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Genome Methylation Predicts Age and Longevity of Bats

View ORCID ProfileGerald S. Wilkinson, Danielle M. Adams, Bryan D. Arnold, Hope C. Ball, Charles E. Breeze, Gerald Carter, Lisa Noelle Cooper, Dina K.N. Dechmann, Paolo S. Devanna, Nicolas J. Fasel, Alexander V. Galazyuk, Linus Gunther, Amin Haghani, Caesar Z. Li, Ake T Lu, Edward Hurme, Gareth Jones, Mirjam Knornschild, Ella Z. Lattenkamp, Frieder Mayer, Rodrigo A. Medellin, Martina Nagy, Brian Pope, Megan L. Power, Roger D. Ransome, View ORCID ProfileJosephine A. Reinhardt, View ORCID ProfileEmma C. Teeling, View ORCID ProfileSonja C. Vernes, Daniel Zamora-Mejías, Joshua Zhang, Joseph Zoller, View ORCID ProfileSteve Horvath
doi: https://doi.org/10.1101/2020.09.04.283655
Gerald S. Wilkinson
1Department of Biology, University of Maryland, College Park 20742 USA
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  • For correspondence: wilkinso@umd.edu shorvath@mednet.ucla.edu
Danielle M. Adams
1Department of Biology, University of Maryland, College Park 20742 USA
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Bryan D. Arnold
2Department of Biology, Illinois College, Jacksonville, IL 62650 USA
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Hope C. Ball
3Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, Ohio, U.S.A. 44272-0095
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Charles E. Breeze
4Altius Institute for Biomedical Sciences, Seattle, WA, 98121 USA
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Gerald Carter
5Department of Evolution, Ecology and Organismal Biology, The Ohio State University, 318 W. 12th Avenue, Columbus, OH, 43210 - 1293 USA
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Lisa Noelle Cooper
3Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, Ohio, U.S.A. 44272-0095
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Dina K.N. Dechmann
6Department of Migration, Max Planck Institute of Animal Behavior, Radolfzell, Germany
7Department of Biology, University of Konstanz, Konstanz, Germany
8Smithsonian Tropical Research Institute, Panama
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Paolo S. Devanna
10Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
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Nicolas J. Fasel
11Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
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Alexander V. Galazyuk
3Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, Ohio, U.S.A. 44272-0095
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Linus Gunther
12Museum für Naturkunde, Leibniz-Institute for Evolution and Biodiversity Science, Berlin, Germany
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Amin Haghani
13Department of Human Genetics, David Geffen School of Medicine, University of California, Los Angeles USA
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Caesar Z. Li
14Department of Biostatistics, Fielding School of Public Health, University of California, Los Angeles USA
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Ake T Lu
13Department of Human Genetics, David Geffen School of Medicine, University of California, Los Angeles USA
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Edward Hurme
1Department of Biology, University of Maryland, College Park 20742 USA
6Department of Migration, Max Planck Institute of Animal Behavior, Radolfzell, Germany
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Gareth Jones
15School of Biological Sciences, University of Bristol, Bristol, UK
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Mirjam Knornschild
8Smithsonian Tropical Research Institute, Panama
12Museum für Naturkunde, Leibniz-Institute for Evolution and Biodiversity Science, Berlin, Germany
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Ella Z. Lattenkamp
9Department Biology II, Ludwig Maximilians University Munich, Martinsried, Germany
10Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
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Frieder Mayer
12Museum für Naturkunde, Leibniz-Institute for Evolution and Biodiversity Science, Berlin, Germany
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Rodrigo A. Medellin
20Instituto de Ecología, Universidad Nacional Autónoma de México, Ap. Postal 70-275 04510, Ciudad Universitaria, México
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Martina Nagy
12Museum für Naturkunde, Leibniz-Institute for Evolution and Biodiversity Science, Berlin, Germany
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Brian Pope
21Lubee Bat Conservancy, 1309 NW 192nd Avenue, Gainesville, FL 32609 USA
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Megan L. Power
19School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland
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Roger D. Ransome
15School of Biological Sciences, University of Bristol, Bristol, UK
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Josephine A. Reinhardt
16Department of Biology, State University of New York, Geneseo USA
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Emma C. Teeling
19School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland
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Sonja C. Vernes
10Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
17Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
18School of Biology, The University of St Andrews, Fife, UK
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Daniel Zamora-Mejías
20Instituto de Ecología, Universidad Nacional Autónoma de México, Ap. Postal 70-275 04510, Ciudad Universitaria, México
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Joshua Zhang
13Department of Human Genetics, David Geffen School of Medicine, University of California, Los Angeles USA
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Joseph Zoller
14Department of Biostatistics, Fielding School of Public Health, University of California, Los Angeles USA
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Steve Horvath
13Department of Human Genetics, David Geffen School of Medicine, University of California, Los Angeles USA
14Department of Biostatistics, Fielding School of Public Health, University of California, Los Angeles USA
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  • For correspondence: wilkinso@umd.edu shorvath@mednet.ucla.edu
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Summary

