Estimation of environmental and genetic contributions to telomere length variation in a wild mammal

Lieshout, Sil H. J. van; Sparks, Alexandra M.; Bretman, Amanda; Newman, Chris; Buesching, Christina D.; Burke, Terry; Macdonald, David W.; Dugdale, Hannah L.

doi:10.32942/osf.io/s5dnr

Cited by 2 publications

(5 citation statements)

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“…2) represents evidence for an appreciable genetic contribution to variation in TL in a wild mammal. Recent studies in wild badgers and bats have used similar pedigree-based "animal models" but found both the repeatability and heritability of TL to be negligible (36,37). Our estimate was lower than in a recent longitudinal study of farmed dairy cattle [32-38% ( 38)], which is unsurprising given the expectation of reduced environmental variation in livestock compared to wild systems.…”

Section: Discussioncontrasting

confidence: 60%

Heritable variation in telomere length predicts mortality in Soay sheep

Froy

Underwood

Dorrens

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Telomere length (TL) is considered an important biomarker of whole-organism health and aging. Across humans and other vertebrates, short telomeres are associated with increased subsequent mortality risk, but the processes responsible for this correlation remain uncertain. A key unanswered question is whether TL–mortality associations arise due to positive effects of genes or early-life environment on both an individual’s average lifetime TL and their longevity, or due to more immediate effects of environmental stressors on within-individual TL loss and increased mortality risk. Addressing this question requires longitudinal TL and life history data across the entire lifetimes of many individuals, which are difficult to obtain for long-lived species like humans. Using longitudinal data and samples collected over nearly two decades, as part of a long-term study of wild Soay sheep, we dissected an observed positive association between TL and subsequent survival using multivariate quantitative genetic models. We found no evidence that telomere attrition was associated with increased mortality risk, suggesting that TL is not an important marker of biological aging or exposure to environmental stress in our study system. Instead, we find that among-individual differences in average TL are associated with increased lifespan. Our analyses suggest that this correlation between an individual’s average TL and lifespan has a genetic basis. This demonstrates that TL has the potential to evolve under natural conditions, and suggests an important role of genetics underlying the widespread observation that short telomeres predict mortality.

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Section: Discussioncontrasting

confidence: 60%

Heritable variation in telomere length predicts mortality in Soay sheep

Froy

Underwood

Dorrens

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…Furthermore, many studies have documented no parental age at conception effects (Heidinger et al 2016;Froy et al 2017;McLennan et al 2018;Belmaker et al 2019;van Lieshout et al 2020a), while one study found a positive maternal but no paternal age at conception effect (Asghar et al 2015). In studies investigating telomere heritability, only one has controlled for parental age at conception effects (Asghar et al 2015).…”

Section: Discussionmentioning

confidence: 99%

“…Heritabilities can be re-evaluated with the total phenotypic variance excluding any technical variance to reflect true biological variance (de Villemereuil et al 2018). Measurement error in qPCR studies could come from various factors such as between-and within-plate effects, technician, storage time, changes in reagents and extraction method effects (Eisenberg et al 2015;Seeker et al 2016;Reichert et al 2017;van Lieshout et al 2020b). Such measurement error should be incorporated into analyses and reported to prevent it from biasing results (Nettle et al 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Such measurement error should be incorporated into analyses and reported to prevent it from biasing results (Nettle et al 2019). Further, future studies should ensure samples on plates reflect multiple years and ages to enable the greatest statistical power to separate variances of technical and biological interest (van Lieshout et al 2020b).…”

Section: Discussionmentioning

confidence: 99%

“…An alternative (not mutually exclusive) hypothesis is the selective survival or proliferation of germ stem cells with longer telomeres (Kimura et al 2008;Hjelmborg et al 2015). However, studies in non-human vertebrates, including a longitudinal study in jackdaws (Bauch et al 2019), report conflicting results; while some have also found a positive correlation between offspring telomere length and paternal (Eisenberg et al 2017) or maternal age (Asghar et al 2015), others have found negative paternal age correlations (Olsson et al 2011;de Frutos et al 2016;Criscuolo et al 2017;Bouwhuis et al 2018;Noguera et al 2018;Bauch et al 2019) or no parental age effects (Heidinger et al 2016;Froy et al 2017;McLennan et al 2018;Belmaker et al 2019;van Lieshout et al 2020a). Work on a wider range of species, using longitudinal data, is required to identify the drivers of variation in parental age at conception effects.…”

Section: Introductionmentioning

confidence: 99%

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Telomere heritability and parental age at conception effects in a wild avian population

Sparks¹,

Spurgin²,

Velde³

et al. 2020

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Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. In previous studies, heritability of telomere length has primarily been calculated using parent-offspring regression, but shared environments can confound such estimates. Furthermore, associations with age and parental age at conception effects are typically not accounted for but can also bias heritability estimates. To control for these confounding variables, quantitative genetic ‘animal models’ can be used. However, the few studies on wild populations using this approach have been restricted by power. Here, we investigated the heritability of telomere length and parental age at conception effects in the Seychelles warbler using 2664 telomere length measures from 1318 birds over 20 years and a multi-generational pedigree. We found a weak negative within-paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between-maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). While parent–offspring regressions did not detect heritability, animal models provided evidence that heritability of telomere length was low in this population. Environmental and technical variation largely influenced telomere length and would have biased heritability estimates if unaccounted for. Estimating the heritability of telomere length is complex, requiring large sample sizes and accounting for confounding effects in order to improve our understanding of the evolutionary potential of telomere length in the wild.

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Estimation of environmental and genetic contributions to telomere length variation in a wild mammal

Cited by 2 publications

References 94 publications

Heritable variation in telomere length predicts mortality in Soay sheep

Heritable variation in telomere length predicts mortality in Soay sheep

Telomere heritability and parental age at conception effects in a wild avian population

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