Ectothermic telomeres: it's time they came in from the cold

Abstract

We review the evolutionary ecology and genetics of telomeres in taxa that cannot elevate their body temperature to a preferred level through metabolism but do so by basking or seeking out a warm environment. This group of organisms contains all living things on earth, apart from birds and mammals. One reason for our interest in this synthetic group is the argument that high, stable body temperature increases the risk of malignant tumours if long, telomerase-restored telomeres make cells ‘live forever’. If this holds true, ectotherms should have significantly lower cancer frequencies. We discuss to what degree there is support for this ‘anti-cancer’ hypothesis in the current literature. Importantly, we suggest that ectothermic taxa, with variation in somatic telomerase expression across tissue and taxa, may hold the key to understanding ongoing selection and evolution of telomerase dynamics in the wild. We further review endotherm-specific effects of growth on telomeres, effects of autotomy (‘tail dropping’) on telomere attrition, and costs of maintaining sexual displays measured in telomere attrition. Finally, we cover plant ectotherm telomeres and life histories in a separate ‘mini review’.This article is part of the theme issue ‘Understanding diversity in telomere dynamics'.

Maternal predator‐exposure affects offspring size at birth but not telomere length in a live‐bearing fish

“…In the great reed warblers, Acrocephalus arundinaceus , it has also been found a strong maternal effect on offspring telomere length at birth (Asghar et al, ), but the possible underlying factors are unknown. Opposite to our results, in the Atlantic salmon ( Salmo salar ) a significant paternal but not maternal effect on offspring telomere length has been found (McLennan et al, ) confirming the extreme variation in telomere dynamics among teleosts (Olsson et al, ). Finally, we found that newborn guppies have longer telomeres than their mothers.…”

“…Telomeric nucleotide repeats shorten at each cell cycle until telomeres reach a critical size and ultimately limit cell growth (Shay & Wright, ). This entails for the observed telomere shortening with age in both mammals and birds (Haussmann et al, ), while studies on ectotherms have yielded mixed results (Hartmann et al, ; Hatakeyama et al, ; Lund, Glass, Tolar, & Blazar, ; reviewed in Olsson, Wapstra, & Friesen, ). Telomeres are particularly susceptible to oxidative damages because of their high guanine content (Monaghan, ); thus, oxidative stress is thought to be the most relevant cause of telomere attrition in wild vertebrates (Haussmann & Marchetto, ; von Zglinicki, ).…”

“…Barnes, Fouquerel, & Opresko, 2019;Chatelain, Drobniak, & Szulkin, 2020;Epel et al, 2004;Kotrschal, Ilmonen, & Penn, 2007;Reichert & Stier, 2017), which in turn may increase aging rate and hence shortening life span (Heidinger et al, 2012;Wilbourn et al, 2018). Despite the increasing interest in studying telomere dynamics (Monaghan, Eisenberg, Harrington, & Nussey, 2018), the effect of environmental stress on telomere attrition in ectotherms is still largely unknown (Angelier, Costantini, Blévin, & Chastel, 2018;Chatelain et al, 2020;Olsson et al, 2018). One reason why understanding telomere dynamics is often difficult is that maternal effects are known to affect offspring phenotype including offspring telomere length (Asghar, Bensch, Tarka, Hansson, & Hasselquist, 2015;Haussmann & Heidinger, 2015;Marasco, Boner, Griffiths, Heidinger, & Monaghan, 2019) which, along with environmental stressors, determines the subsequent telomere dynamic in the adulthood (Heidinger et al, 2012).…”

Carry‐over effects of early thermal conditions on somatic and germline oxidative damages are mediated by compensatory growth in sticklebacks

“…antioxidant, catch-up growth, climate change, oxidative damage, sperm, stickleback, telomere However, similar studies in ectotherms are limited and report contrasting results with both increases and decreases of telomere length after stress exposure (reviewed in Olsson, Wapstra, & Friesen, 2018).…”

Understanding diversity in telomere dynamics

“…Indeed, the range of taxa for which telomere data are available in healthy individuals remains very limited, and is biased towards the endothermic vertebrates, the birds and mammals. The paper by Olsson et al [21] draws attention to this shortcoming in the literature and points out how much we have to gain from studies of ectotherms, both in deepening our knowledge of diversity in telomere dynamics, and in the context of understanding the costs and benefits of telomere restoration in tissue regeneration and disease prevention.…”