Estimation of environmental, genetic and parental age at conception effects on telomere length in a wild mammal

Abstract

Understanding individual variation in fitness‐related traits requires separating the environmental and genetic determinants. Telomeres are protective caps at the ends of chromosomes that are thought to be a biomarker of senescence as their length predicts mortality risk and reflect the physiological consequences of environmental conditions. The relative contribution of genetic and environmental factors to individual variation in telomere length is, however, unclear, yet important for understanding its evolutionary dynamics. In particular, the evidence for transgenerational effects, in terms of parental age at conception, on telomere length is mixed. Here, we investigate the heritability of telomere length, using the ‘animal model’, and parental age at conception effects on offspring telomere length in a wild population of European badgers (Meles meles). Although we found no heritability of telomere length and low evolvability (<0.001), our power to detect heritability was low and a repeatability of 2% across individual lifetimes provides a low upper limit to ordinary narrow‐sense heritability. However, year (32%) and cohort (3%) explained greater proportions of the phenotypic variance in telomere length, excluding qPCR plate and row variances. There was no support for cross‐sectional or within‐individual parental age at conception effects on offspring telomere length. Our results indicate a lack of transgenerational effects through parental age at conception and a low potential for evolutionary change in telomere length in this population. Instead, we provide evidence that individual variation in telomere length is largely driven by environmental variation in this wild mammal.

Genetic architecture and heritability of early-life telomere length in a wild passerine

“…nestling collared flycatchers, Ficedula albicollis(h 2 =0.09, Voillemot et al, 2012), Seychelles warblers (h 2 =0.03-0.08, Sparks et al, 2021) and adult greater mouse-eared bats, Myotis myotis(h 2 =0.01-0.06, Foley et al, 2020), in which TL correlates with several weather variables. These studies also documented considerable year effects on TL (Foley et al, 2020;Sparks et al, 2021) similar to studies finding no heritability of TL in white-throated dippers (Becker et al, 2015) and European badgers (Meles meles , van Lieshout et al, 2021). In comparison, studies based on parent-offspring regression have often found higher TL heritabilities in e.g.…”

“…years, range 1-8 years], n =388 fathers with n =1927 offspring) predicted TL in offspring from Hestmannoy and Traena. We applied within-subject centering (van de Pol & Wright, 2009) to separate within-parental age effects (e.g. senescence) from between-parental age effects (e.g.…”

High heritability of telomere length, but low evolvability, and no significant heritability of telomere shortening in wild jackdaws

“…this study; Benetos et al, 2019;Bichet et al, 2020vs. Foley et al 2020Sparks et al, 2020;van Lieshout et al, 2020;meta-analysis: Kärkkäinen et al in prep). This is of relevance as TL repeatability sets, with exceptions, the upper limit to heritability (Dohm, 2002).…”

Evidence of paternal effects on telomere length increases in early-life

“…While telomere lengths in offspring have been shown to be affected by an offspring's environment (Dugdale and Richardson, 2018;Lieshout et al, 2021), effects of paternal age in birds have been found to be independent of this (Bauch et al, 2019;Boonekamp et al, 2014). As such, overall, there is growing support for at least contributory paternal inheritance of telomere length in some species of birds (Bouwhuis et al, 2018;Olsson et al, 2011;this study).…”