Heritability of telomere variation: it is all about the environment!

Abstract

Individual differences in telomere length have been linked to survival and senescence. Understanding the heritability of telomere length can provide important insight into individual differences and facilitate our understanding of the evolution of telomeres. However, to gain accurate and meaningful estimates of telomere heritability it is vital that the impact of the environment, and how this may vary, is understood and accounted for. The aim of this review is to raise awareness of this important, but much under-appreciated point. We outline the factors known to impact telomere length and discuss the fact that telomere length is a trait that changes with age. We highlight statistical methods that can separate genetic from environmental effects and control for confounding variables. We then review how well previous studies in vertebrate populations including humans have taken these factors into account. We argue that studies to date either use methodological techniques that confound environmental and genetic effects, or use appropriate methods but lack sufficient power to fully separate these components. We discuss potential solutions. We conclude that we need larger studies, which also span longer time periods, to account for changing environmental effects, if we are to determine meaningful estimates of the genetic component of telomere length.This article is part of the theme issue ‘Understanding diversity in telomere dynamics'.

Individual variation in early‐life telomere length and survival in a wild mammal

“…As well as environmental effects, variation in early‐life RLTL can also be caused by additive genetic effects (Dugdale & Richardson, ). In wild populations, using a quantitative genetic animal model, no heritability of telomere length was found in white‐throated dippers ( Cinclus cinclus ; Becker et al, ), and high heritability (0.35–0.48) was found in the great reed warbler (Acrocephalus arundinaceus ; Asghar, Bensch, et al, ).…”

Telomere attrition predicts reduced survival in a wild social bird, but short telomeres do not

“…Telomere attrition could effectively capture declines in SI, but fail to manifest as an evident relationship between telomere length and SI (and hence survival) due to unrelated sources of among‐individual variation in telomere length (see Boonekamp et al, for similar logic). For example, among‐individual variation in telomere length, particularly in early life, could be a product in part of genetic and/or epigenetic sources of variation in “initial” telomere length at conception and (in studies such as ours that assess telomere length using qPCR) among‐individual variation in the incidence of interstitial telomeric repeats (Delany et al, ; Dugdale & Richardson, ; Eisenberg & Kuzawa, ). Indeed, while such sources of variation in telomere length could conceivably obscure relationships between telomere length per se and survival, it is also worth noting their potential to artificially generate such relationships (if a source of variation in an offspring's “initial” telomere length independently impacts their downstream survival, such as might be imagined for parental age effects).…”

Ultralong telomeres shorten with age in nestling great tits but are static in adults and mask attrition of short telomeres

“…Telomeres are noncoding DNA repeats forming the end‐caps of linear chromosomes, thereby safeguarding chromosome integrity (Blackburn, ). TL is to a large extent genetically determined, although heritability estimates vary widely between studies (range h 2 : 0–1; overviews in Atema et al, ; Dugdale, Richardson, & Richardson, ). TL generally shortens with age, and telomere shortening is accelerated by environmental challenges (Boonekamp, Mulder, Salomons, Dijkstra, & Verhulst, ; Reichert et al, ; Watson, Bolton, & Monaghan, ), reproductive effort (Bauch, Becker, & Verhulst, ), stress during adulthood (Hau et al, ) and disease (Asghar et al, ; Beirne, Delahay, Hares, & Young, ), and can differ between habitats (Angelier, Vleck, Holberton, & Marra, ; Stier et al, ).…”