Associations between DNA methylation and telomere length during early life: insight from wild zebra finches (Taeniopygia guttata)

Abstract

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.

Effects of heat waves on telomere dynamics and parental brooding effort in nestlings of the zebra finch (Taeniopygia castanotis)

“…Finally, we also found a negative correlation between telomere length and body mass independently of treatment and age, and this is important because both telomere and body size have been shown to be heritable (Jensen et al 2003;Boonekamp et al 2020), and may influence bird fitness (Ringsby et al 2015). Similar results were previously generated in a selection experiment aimed at manipulating tarsus length which is related to structural size (Ringsbyet al 2015), and in a descriptive study on the same species used here (Sheldon et al 2021). Similar to the findings of another study (Boonekamp et al 2020), variation in telomere length in our analysis did not appear to be associated with differences in rates of growth.…”

“…To date our understanding of parental care and ambient temperature in explaining post-natal telomere dynamics at different thermoregulatory stages is limited. Descriptive studies of wild zebra finchesTaeniopygia castanotis , exposed to natural variation in ambient conditions have revealed positive correlations between ambient temperatures and another biomarker of aging, the DNA methylation rate (Sheldon et al 2020), and of the latter with rates of telomere shortening (Sheldon et al 2021). These correlative results suggest that thermal conditions during early life influence telomeres, but since temperature was not manipulated in that study (Sheldonet al 2021), other factors may affect the results such as seasonal variation in reproductive investment, parental condition, or food availability.…”

“…Therefore, the physiological adjustments triggered by heat in our previous experiment may be beneficial for telomeres as predicated under the uncoupling to survive hypothesis (Brand 2000), or detrimental depending on the thermoregulatory conditions. While telomeres were not considered in the aforementioned studies, those findings (Sheldon et al 2020, Sheldon et al 2021, Ton et al 2021a provide testable predictions about the likely effects of the experimental treatment on telomere length.…”

Integrating telomere biology into the ecology and evolution of natural populations: Progress and prospects

“…In European badgers Meles meles , van Lieshout et al (2021) report that cubs born in warmer, wetter springs have longer telomere lengths, which is in turn linked to survival. In purple‐crowned fairy wrens ( Malurus coronatus ) the rate of telomere shortening in the first year of life predicted lifespan (Sheldon, Ton, et al, 2021). More broadly, it has been hypothesized that measuring the effects of adverse environmental conditions induced by anthropogenic stressors (such as chemical pollutants, noise and inappropriate light) on telomere dynamics could assist in the monitoring and conservation of wildlife.…”

Editorial 2023

“…A final group of manuscripts explores the intriguing nature of heritability of telomere length and rate of shortening (Bauch et al, 2022; Kärkkäinen, Briga, et al 2022; Le Pepke, Kvalnes, Lundregan, et al, 2022; Sparks et al, 2022; Vedder et al, 2022). Throughout the special issue, a number of articles also delve into the putative mechanisms underlying telomere dynamics (Metcalfe & Olsson, 2022; Wolf et al, 2022) including telomerase activity, which is crucial to telomere maintenance (Noguera et al, 2022; Sheldon, Ton, et al, 2022; Smith et al, 2022). Collectively, the body of work in this special issue demonstrates the powerful and complex role telomeres play in the ecology and evolution of natural populations and highlights the need for continued research in this area (Monaghan et al, 2022).…”