Spatio‐temporal variation in lifelong telomere dynamics in a long‐term ecological study

Abstract

Understanding individual‐level variation in response to the environment is fundamental to understanding life‐history evolution and population dynamics. Telomeres, the protective caps at the ends of chromosomes, shorten in response to oxidative stress, and telomere shortening is correlated with reduced survival and life span. Investigating telomere dynamics may help us quantify individual variation in the costs experienced from social and ecological factors, and enhance our understanding of the dynamics of natural populations.Here, we study spatio‐temporal variation in lifelong telomere dynamics in the Seychelles warbler, Acrocephalus sechellensis. We combine long‐term life history and ecological data with a large longitudinal dataset of mean telomere lengths, consisting of 1,808 samples from 22 cohorts born between 1993 and 2014. We provide a detailed analysis of how telomere dynamics vary over individual life spans and cohorts, and with spatio‐temporal variation in the social and ecological environment.We found that telomere length decreases with cross‐sectional and longitudinal measures of age, and most rapidly very early in life. However, both cross‐sectional and longitudinal data suggested that against this overall pattern of shortening, bouts of telomere length increase occur in some individuals. Using a large number of repeated measurements we show statistically that these increases are unlikely to be explained solely by qPCR measurement error.Telomere length varied markedly among cohorts. Telomere length was positively associated with temporal variation in island‐wide insect abundance—a key resource for the insectivorous Seychelles warbler—suggesting that the costs associated with living in harsher environments can be studied by investigating telomere dynamics. We also found evidence for sex‐specific relationships between telomeres and tarsus length, potentially reflecting differential costs of growth.Our long‐term data show that in a natural population, telomere dynamics vary in a complex manner over individual life spans, and across space and time. Variance in telomere dynamics among individuals is the product of a wide array of genetic, parental and environmental factors. Explaining this variation more fully will require the integration of comprehensive long‐term ecological and genetic data from multiple populations and species.

Divergent patterns of telomere shortening in tropical compared to temperate stonechats

“…Similar to other studies (e.g., Spurgin et al, 2018), we find that mean telomere length decreased fastest during the first year of life in temperate stonechats. Similar to other studies (e.g., Spurgin et al, 2018), we find that mean telomere length decreased fastest during the first year of life in temperate stonechats.…”

“…that, in general, older individuals have shorter telomeres than younger ones with the greatest loss in telomeres occurring early in life (Heidinger et al, 2012;Pauliny, Larsson, & Blomqvist, 2012;Salomons et al, 2009;Spurgin et al, 2018;Tricola et al, 2018).…”

Individual variation in early‐life telomere length and survival in a wild mammal

“…Within‐individual RLTL correlations in humans were high (0.82–0.93; Benetos et al, ) and individual repeatability in RLTL in avian TRF studies was also high (81%–83%; Bauch et al, ; Boonekamp et al, ). In contrast, lifelong qPCR studies in wild populations provide substantially lower repeatability estimates (7%; Spurgin et al, ; 13%; Fairlie et al, ). The individual repeatability estimate in RLTL in our system is in the lower spectrum of qPCR‐studies.…”

“…Hence, studies of wild populations have informed understanding of how early‐life environments shape individual senescence patterns (Cooper & Kruuk, ; Lemaitre et al, ; Nussey, Froy, Lemaitre, Gaillard, & Austad, ). This understanding has been further improved by quantification of extrinsic effects through biomarkers that reflect ecological effects that are otherwise difficult to measure (Bebbington et al, ; Spurgin et al, ).…”

“…Correlations among within‐individual telomere measurements in humans were high (0.82–0.93; Benetos et al, ), which corroborates the high individual repeatability (i.e., 81%–83%) in telomere length in wild populations using TRF (telomere restriction fragment) methods (Bauch, Becker, & Verhulst, ; Boonekamp, Mulder, Salomons, Dijkstra, & Verhulst, ). However, longitudinal studies in wild populations using a qPCR (quantitative‐PCR) approach across individual lifetimes reported much lower (i.e., 7%–13%) individual repeatability in telomere length (Fairlie et al, ; Spurgin et al, ), indicating that telomeres are highly dynamic over individual lifetimes. Indeed, telomere length can both decrease and increase with age (Bateson & Nettle, ), which has been attributed to measurement error (Steenstrup, Hjelmborg, Kark, Christensen, & Aviv, ) but cannot be explained by measurement error alone (Spurgin et al, ).…”