Telomeres positively correlate with pace-of-life and elongate with age in a wild mammal

Abstract

Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and to modulate life-history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade-off hypothesis predicts that short telomeres have thus co-evolved with early reproduction, proactive behaviour and reduced lifespan, i.e. a fast Pace-of-Life Syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anti-cancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life-history strategies is hampered by a lack of study on wild short-lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age and do not limit lifespan in this species. Furthermore, short telomeres correlated with a slow POLS in a sex-specific way. Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, whereas those differences were not recorded in males. Our findings support most predictions adapted from the anti-cancer hypothesis, but none of those made under the resource allocation trade-off hypothesis. Results are in line with an increasing body of evidence suggesting that resource allocation trade-offs alone cannot explaining the diversity of telomere length in adult somatic cells and life-histories observed across the tree of life.

Seasonal variation in telomerase activity and telomere dynamics in a hibernating rodent, the garden dormouse (Eliomys quercinus)

“…In contrast to early research in humans and cancer models, where telomeres typically shorten with age as a result of the end replication problem and oxidative stress OPEN ACCESS EDITED BY James Harper, Sam Houston State University, United States (Harley et al, 1990;Blasco, 2007;Aubert, 2014), recent research has shown that in some organisms telomeres can lengthen as individuals become older and that telomeres can even have a complex and dynamic role in life histories (Monaghan and Ozanne, 2018;Marasco et al, 2022). Such findings of active telomere maintenance struggled to find traction initially but repeated examples across many taxa have led to a general acceptance that the process is not uncommon non-model species (Hoelzl et al, 2016b;Criscuolo et al, 2020;Panasiak et al, 2020;Tissier et al, 2022;Giroud et al, 2023). The underlying mechanisms for telomere repair, however, remain poorly understood.…”

“…All hibernation periods are typified by periods of extreme reduction in metabolism and body temperature (torpor) interspersed with short bursts of euthermia where individuals return to normal metabolism and body temperature before returning into the torpor phase (Lyman et al, 1982;Carey et al, 2003;Heldmaier et al, 2004;Hoelzl et al, 2015). Telomere attrition across hibernation has been shown in both edible dormice (Glis glis) and garden dormice (E. quercinus) as well as in other hibernating rodents such as Columbian ground squirrels (Urocitellus columbianus), eastern chipmunks (Tamias striatus), and also in some bat species (Hoelzl et al, 2016b;Foley et al, 2018;Nowack et al, 2019;Giroud et al, 2022;Tissier et al, 2022;Viblanc et al, 2022). In garden dormice however, individuals were able to maintain or increase relative telomere length (RTL) during hibernation when provided with food ad libitum (Giroud et al, 2023).…”

“…Although, during this time the costs of lipogenesis are likely very high and may not allow investment into telomere maintenance and increased TA, especially in the liver. While research has shown that telomeres can be elongated in edible dormice in the active season when food availability is high (Hoelzl et al, 2016a) and also with chronological age in Eastern chipmunks (Tissier et al, 2022), telomerase activity was not measured in the same individuals, so the mechanism for telomere repair is still unclear. Sampling individuals throughout the entire active season and also throughout hibernation, including during deep torpor and IBE, and measuring telomerase activity as well as telomere length, is the only way to resolve the timing and likely mechanism of telomere maintenance.…”