Telomere dynamics in female Columbian ground squirrels: recovery after emergence and loss after reproduction

Viblanc, Vincent A.; Criscuolo, François; Sosa, Sebastiàn; Schull, Quentin; Boonstra, Rudy; Saraux, Claire; Lejeune, Mathilde; Roth, Jeffrey D.; Uhlrich, Pierre; Zahn, Sandrine; Dobson, F. Stephen

doi:10.1007/s00442-022-05194-9

Cited by 6 publications

(4 citation statements)

References 84 publications

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“…We found no differences in telomere length between retained and changed mates, suggesting both types of parents might not differ in ‘quality’. Interestingly, gannets’ telomeres were stabilized during the favorable year and shortened during unfavorable breeding conditions when parental effort increased, aligning with life history theory ( Stearns, 1992 ) and observations of telomere attrition being influenced by seasonal variations and non-permanent states ( Criscuolo et al, 2020 ; Tissier et al, 2022 ; Viblanc et al, 2022 ). These results are also in line with other recent studies ( Pepke et al, 2022 ; Pepke et al, 2023 ), which have shown that the variation due to year effects were larger than that due to all other environmental, parental or genetic factors included, suggesting that individual heterogeneity in telomere dynamics is mainly driven by annual environmental stochasticity.…”

Section: Discussionsupporting

confidence: 81%

Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions

Pelletier,

Blier,

Vézina

et al. 2023

PeerJ

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Background Life history theory predicts trade-offs between reproduction and survival in species like the northern gannet (Morus bassanus). During breeding, demanding foraging conditions lead them to expand their foraging range and diversify their diet, increasing the risk of reproductive failure. Changing partners may enhance breeding success but lead to more physiological costs. Methods To investigate the physiological costs of reproduction upon partner changes, we measured and compared 21 biomarkers related to telomere dynamics, oxidative stress, inflammation, hematology, nutritional status, and muscle damage. We used a longitudinal approach with gannets (n = 38) over three contrasting years (2017, 2018 and 2019). Results Our results suggest that annual breeding conditions exert a greater influence on physiological changes than partnership status. Individuals that changed partner experienced greater short-term stress than retained partners. This transient increase in stress was marked by short-term increases in oxidative lipid damage, lower antioxidant capacity, signs of inflammation, and greater weight loss than individuals that retained partners. During favorable conditions, individuals that changed mates had stabilized telomere length, decreased antioxidant capacity, glucose concentration, and muscle damage, along with increased oxygen transport capacity. Conversely, unfavorable breeding conditions led to increased telomere attrition, stabilized antioxidant capacity, decreased inflammation susceptibility, diminished oxygen transport capacity, and increased muscle damage. In the cases where partners were retained, distinct physiological changes were observed depending on the year’s conditions, yet the telomere dynamics remained consistent across both partnership status categories. During the favorable year, there was an increase in unsaturated fatty acids and oxygen transport capacity in the blood, coupled with a reduction in inflammation potential and protein catabolism. In contrast, during the unfavorable year in the retained mates, we observed an increase in oxidative DNA damage, antioxidant capacity, weight loss, but a decrease in inflammation susceptibility as observed in changed mates. Discussion Our study shows that behavioral flexibility such as mate switching can help seabirds cope with the challenges of food scarcity during reproduction, but these coping strategies may have a negative impact on physiological status at the individual level. In addition, the marked reduction in telomere length observed during harsh conditions, coupled with the stabilization of telomere length in favorable conditions, highlights the long-term physiological impact of annual breeding conditions on seabirds. These findings underscore the effect on their potential survival and fitness, emphasizing that the influence of annual breeding conditions is greater than that of partnership status.

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Section: Discussionsupporting

confidence: 81%

Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions

Pelletier,

Blier,

Vézina

et al. 2023

PeerJ

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“…Studies on telomeres in rodents revealed that food availability differentially affects telomere attrition rates in dormouse species (Hoelzl et al ., 2016 a ) while hibernation tends to increase telomere length (Hoelzl et al ., 2016 b ). A similar trend was also observed for post‐hibernation differences in telomere length among female Columbian ground squirrels [ Urocitellus columbianus (Ord)] (Viblanc et al ., 2022). Experimental studies in glucocorticoid‐treated mothers with offspring in the American red squirrel [ Tamiasciurus hudsonicus (Erxleben)] (Dantzer et al ., 2020) found no evidence of maternal stress as measured by endocrine responses adversely affecting telomere length in offspring either during parturition, lactation, or rearing.…”

