides, which activate anabolic pathways though the cellular enzyme target of rapamycin (TOR) preventing telomere attrition. During the energetically demanding growth phase, the regulation of telomeres in response to two contrasting signals—one promoting telomere maintenance and the other inducing attrition—provides an ideal experimental setting to test MeTa. We studied nestlings of a rapidly developing free-living passerine, the great tit (Parus major), that either received glucocorticoids (Cort-chicks), nucleotides (Nuc-chicks), or a combination of both (NucCort-chicks) all compared with controls (Cnt-chicks). Contrary to Cort-chicks, which showed telomere attrition, NucCort-chicks, did not. NucCort-chicks was the only group showing increased gene expression of telo2 (proxy for TOR activation), of mitochondrial enzymes linked to ATP production (atp5f1a-atp5f1b-cox6a1-cox4) and a higher efficiency in aerobically producing ATP. NucCort-chicks had also a higher expression of telomere maintenance genes (trf2) and of enzymatic antioxidant genes (gpx4-sod1). The findings show that nucleotides availability is crucial for preventing telomere erosion during fast growth in stressful environments.

Heat waves are predicted to be detrimental for organismal physiology with costs for survival that could be reflected in markers of biological state such as telomeres. Changes in early life telomere dynamics driven by thermal stress are of particular interest during the early post-natal stages of altricial birds because nestlings quickly shift from being ectothermic to poikilothermic to endothermic after hatching. Telomeres of ectothermic and endothermic organisms respond differently to environmental temperature, but investigations within species that transition from ectothermy to endothermy are lacking. Also, ambient temperature influences parental brooding behavior, which will alter the temperature experienced by offspring and thereby, potentially, their telomeres. We exposed zebra finch nestlings to experimental heat waves, and compared their telomere dynamics to that of a control group at 5, 12 and 80 days of age that correspond to three different thermoregulatory stages (ectothermic, poikilothermic and endothermic respectively); we also recorded parental brooding, offspring sex, mass, growth rates, brood size and hatch order. Nestling mass showed an inverse relationship with telomere length, and nestlings exposed to heat waves showed lower telomere attrition during their first 12 days of life (poikilothermic stage) compared to controls. Additionally, parents of heated broods reduced the time they spent brooding offspring (at five days old) compared to controls. Lower brooding effort was associated with shorter telomeres in 12 day old nestlings. Our results indicate that the effect of heat waves on telomere dynamics likely varies depending on age and thermoregulatory stage of the offspring in combination with parental brooding behavior during growth.

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.