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

Abstract

Human-driven environmental changes are affecting wildlife across the globe. These challenges do not influence species or populations to the same extent and therefore a comprehensive evaluation of organismal health is needed to determine their ultimate impact. Evidence suggests that telomeres (the terminal chromosomal regions) are sensitive to environmental conditions and have been posited as a surrogate for animal health and fitness. Evaluation of their use in an applied ecological context is still scarce. Here, using information from molecular and occupational biomedical studies, we aim to provide ecologists and evolutionary biologists with an accessible synthesis of the links between human disturbances and telomere length. In addition, we perform a systematic review and meta-analysis on studies measuring telomere length in wild/wild-derived animals facing anthropogenic disturbances. Despite the relatively small number of studies to date, our meta-analysis revealed a significant small negative association between disturbances and telomere length (−0.092 [−0.153, −0.031]; n = 28; k = 159). Yet, our systematic review suggests that the use of telomeres as a biomarker to understand the anthropogenic impact on wildlife is limited. We propose some research avenues that will help to broadly evaluate their suitability: (i) further causal studies on the link between human disturbances and telomeres; (ii) investigating the organismal implications, in terms of fitness and performance, of a given telomere length in anthropogenically disturbed scenarios; and (iii) better understanding of the underlying mechanisms of telomere dynamics. Future studies in these facets will help to ultimately determine their role as markers of health and fitness in wildlife facing anthropogenic disturbances.

Higher mercury contamination is associated with shorter telomeres in a long-lived seabird – A direct effect or a consequence of among-individual variation in phenotypic quality?

“…Note also that this scenario may apply more generally to the many pollutants to which seabirds or top predators are exposed, or that an accumulation of different pollutants could amplify the effect. For mercury as for other environmental pollutants, telomeres are promising biomarkers for contamination effects (seabirds: Blévin et al, 2016;Blévin et al, 2017; this study; reviewed across taxa in Salmón and Burraco, 2022).…”

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

“…In this context telomere measurements have the potential advantage over many other biomarkers of representing a potential fitness proxy, allowing effects to be studied over a time scale that could be much shorter than required to measure actual fitness consequences. In line with this, Salmón and Burraco (2022) evaluated the use of changes in telomere dynamics as a way of assessing such anthropogenic impacts, providing an exhaustive literature review and meta-analysis. Oxidative stress induced by internal and external factors can be a major cause of DNA damage which could increase telomere attrition.…”

Editorial 2023

“…The first few manuscripts in this issue provide essential background information, examining the different telomere dynamics among species and across life stages (Brown et al, 2022; Remot et al, 2022) and providing a framework for ecological and evolutionary hypotheses around telomeres (Tobler et al, 2022). The second set of manuscripts explores the effects of ecological and environmental stressors on telomere dynamics, suggesting that telomeres, serving as a proxy for fitness consequences, might be used for conservation monitoring (Salmón & Burraco, 2022). These studies show the critical impacts of stress during early‐life stages (Sheldon, Eastwood, et al, 2022; van Lieshout et al, 2022) and the presence of among‐individual variation in telomeric response to stress (Brown et al, 2022; Kärkkäinen, Laaksonen, et al, 2022; Reichard et al, 2022).…”