Longer telomeres during early life predict higher lifetime reproductive success in females but not males

Heidinger, Britt J.; Kucera, A; Kittilson, Jeff D; Westneat, David F.

doi:10.1098/rspb.2021.0560

Cited by 40 publications

(75 citation statements)

References 57 publications

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“…Based on duplicates of the same sample the sample repeatability of the T/S ratios at 0.5 months was 0.98 (95% confidence interval: 0.97, 0.99), and at 3 months it was 0.99 (95% confidence interval: 0.99, 0.99). The individual repeatability of T/S ratios between the two time points was 0.27 (95% confidence interval: 0.01, 0.51), a similar value to the early life telomere length repeatability estimated by Heidinger et al (2021) (r = 0.28, range 0.18–0.5). All samples were analysed for telomere length at the same time and had a similar shelf time ( Lieshout et al, 2020 ).…”

Section: Methodssupporting

confidence: 71%

“…Other studies find this effect only in relation to older mothers ( Asghar et al, 2015 ), or fathers ( Horn et al, 2011 ; Noguera et al, 2018 ; Sparks et al, 2021 ). Another body of studies find a positive relationship between parental age and early life telomere lengths in offspring (fathers: Heidinger et al, 2021 ; mothers: Sparks et al, 2021 ). Consequently there is a great need for additional studies investigating the complexities of the relationship between parental ages and offspring telomere lengths.…”

Section: Introductionmentioning

confidence: 99%

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Evidence of Paternal Effects on Telomere Length Increases in Early Life

et al. 2022

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Offspring of older parents in many species have decreased longevity, a faster ageing rate and lower fecundity than offspring born to younger parents. Biomarkers of ageing, such as telomeres, that tend to shorten as individuals age, may provide insight into the mechanisms of such parental age effects. Parental age may be associated with offspring telomere length either directly through inheritance of shortened telomeres or indirectly, for example, through changes in parental care in older parents affecting offspring telomere length. Across the literature there is considerable variation in estimates of the heritability of telomere length, and in the direction and extent of parental age effects on telomere length. To address this, we experimentally tested how parental age is associated with the early-life telomere dynamics of chicks at two time points in a captive population of house sparrows Passer domesticus. We experimentally separated parental age from sex effects, and removed effects of age-assortative mating, by allowing the parent birds to only mate with young, or old partners. The effect of parental age was dependent on the sex of the parent and the chicks, and was found in the father-daughter relationship only; older fathers produced daughters with longer telomere lengths post-fledging. Overall we found that chick telomere length increased between the age of 0.5 and 3 months at the population and individual level. This finding is unusual in birds with such increases more commonly associated with non-avian taxa. Our results suggest parental age effects on telomere length are sex-specific either through indirect or direct inheritance. The study of similar patterns in different species and taxa will help us further understand variation in telomere length and its evolution.

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Section: Methodssupporting

confidence: 71%

Section: Introductionmentioning

confidence: 99%

Evidence of Paternal Effects on Telomere Length Increases in Early Life

et al. 2022

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“…However, they found a positive relationship between early-life TL and lifespan in females, but a negative trend between TL and lifespan in males. They therefore suggested that TL reflected differences in quality or condition in females, but did not predict pace-of-life (Heidinger et al, 2021). It will be interesting to see if other studies find contrasting associations between TL and fitness across different populations within the same species in the wild.…”

Section: Discussionmentioning

confidence: 98%

“…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

Preprint

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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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“…Short telomeres can trigger apoptosis and telomere attrition is considered a hallmark of aging (López-Otín, Blasco, Partridge, Serrano, & Kroemer, 2013), although the causal involvement of telomere shortening in organismal senescence is not well understood (Simons, 2015). However, telomere length (TL) may reflect the cumulative stress experienced by an individual (Bateson, 2016;Monaghan, 2014), and TL or TL shortening are associated with health or fitness in several species (Barrett, Burke, Hammers, Komdeur, & Richardson, 2013;Chatelain, Drobniak, & Szulkin, 2020;Froy et al, 2021;Heidinger, Kucera, Kittilson, & Westneat, 2021;Wilbourn et al, 2018). Thus, TL is increasingly used as a biomarker of somatic integrity in studies of physiological or evolutionary ecology (Bateson & Poirier, 2019;Haussmann, 2010;Pepper, Bateson, & Nettle, 2018;Young, 2018).…”

Section: Introductionmentioning

confidence: 99%

Inbreeding is associated with shorter early-life telomere length in a wild passerine

Pepke

Niskanen

Kvalnes

et al. 2021

Preprint

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Inbreeding can have negative effects on survival and reproduction, which may be of conservation concern in small and isolated populations. However, the physiological mechanisms underlying inbreeding depression are not well-known. The length of telomeres, the DNA sequences protecting chromosome ends, has been associated with health or fitness in several species. We investigated effects of inbreeding on early-life telomere length in two small island populations of wild house sparrows (Passer domesticus) known to be affected by inbreeding depression. Using genomic and pedigree-based measures of inbreeding we found that inbred nestling house sparrows have shorter telomeres. This negative effect of inbreeding on telomere length may have been complemented by a heterosis effect resulting in longer telomeres in individuals that were less inbred than the population average. Furthermore, we found some evidence of stronger effects of inbreeding on telomere length in males than females. Thus, telomere length may reveal subtle costs of inbreeding in the wild and demonstrate a route by which inbreeding negatively impacts the physiological state of an organism already at early life-history stages.

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Longer telomeres during early life predict higher lifetime reproductive success in females but not males

Cited by 40 publications

References 57 publications

Evidence of Paternal Effects on Telomere Length Increases in Early Life

Evidence of Paternal Effects on Telomere Length Increases in Early Life

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

Inbreeding is associated with shorter early-life telomere length in a wild passerine

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