Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

Abstract

Poor conditions during early development can initiate trade‐offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life‐history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early‐life conditions to lifespan and fitness. In wild purple‐crowned fairy‐wrens, we combined measurements of nestling telomere length (TL) with detailed life‐history data to investigate whether early‐life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age‐dependent with early‐life TL having a positive effect on lifespan only among individuals that survived their first year. Early‐life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early‐life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early‐life TL, which reflects growth, accumulated early‐life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early‐life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early‐ and late‐life performance and trade‐offs across a lifetime.

Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long‐lived seabird

“…Moreover, little is known about the dynamics of interstitial telomeric DNA, which is included in qPCR measures of telomere length. A large difference in the amount of measurement error between measurement methods would also provide an explanation, but some qPCR studies report intrasample repeatabilities that are similar to those obtained in TRF studies (e.g., Eastwood et al, ; van Lieshout et al, ). More studies with repeatedly sampled individuals over a long time period will be required to resolve this issue.…”

“…In agreement with other studies (Wilbourn et al, ), we found that longer telomere length, corrected for age, predicted a longer remaining lifespan and a lower mortality hazard in adults. Combined with the high within‐individual repeatability in telomere length, this raises the intriguing question of whether an individual's telomere length and lifespan are already partly determined early in life (Eastwood et al, ; Heidinger et al, ). In the same colony of common terns, we were previously unable to identify environmental factors that affected telomere length after hatching (Vedder, Verhulst, et al, ), but conditions during embryonic development (Vedder et al, ), as well as paternal age (Bouwhuis, Verhulst, Bauch, & Vedder, ; see also Bauch, Boonekamp, Korsten, Mulder, & Verhulst, for a longitudinal study in jackdaws Corvus monedula ), affected telomere length in common tern chicks.…”

Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets

“…In adult humans, telomere shortening is related to stress (Epel et al 2004;Entringer et al 2011), disease (Calado & Young 2009), and lifestyle factors (Lin et al 2012) and telomere length predicts mortality risk (Boonekamp et al 2013). Telomere length also predicts mortality (Wilbourn et al 2018) and fitness (Eastwood et al 2019) in natural populations of vertebrates and the rate of telomere attrition is correlated to lifespan across species (Tricola et al 2018). Gradual telomere erosion with growth and/or age could reflect a multilevel process of cell division, damage, and repair, linked to fitness.…”

Universal assay for measuring vertebrate telomeres by real-time quantitative PCR

“…The length of telomere DNA shortens at each cell division, and telomere shortening eventually leads to cellular senescence, which affects tissue function, organismal health and lifespan. Studies in vertebrate systems have shown that the length of telomere repeat regions correlate with phenotypic quality, and can even predict longevity, and reproductive success [2][3][4] . Telomere lengths are therefore an established predictive biomarker for health and aging.…”