Bats hold considerable potential for understanding exceptional longevity because some species can live eight times longer than other mammals of similar size [1]. Estimating their age or longevity is difficult because they show few signs of aging. DNA methylation (DNAm) provides a potential solution given its utility for estimating age [2-4] and lifespan [5-7] in humans. Here, we profile DNAm from wing biopsies of nearly 700 individuals representing 26 bat species and demonstrate that DNAm can predict chronological age accurately. Furthermore, the rate DNAm changes at age-informative sites is negatively related to longevity. To identify longevity-informative sites, we compared DNAm rates between three long-lived and two short-lived species. Hypermethylated age and longevity sites are enriched for histone and chromatin features associated with transcriptional regulation and preferentially located in the promoter regions of helix-turn-helix transcription factors (TFs). Predicted TF binding site motifs and enrichment analyses indicate that age-related methylation change is influenced by developmental processes, while longevity-related DNAm change is associated with innate immunity or tumorigenesis genes, suggesting that bat longevity results, in part, from augmented immune response and cancer suppression.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • http://hdl.handle.net/1903/26373

  • https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GPL28271

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Genome Methylation Predicts Age and Longevity of Bats
Gerald S. Wilkinson, Danielle M. Adams, Bryan D. Arnold, Hope C. Ball, Charles E. Breeze, Gerald Carter, Lisa Noelle Cooper, Dina K.N. Dechmann, Paolo S. Devanna, Nicolas J. Fasel, Alexander V. Galazyuk, Linus Gunther, Amin Haghani, Caesar Z. Li, Ake T Lu, Edward Hurme, Gareth Jones, Mirjam Knornschild, Ella Z. Lattenkamp, Frieder Mayer, Rodrigo A. Medellin, Martina Nagy, Brian Pope, Megan L. Power, Roger D. Ransome, Josephine A. Reinhardt, Emma C. Teeling, Sonja C. Vernes, Daniel Zamora-Mejías, Joshua Zhang, Joseph Zoller, Steve Horvath
bioRxiv 2020.09.04.283655; doi: https://doi.org/10.1101/2020.09.04.283655
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Genome Methylation Predicts Age and Longevity of Bats
Gerald S. Wilkinson, Danielle M. Adams, Bryan D. Arnold, Hope C. Ball, Charles E. Breeze, Gerald Carter, Lisa Noelle Cooper, Dina K.N. Dechmann, Paolo S. Devanna, Nicolas J. Fasel, Alexander V. Galazyuk, Linus Gunther, Amin Haghani, Caesar Z. Li, Ake T Lu, Edward Hurme, Gareth Jones, Mirjam Knornschild, Ella Z. Lattenkamp, Frieder Mayer, Rodrigo A. Medellin, Martina Nagy, Brian Pope, Megan L. Power, Roger D. Ransome, Josephine A. Reinhardt, Emma C. Teeling, Sonja C. Vernes, Daniel Zamora-Mejías, Joshua Zhang, Joseph Zoller, Steve Horvath
bioRxiv 2020.09.04.283655; doi: https://doi.org/10.1101/2020.09.04.283655

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