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'.

Keywords: animal models; environmental effects; genetic effects; heritability; telomeres; variation.

Figure 1.

Hypothetical proportion of telomere length variation among individuals explained by genetic (blue) and environmental (green) effects: (a) in a population where individuals experience: (1) highly variable environments versus (2) relatively constant environments; and (b) estimated using mixed models of increasing complexity, based on repeated measures of telomere length per individual: model (3) a mixed model to separate individual variation from environmental (residual) variation, model (4) an ‘animal’ model where individual variation is separated into additive genetic and permanent environmental effects, and model (5) where maternal identity is included to estimate maternal effects.

Figure 2.

Relative telomere length (RTL) among cohorts in relation to age in Seychelles warblers, Acrocephalus sechellensis. Lines represent fitted values from a linear regression of RTL and log-transformed age. Colours represent birth years (1993–2014). Adapted from [30].

Figure 3.

Leukocyte telomere length (LTL) dynamics for 11 female Soay sheep, Ovis aries, measured twice as lambs and at least six further times thereafter during their lives. Each colour and symbol combination represents a different individual. Adapted from [20].