A meta‐analysis on the heritability of vertebrate telomere length

Chik, Heung Ying Janet; Sparks, Alexandra M.; Schroeder, Julia; Dugdale, Hannah L.

doi:10.1111/jeb.14071

Cited by 24 publications

(26 citation statements)

References 102 publications

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“…Such inconsistency among studies could have a biological explanation, for example being due to stronger selection pressure reducing genetic variation in our population. However, telomere length heritability estimates are also influenced by telomere assay, the statistical methods used to estimate heritability, and potentially age at sampling (14), which differed between these studies. During ageing, telomere length is expected to become less heritable as it becomes increasingly dependent on the environment -e.g.…”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…Estimates for the proportion of additive genetic variance (𝑉𝑉 a ) to total phenotypic variance (𝑉𝑉 t ) -the heritability -range from 0 to 1 among vertebrate studies (14,15). This variation is partly driven by the choice of statistical methods, as commonly applied methods confound genetic and common environmental effects, resulting in inflated heritability estimates (14). Also, the majority of heritability estimates come from laboratory animals of controlled ages and environments, limiting our ability to deduce the roles of selection and evolution under natural conditions (16).…”

Section: Introductionmentioning

confidence: 99%

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Heritability and age-dependent changes in genetic variation of telomere length in a wild house sparrow population

Chik¹,

Sibma²,

Mannarelli³

et al. 2023

Preprint

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Telomeres are a popular biomarker of senescence, as telomere dynamics are linked with survival and lifespan. However, the evolutionary potential of telomere dynamics, and the selection pattern that gives rise to senescence, are not well known. To better understand this, it is necessary to quantify genetic variation in telomere length, and how such variation changes with age. Here, we analysed a longitudinal dataset (2,156 samples from 1,267 individuals across 15 years) from a wild, insular house sparrow (Passer domesticus) population with complete life-history and genetic relatedness data. Using a series of ‘animal’ models, we confirmed that telomere length (TL): (1) changes with age, reflecting senescence in this population. We then showed that (2) TL is repeatable (15.7%, 95% CrI: 10.2–21.0%) and heritable (14.0%, 95% CrI: 8.7–19.5%); and, for the first time in the wild, (3) that TL shows a genotype-by-age interaction, meaning that genotypes differ in their rate of TL change, where additive genetic variance increases at older ages. Our findings provide empirical evidence from a wild population that supports hypotheses explaining the evolution of senescence, and highlights the importance of telomere dynamics as a key biomarker of body physiology for the evolution of senescence.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Heritability and age-dependent changes in genetic variation of telomere length in a wild house sparrow population

Chik¹,

Sibma²,

Mannarelli³

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…Even though our moderators substantially reduced the observed study heterogeneity there was significant residual variation indicating that there are other factors involved that we did not capture in our meta-analysis. Interspecific variation in the heritability of telomere length could be important (Chik et al 2022). Genetic variation appears much smaller for telomere attrition (Bauch et al 2021) but there can be many other non-genetic factors causing variation in telomere attrition.…”

Section: Discussionmentioning

confidence: 99%

Does oxidative stress shorten telomeres in vivo? A meta-analysis

Armstrong

Boonekamp

2022

Preprint

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Telomere attrition is considered a hallmark of ageing. Untangling the proximate causes of telomere attrition may therefore reveal important aspects about the ageing process. In a landmark paper in 2002 Thomas von Zglinicki demonstrated that oxidative stress causes telomere attrition in cell culture. In the next 20 years, oxidative stress became firmly embedded into modern theories of ageing and telomere attrition. However, a recent surge of in vivo studies reveals an inconsistent pattern questioning the unequivocal role of oxidative stress in telomere dynamics, in living organisms. Here we report the results of the first formal meta-analysis on the association between oxidative stress and telomere dynamics in vivo, representing 37 studies, 4,834 individuals, and 18,590 correlational measurements. The overall correlation between oxidative stress markers and telomere dynamics was indistinguishable from zero. This result was independent of the type of oxidative stress marker, telomere dynamic, or taxonomic group. However, telomere measurement method affected the analysis with TRF but not qPCR-based studies showing a significant overall correlation. The correlation was more pronounced in short-lived species and during the adult life phase, when ageing becomes apparent. We then performed an additional meta-analysis of interventional studies (n=7) manipulating oxidative stress. This revealed a significant effect of treatment on telomere dynamics. Our findings indicate that oxidative stress may have a profound effect on telomere dynamics in living organisms fundamentally underpinning the process of ageing.

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“…Heritability estimates of TL vary greatly across species and populations [26,[38][39][40]. However, if TL is measured in adults, it is not clear whether the estimated heritability re ects additive genetic effects (V A ) of TL itself versus V A of individual susceptibility to telomere shortening during their lifetime prior to TL measurement, or both.…”

Section: Introductionmentioning

confidence: 99%

Longitudinal telomere dynamics within natural lifespans of a wild bird

Pepke

Kvalnes

Wright

et al. 2022

Preprint

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Telomeres, the nucleotide sequences that protect the ends of eukaryotic chromosomes, shorten with each cell division and telomere loss may be increased by factors such as oxidative stress. Telomere length (TL) decreases with age in several species, and TL or the change in TL (∆TL) have emerged as biomarkers reflecting experienced stress. In this study, we tracked changes in TL throughout the natural lifespan (from a few months to almost 9 years) of free-living house sparrows (Passer domesticus) in two different island populations. TL was measured in nestlings and subsequently up to 4 times during their lifetime. TL generally decreased with age (senescence), but we also observed instances of telomere lengthening within individuals. We found some evidence for selective disappearance of individuals with shorter telomeres through life. Early-life TL positively predicted later-life TL, but the within-individual repeatability in TL was low (9.2%). Using genetic pedigrees, we found a moderate heritability of ∆TL (h2 = 0.21), which was higher than the heritabilities of early-life TL (h2 = 0.14) and later-life TL measurements (h2 = 0.15). Cohort effects explained considerable proportions of variation in early-life TL (60%), later-life TL (53%), and ∆TL (37%), which suggests persistent impacts of the early-life environment on lifelong telomere dynamics. Individual changes in TL were independent of early-life TL. Finally, there was weak evidence for population differences in ∆TL that may be linked to ecological differences in habitat types. Combined, our results show that individual telomere biology is highly dynamic and influenced by both genetic and environmental variation in natural conditions.

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A meta‐analysis on the heritability of vertebrate telomere length

Cited by 24 publications

References 102 publications

Heritability and age-dependent changes in genetic variation of telomere length in a wild house sparrow population

Heritability and age-dependent changes in genetic variation of telomere length in a wild house sparrow population

Does oxidative stress shorten telomeres in vivo? A meta-analysis

Longitudinal telomere dynamics within natural lifespans of a wild bird

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