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

Alexandra M Sparks,Marco Van Der Velde,Terry Burke,Hannah L Dugdale,Jan Komdeur,David S Richardson,Eleanor A Fairfield,Lewis G Spurgin

doi:10.1111/mec.15804

Abstract

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. Heritability of telomere length has primarily been calculated using parent-offspring regression which can be confounded by shared environments. To control for confounding variables, quantitative genetic "animal models" can be used, but few studies have applied animal models in wild populations. Furthermore, parental age at conception may also influence offspring telomere length, but most studies have been cross-sectional. We investigated within- and between-parental age at conception effects and heritability of telomere length in the Seychelles warbler using measures from birds caught over 20years and a multigenerational 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). Animal models provided evidence that heritability and evolvability of telomere length were low in this population, and that variation in telomere length was not driven by early-life effects of hatch period or parental identities. Quantitative polymerase chain reaction plate had a large influence on telomere length variation and not accounting for it in the models would have underestimated heritability. Our study illustrates the need to include and account for technical variation in order to accurately estimate heritability, as well as other environmental effects, on telomere length in natural populations.

Highlights

A complete understanding of the relative impact of genetic and environmental effects on senescence requires quantifying individual variation in senescence, but this is difficult to achieve, for instance because it can be difficult to quantify the costs of different conditions experienced, especially in wild populations (Nussey et al, 2008; de Pol & Verhulst, 2006; van Charmantier et al, 2014)
Maternal and paternal age at conception (MAC and PAC, respectively) were not significantly associated with offspring relative telomere length (RTL) when using telomere lengths across all ages, or when the data set was restricted to the first offspring measurements taken as nestlings, or when all measurements were taken from juvenile offspring (
When parental age at conception effects were separated into within-vs. between-parental age effects for lifelong RTL, there was a significant negative within-paternal age effect and a significant positive between-maternal age effect

Summary

Introduction

A complete understanding of the relative impact of genetic and environmental effects on senescence requires quantifying individual variation in senescence, but this is difficult to achieve, for instance because it can be difficult to quantify the costs of different conditions experienced, especially in wild populations (Nussey et al, 2008; de Pol & Verhulst, 2006; van Charmantier et al, 2014). The identification of biomarkers, such as telomeres that reflect an individual's intrinsic state and mortality risk (Wilbourn et al, 2018), can shed light on the candidate mechanisms underlying senescence (Nakagawa et al, 2004). Whether causal, or just correlational (Simons, 2015; Young, 2018), telomere length relative to age positively predicts health (Blackburn et al, 2015; Boonekamp et al, 2013) and survival/lifespan within species (Barrett et al, 2013; Wilbourn et al, 2018). Telomeres are increasingly used in evolutionary ecology studies as a biomarker of senescence and to measure an individual's physiological response to their environmental experiences (Bauch et al, 2013; Bebbington et al, 2016; Bize et al, 2009; Fairlie et al, 2016)

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