Decline in telomere length with increasing age across nonhuman vertebrates: A meta‐analysis

Abstract

The prediction that telomere length (TL) shortens with increasing age is a major element in considering the role of telomeres as a key player in evolution. While telomere attrition is found in humans both in vitro and in vivo, the increasing number of studies reporting diverse age-specific patterns of TL challenges the hypothesis of a universal decline of TL with increasing age. Here we performed a meta-analysis to estimate the relationship between TL and age across 175 estimates encompassing 98 species of vertebrates. We found that, on average, TL does decline with increasing age during adulthood. However, this decline was weak and variable across vertebrate classes, and we also found evidence for a publication bias that might weaken our current evidence of decreasing TL with increasing age. We found no evidence for a faster decline in TL with increasing age when considering the juvenile stage (from birth to age at first reproduction) compared to the adult stage. Heterogeneity in TL ageing rates was explained by the method used to measure telomeres: detectable TL declines with increasing age were found only among studies using TRF with in-gel hybridisation and qFISH methods, but not in studies using qPCR and Southern blot-based TRF methods. While we confirmed that TL declines with increasing age in most adult vertebrates, our results identify an influence of telomere measurement methodology, which highlights the need to examine more thoroughly the effect of the method of measurement on TL estimates.

Two aspects of longevity are associated with the rate of loss of telomeres in birds

“…In the present study, we focused on 30 species for which adult telomere length, TROC, and life history variables were all recorded. For these species, telomere lengths were estimated in kilobases (kb) using electrophoretic separation of telomere restriction fragments or by quantitative fluorescent in situ hybridization (respectively, TRF and Q-FISH; Remot et al 2021). All studies used samples of erythrocytes.…”

“…Thus, we estimated TROC only from samples of adult birds. A further problem is that some estimates of telomere length measure only DNA sequences of the terminal telomere repeats, whereas other methods include DNA sequences from the body of the chromosome (Remot et al 2021). We restricted our analyses to those studies that used the former methods and thus produced the best estimates of telomere lengths.…”

Integrating telomere biology into the ecology and evolution of natural populations: progress and prospects

“…The approach of will hopefully be followed by others, potentially using existing selection experiments on growth and body size. Though to fully understand the results it may be important to also know more about cell division rates and growth patterns in the individuals attaining different body sizes While the general pattern from human studies is that telomeres shorten with age, findings in other species, including those in this special issue mentioned earlier in relation to stress exposure, suggest that this is not always the case (meta-analysed by Remot et al 2021 in this issue). For example, there is evidence of telomere elongation in some hibernating mammals and snakes (Olsson 2018).…”

Telomeres and anthropogenic disturbances in wildlife: A systematic review and meta‐analysis

“…In addition, their biological implications at the organismal level remain unclear. Other biological characteristics, such as the change with age or the withinindividual repeatability, have also been shown to be sensitive to the method employed in telomere estimation (Atema et al, 2019;Kärkkäinen et al, 2021;Remot et al, 2021). Therefore, these technical limitations could influence any inferences about past stress exposure or future long-term consequences for a given telomere length if not considered beforehand.…”