Understanding seasonal telomere length dynamics in hibernating species.

Oxidative stress is thought to be one of the main causes of ageing as it progressively damages cell components throughout life, eventually causing cellular failure and apoptosis. In many organisms, telomeres shorten throughout life under the effect of, amongst other factors, oxidative stress, and are therefore commonly used as marker of biological ageing. However, hibernators, which are regularly exposed to acute oxidative stress when rewarming from torpor, are unexpectedly long-lived. In this review, we explore the causes of oxidative stress associated with hibernation and its impact on telomere dynamics in different taxa, focussing on hibernating rodents. We then speculate on the adaptive mechanisms of hibernators to compensate for the effects of oxidative stress, which may explain their increased longevity. Because winter hibernation appears to be associated with high oxidative stress, hibernators, particularly rodents, may periodically invest in repair mechanisms and antioxidant defences, resulting in seasonal variations in telomere lengths. This research shows how species with a slow life-history strategy deal with large changes in oxidative stress, unifying evolutionary and physiological theories of ageing. Because of the marked seasonal variation in telomere length, we also draw attention when using telomeres as markers for biological aging in seasonal heterotherms and possibly in other highly seasonal species.

Evolutionary trade-offs in dormancy phenology.

Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the 'life-history' hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.

Integrating Mortality Risk and the Adaptiveness of Hibernation.

Low mortality rate is often associated with slow life history, and so far, has mainly been assessed through examinations of specific adaptations and lifestyles that limit mortality risk. However, the organization of activity time budgets also needs to be considered, since some activities and the time afforded for performing them may expose animals to higher mortality risks such as increased predation and/or increased metabolic stress. We examined the extent of activity time budgets contribution to explaining variation in life history traits in mammals. We specifically focused on hibernating species because of their marked seasonal cycle of activity/inactivity associated with very different mortality risks. Hibernation is considered a seasonal adaptation to prolonged periods of food shortage and cold. This inactivity period may also reduce both extrinsic and intrinsic mortality risks, by decreasing exposure to predators and drastically reducing metabolic rate. In turn, reduction in mortality may explain why hibernators have slower life history traits than non-hibernators of the same size. Using phylogenetically controlled models, we tested the hypothesis that longevity was positively correlated with the hibernation season duration (the time spent between immergence and emergence from the hibernaculum or den) across 82 different mammalian species. We found that longevity increased significantly with hibernation season duration, an effect that was particularly strong in small hibernators (<1.5 kg) especially for bats. These results confirm that hibernation not only allows mammals to survive periods of energy scarcity, but further suggest that activity time budgets may be selected to reduce mortality risks according to life history pace.