Species that hibernate generally live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor–arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause ageing suppression. Metabolic rate is also a known correlate of longevity; we thus proposed the ‘hibernation–ageing hypothesis’ whereby ageing is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots (Marmota flaviventer), which spend 7–8 months per year hibernating. We used two approaches to estimate epigenetic age: the epigenetic clock and the epigenetic pacemaker. Variation in epigenetic age of 149 samples collected throughout the life of 73 females was modelled using generalized additive mixed models (GAMM), where season (cyclic cubic spline) and chronological age (cubic spline) were fixed effects. As expected, the GAMM using epigenetic ages calculated from the epigenetic pacemaker was better able to detect nonlinear patterns in epigenetic ageing over time. We observed a logarithmic curve of epigenetic age with time, where the epigenetic age increased at a higher rate until females reached sexual maturity (two years old). With respect to circannual patterns, the epigenetic age increased during the active season and essentially stalled during the hibernation period. Taken together, our results are consistent with the hibernation–ageing hypothesis and may explain the enhanced longevity in hibernators.
Bibliographical noteFunding Information:
We are grateful for all the marmoteers who diligently collected the data over the years, and for the Blumstein, Horvath and Wayne labs for supportive feedback. Thanks also for the helpful insights from the UCLA Statistical Consulting Group, especially to A. Lin and S. Jalal. This work was supported by the Paul G. Allen Frontiers Group (PI S.H.). G.M.P. was supported by the Science Without Borders programme of the National Counsel of Technological and Scientific Development of Brazil and the UCLA Canadian Studies Program. The long-term marmot project (PI D.T.B.) is supported by the National Geographic Society, UCLA (Faculty Senate and the Division of Life Sciences), a Rocky Mountain Biological Laboratory research fellowship and by the National Science Foundation (IDBR-0754247, DEB-1119660 and DEB-1557130 to D.T.B., as well as DBI-0242960, DBI-0731346 and DBI-1226713 to the Rocky Mountain Biological Laboratory). Except by providing financial support, our funding sources were not involved in any stage of development of this manuscript.
© 2022, The Author(s).
ASJC Scopus subject areas
- Ecology, Evolution, Behavior and Systematics