Heritable variation in telomere length predicts mortality in Soay sheep

Froy, Hannah; Underwood, Sarah; Dorrens, Jennifer; Seeker, Luise A.; Watt, Kathryn; Wilbourn, Rachael V.; Pilkington, Jill G.; Harrington, Lea; Pemberton, Josephine M.; Nussey, Daniel H.

doi:10.1073/pnas.2020563118

Cited by 38 publications

(79 citation statements)

References 68 publications

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“…1b). The activity of telomerase is often downregulated after birth, which likely explains the negative relationship between telomere length and age observed across taxa (Olsson et al 2011, Heidinger et al 2012, Louzon et al 2020, Sánchez‐Montes et al 2020, Froy et al 2021), although this pattern might not be universal (Hoelzl et al 2016, Ujvari et al 2017). As discussed below, the rate of telomere shortening is often increased under energy‐demanding processes that involve allocation of resources from telomere maintenance to other functions.…”

Section: The Use Of Telomeres In Eco‐evolutionary Studiesmentioning

confidence: 99%

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

2021

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Ageing refers to the loss of organismal functionality with age, a process that is characterised by decreased reproduction and survival probability. In natural populations, it is expected that environmental conditions influence an individual's ageing trajectory. Understanding the role of environmental heterogeneity on ageing variation could provide critical insights into population resilience and species distribution but remains overlooked. Telomeres, the end cap of chromosomes, are a promising integrative physiological marker of an individual's health and a possible proxy to aid the understanding of variation in ageing trajectories. Here, we review the existing information on telomere length and its dynamics in wild populations distributed across spatial scales. Despite a relative scarcity of information, there is evidence for divergence in telomere length between populations facing contrasting environments. Nonetheless, a higher spatial resolution and temporal replication are needed to fully understand the role that environmental conditions play on telomere length variation. Since most of the existing studies are correlational, future field and laboratory experiments are required. For the first time, we demonstrate the use of population telomere data to predict species habitat suitability through species distribution models (SDMs). This represents a promising new research area in the study of ageing pattern variation in wild populations. Furthermore, the inclusion of telomere data in future physiological SDMs may improve our understanding of species distribution and population resilience. However, the use of telomeres within this context could be limited if no previous knowledge on the relevance of telomeres as markers of health and survival at the species level is available. Finally, we suggest some key practical and theoretical considerations that, ideally, future studies combining biogeographic and telomere data should pay attention.

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Section: The Use Of Telomeres In Eco‐evolutionary Studiesmentioning

confidence: 99%

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

2021

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“…This suggests a mechanistic link between environmental change and physiological change mediated by TL dynamics in early-life (Chatelain et al, 2020;Giraudeau et al, 2019a). TL has been shown to be associated with important components of fitness in some wild species (Eastwood et al, 2019;Froy et al, 2021;van Lieshout et al, 2019;Wilbourn et al, 2018). However, we found little evidence that variation in TL in early life had any fitness consequences in terms of survival, but there was a tendency for a negative effect of TL on reproductive success (Tables S2.4-2.6).…”

Section: Discussionmentioning

confidence: 64%

“…In several species, longer TL is associated with higher survival (Bichet et al, 2020;Crocco et al, 2021;Eastwood et al, 2019;Froy et al, 2021;Heidinger et al, 2021;Ilska-Warner et al, 2019;van Lieshout et al, 2021;Wilbourn et al, 2018, but see Vedder et al, 2017. We found no evidence for an association between TL and first-year survival or mortality over the lifespan in house sparrows (Figs.…”

Section: Discussionmentioning

confidence: 99%

Causes and consequences of variation in early-life telomere length in a bird metapopulation

Pepke¹,

Kvalnes²,

Ranke³

et al. 2021

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1.Environmental conditions during early-life development can have lasting effects on individual quality and fitness. Telomere length (TL) may correlate with early-life conditions and may be an important mediator or biomarker of individual quality or pace-of-life, as periods of increased energy demands can increase telomere attrition due to oxidative stress. Thus, knowledge of the mechanisms that generate variation in TL, and the relation between TL and fitness, is important in understanding the role of telomeres in ecology and life-history evolution. 2.Here, we investigate how environmental conditions and morphological traits are associated with early-life TL and if TL predicts natal dispersal probability or components of fitness in two populations of wild house sparrows (Passer domesticus). 3.We measured morphological traits and blood TL in 2746 nestlings from 20 cohorts (1994-2013) and retrieved data on weather conditions. We monitored population fluctuations, and individual survival and reproductive output using field observations and genetic pedigrees. We then used generalized linear mixed-effects models to test which factors affected TL in early-life, and if TL predicted dispersal propensity, or was associated with recruitment probability, mortality risk, or reproductive success.4.We found a negative effect of population density on TL, but only in one of the populations. There was a curvilinear association between TL and the maximum daily North Atlantic Oscillation (NAO) index during incubation, suggesting that there are optimal weather conditions that result in the longest TL. Dispersers tended to have shorter telomeres than non-dispersers. TL did not predict survival, but we found a tendency for individuals with short telomeres to have higher annual reproductive success.5.Our study showed how early-life TL is shaped by effects of growth, weather conditions and population density, supporting that environmental stressors negatively affect TL in wild populations. In addition, TL may be a mediator or biomarker of individual pace-of-life, with higher dispersal rates and annual reproduction tending to be associated with shorter early-life TL in this study. However, clear associations between early-life TL and individual fitness seems difficult to establish and may differ between different populations in the wild.

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“…Bivariate models allow estimation of variance for each of the two focal response variables, as well as estimation of the covariance between them at different hierarchical levels (Froy et al, 2019(Froy et al, , 2021.…”

Section: Bivariate Analysesmentioning

confidence: 99%

The association between female reproductive performance and leukocyte telomere length in wild Soay sheep

et al. 2021

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Telomere length (TL), typically measured across a sample of blood cells, has emerged as an exciting potential marker of physiological state and of the costs of investment in growth and reproduction within evolutionary ecology. While there is mounting evidence from studies of wild vertebrates that short TL predicts raised subsequent mortality risk, the relationship between reproductive investment and TL is less clear cut, and previous studies report both negative and positive associations. In this study, we examined the relationship between TL and different aspects of maternal reproductive performance in a free-living population of Soay sheep. We find evidence for shorter TL in females that bred, and thus paid any costs of gestation, compared to females that did not breed. However, we found no evidence for any association between TL and litter size. Furthermore, females that invested in gestation and lactation actually had longer TL than females who only invested in gestation because their offspring died shortly after birth. We used multivariate models to decompose these associations into among-and within-individual effects, and discovered that within-individual effects were driving both the negative association between TL and gestation, and the positive association between TL and lactation. This suggests that telomere dynamics may reflect recent physiologically costly investment or variation in physiological condition, depending on the aspect of reproduction being investigated. Our results highlight the physiological complexity of vertebrate reproduction, and the need to better understand how and why different aspects of physiological variation underpinning life histories impact blood cell TL.

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Heritable variation in telomere length predicts mortality in Soay sheep

Cited by 38 publications

References 68 publications

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

Causes and consequences of variation in early-life telomere length in a bird metapopulation

The association between female reproductive performance and leukocyte telomere length in wild Soay sheep

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