Ageing across the great divide: tissue transformation, organismal growth and temperature shape telomere dynamics through the metamorphic transition

Abstract

Telomere attrition is considered a useful indicator of cellular and whole-organism ageing rate. While approximately 80% of animal species undergo metamorphosis that includes extensive tissue transformations (involving cell division, apoptosis, de-differentiation and de novo formation of stem cells), the effect on telomere dynamics is unknown. We measured telomeres in Xenopus laevis developing from larvae to adults under contrasting environmental temperatures . Telomere dynamics were linked to the degree of tissue transformation during development. Average telomere length in gut tissue increased dramatically during metamorphosis, when the gut shortens by 75% and epithelial cells de-differentiate into stem cells. In the liver (retained from larva) and hindlimb muscle (newly formed before metamorphosis), telomeres gradually shortened until adulthood, likely due to extensive cell division. Tail muscle telomere lengths were constant until tail resorption, and those in heart (retained from larva) showed no change over time. Telomere lengths negatively correlated with larval growth, but for a given growth rate, telomeres were shorter in cooler conditions, suggesting that growing in the cold is more costly. Telomere lengths were not related to post-metamorphic growth rate. Further research is now needed to understand whether telomere dynamics are a good indicator of ageing rate in species undergoing metamorphosis.

Ionizing radiation has negligible effects on the age, telomere length, and corticosterone levels of Chornobyl tree frogs

“…Likewise, Chornobyl tree frogs with high dose rates do not experience higher lipid peroxidation levels [31], which may indicate physiological compensatory responses to radiation, similar to those observed in other amphibians coping with detrimental conditions earlier in their life [59]. We should also notice that we measured telomere length in the hindlimb muscle of frogs, but telomere dynamics can be tissue-specific in amphibians and other vertebrates [23,60,61]. Indeed, telomere dynamics differ across tissues in bank voles from the Chornobyl Exclusion Zone [23].…”

Influence of breed and environment on leukocyte telomere length in cattle

“…Indeed, longer telomere lengths detected in animals from the Sakha Republic with colder climates compared to the control population from Rostov Oblast imply that there could be a mechanism of telomere maintenance in colder climates in cattle. In ectotherms, however, there are reports that at cooler conditions telomere shortening happens during development (Friesen et al, 2022;Burraco et al, 2023), but other authors did not confirm this observation (McLennan et al, 2018).…”

Shorter telomeres are associated with shell anomalies in a long‐lived tortoise

“…However, there is no clear unique pattern described for TL dynamics in ectotherms (Fitzpatrick et al., 2021; Olsson et al., 2018a, 2021), which could even change across their life stages (e.g. amphibian metamorphosis, Burraco et al., 2023; Sánchez‐Montes et al., 2020). For instance, different strains of zebrafish ( Danio rerio ) have been reported to exhibit both stable telomere length (TL) and age‐related telomere shortening (Henriques et al., 2013; Lund et al., 2009).…”