Section: Biological Clocks and Agementioning

confidence: 99%

Biological clocks as age estimation markers in animals: a systematic review and meta‐analysis

et al. 2023

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Various biological attributes associated with individual fitness in animals change predictably over the lifespan of an organism. Therefore, the study of animal ecology and the work of conservationists frequently relies upon the ability to assign animals to functionally relevant age classes to model population fitness. Several approaches have been applied to determining individual age and, while these methods have proved useful, they are not without limitations and often lack standardisation or are only applicable to specific species. For these reasons, scientists have explored the potential use of biological clocks towards creating a universal age‐determination method. Two biological clocks, tooth layer annulation and otolith layering have found universal appeal. Both methods are highly invasive and most appropriate for post‐mortem age‐at‐death estimation. More recently, attributes of cellular ageing previously explored in humans have been adapted to studying ageing in animals for the use of less‐invasive molecular methods for determining age. Here, we review two such methods, assessment of methylation and telomere length, describing (i) what they are, (ii) how they change with age, and providing (iii) a summary and meta‐analysis of studies that have explored their utility in animal age determination. We found that both attributes have been studied across multiple vertebrate classes, however, telomere studies were used before methylation studies and telomere length has been modelled in nearly twice as many studies. Telomere length studies included in the review often related changes to stress responses and illustrated that telomere length is sensitive to environmental and social stressors and, in the absence of repair mechanisms such as telomerase or alternative lengthening modes, lacks the ability to recover. Methylation studies, however, while also detecting sensitivity to stressors and toxins, illustrated the ability to recover from such stresses after a period of accelerated ageing, likely due to constitutive expression or reactivation of repair enzymes such as DNA methyl transferases. We also found that both studied attributes have parentally heritable features, but the mode of inheritance differs among taxa and may relate to heterogamy. Our meta‐analysis included more than 40 species in common for methylation and telomere length, although both analyses included at least 60 age‐estimation models. We found that methylation outperforms telomere length in terms of predictive power evidenced from effect sizes (more than double that observed for telomeres) and smaller prediction intervals. Both methods produced age correlation models using similar sample sizes and were able to classify individuals into young, middle, or old age classes with high accuracy. Our review and meta‐analysis illustrate that both methods are well suited to studying age in animals and do not suffer significantly from variation due to differences in the lifespan of the species, genome size, karyotype, or tissue type but rather that quantitative method, patterns of inheritance, and environmental factors should be the main considerations. Thus, provided that complex factors affecting the measured trait can be accounted for, both methylation and telomere length are promising targets to develop as biomarkers for age determination in animals.

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“…Such work has since been done, and it has demonstrated that telomere dynamics are perhaps even more plastic than previously thought [74] . For example, telomeres (mainly measured in blood cells) may both shorten and lengthen with time within individuals [75][76][77] even in absence of apparent telomerase activity, [78] and TL can exhibit seasonal changes, [79,80] or transient [81] or delayed [82,83] responses to stressors. Although telomeres cannot be used for individual age estimation, TL may still be relevant in conservation biology today as a tool for qualitative comparisons of population demography, viability or for monitoring responses to environmental change (see [17,[84][85][86] ).…”

Section: A Brief History Of Using Telomeres For Chronological Age Est...mentioning

confidence: 99%

Telomere length is not a useful tool for chronological age estimation in animals

Pepke

2023

BioEssays

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Telomeres are short repetitive DNA sequences capping the ends of chromosomes. Telomere shortening occurs during cell division and may be accelerated by oxidative damage or ameliorated by telomere maintenance mechanisms. Consequently, telomere length changes with age, which was recently confirmed in a large meta‐analysis across vertebrates. However, based on the correlation between telomere length and age, it was concluded that telomere length can be used as a tool for chronological age estimation in animals. Correlation should not be confused with predictability, and the current data and studies suggest that telomeres cannot be used to reliably predict individual chronological age. There are biological reasons for why there is large individual variation in telomere dynamics, which is mainly due to high susceptibility to a wide range of environmental, but also genetic factors, rendering telomeres unfeasible as a tool for age estimation. The use of telomeres for chronological age estimation is largely a misguided effort, but its occasional reappearance in the literature raises concerns that it will mislead resources in wildlife conservation.

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Telomere dynamics in female Columbian ground squirrels: recovery after emergence and loss after reproduction

Abstract: Author contribution statementVAV, FSD and FC designed the study. VAV, SS, CS, JFR, QS and FSD collected the data in the field. VAV and CS performed the statistical analysis and ML and SZ the laboratory analyses and check the quality of the qPCR results with FC.

Cited by 6 publications

References 84 publications

Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions

Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions

Biological clocks as age estimation markers in animals: a systematic review and meta‐analysis

Telomere length is not a useful tool for chronological age estimation in animals

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