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Hibernation slows epigenetic aging in yellow-bellied marmots

View ORCID ProfileGabriela M. Pinho, View ORCID ProfileJulien G. A. Martin, Colin Farrell, View ORCID ProfileAmin Haghani, View ORCID ProfileJoseph A. Zoller, Joshua Zhang, Sagi Snir, Matteo Pellegrini, View ORCID ProfileRobert K. Wayne, Daniel T. Blumstein, View ORCID ProfileSteve Horvath
doi: https://doi.org/10.1101/2021.03.07.434299
Gabriela M. Pinho
aDepartment of Ecology and Evolutionary Biology, University of California, 621 Young Drive South, Los Angeles, CA 90095–1606, USA
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  • ORCID record for Gabriela M. Pinho
  • For correspondence: gabriela.m.pinho@gmail.com julien.martin@uottawa.ca marmots@ucla.edu SHorvath@mednet.ucla.edu
Julien G. A. Martin
bDepartment of Biology, University of Ottawa, 30 Marie Curie, Ottawa, ON K1N 6N5, Canada
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  • ORCID record for Julien G. A. Martin
  • For correspondence: gabriela.m.pinho@gmail.com julien.martin@uottawa.ca marmots@ucla.edu SHorvath@mednet.ucla.edu
Colin Farrell
cDepartment of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA, USA
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Amin Haghani
dHuman Genetics, David Geffen School of Medicine, University of California, Los Angeles CA 90095, USA
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  • ORCID record for Amin Haghani
Joseph A. Zoller
dHuman Genetics, David Geffen School of Medicine, University of California, Los Angeles CA 90095, USA
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Joshua Zhang
dHuman Genetics, David Geffen School of Medicine, University of California, Los Angeles CA 90095, USA
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Sagi Snir
eDepartment of Evolutionary & Environmental Biology, Institute of Evolution, University of Haifa, Haifa, Israel
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Matteo Pellegrini
cDepartment of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA, USA
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Robert K. Wayne
aDepartment of Ecology and Evolutionary Biology, University of California, 621 Young Drive South, Los Angeles, CA 90095–1606, USA
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Daniel T. Blumstein
aDepartment of Ecology and Evolutionary Biology, University of California, 621 Young Drive South, Los Angeles, CA 90095–1606, USA
fRocky Mountain Biological Laboratory, Box 519, Crested Butte, CO 81224, USA
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  • For correspondence: gabriela.m.pinho@gmail.com julien.martin@uottawa.ca marmots@ucla.edu SHorvath@mednet.ucla.edu
Steve Horvath
dHuman Genetics, David Geffen School of Medicine, University of California, Los Angeles CA 90095, USA
gBiostatistics, Fielding School of Public Health, University of California, Los Angeles, Los Angeles, California, USA
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  • ORCID record for Steve Horvath
  • For correspondence: gabriela.m.pinho@gmail.com julien.martin@uottawa.ca marmots@ucla.edu SHorvath@mednet.ucla.edu
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Abstract

Species that hibernate 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 aging suppression. Metabolic rate is also a known correlate of longevity, we thus proposed the ‘hibernation-aging hypothesis’ whereby aging 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 were modeled 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 age change 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 (2-years old). With respect to circannual patterns, the epigenetic age increased during the summer and essentially stalled during the winter. Our enrichment analysis of age-related CpG sites revealed pathways related to development and cell differentiation, while the season-related CpGs enriched pathways related to central carbon metabolism, immune system, and circadian clock. Taken together, our results are consistent with the hibernation-aging hypothesis and may explain the enhanced longevity in hibernators.

Competing Interest Statement

SH is a founder of the non-profit Epigenetic Clock Development Foundation which plans to license several patents from his employer UC Regents. These patents list SH as inventor. The other authors declare no conflicts of interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 08, 2021.
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Hibernation slows epigenetic aging in yellow-bellied marmots
Gabriela M. Pinho, Julien G. A. Martin, Colin Farrell, Amin Haghani, Joseph A. Zoller, Joshua Zhang, Sagi Snir, Matteo Pellegrini, Robert K. Wayne, Daniel T. Blumstein, Steve Horvath
bioRxiv 2021.03.07.434299; doi: https://doi.org/10.1101/2021.03.07.434299
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Hibernation slows epigenetic aging in yellow-bellied marmots
Gabriela M. Pinho, Julien G. A. Martin, Colin Farrell, Amin Haghani, Joseph A. Zoller, Joshua Zhang, Sagi Snir, Matteo Pellegrini, Robert K. Wayne, Daniel T. Blumstein, Steve Horvath
bioRxiv 2021.03.07.434299; doi: https://doi.org/10.1101/2021.03.07.434299

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