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The biology of aging in a social world: insights from free-ranging rhesus macaques

Laura E. Newman, View ORCID ProfileCamille Testard, Alex R. DeCasien, View ORCID ProfileKenneth L. Chiou, View ORCID ProfileMarina M. Watowich, View ORCID ProfileMareike C. Janiak, Melissa A. Pavez-Fox, Mitchell R. Sanchez Rosado, View ORCID ProfileEve B. Cooper, Christina E. Costa, View ORCID ProfileRachel M. Petersen, View ORCID ProfileMichael J. Montague, Michael L. Platt, View ORCID ProfileLauren J.N. Brent, View ORCID ProfileNoah Snyder-Mackler, James P. Higham
doi: https://doi.org/10.1101/2023.01.28.525893
Laura E. Newman
1Department of Anthropology, New York University, New York, New York, USA
2The New York Consortium in Evolutionary Primatology (NYCEP), New York, New York, USA
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  • For correspondence: laura.newman@nyu.edu camille.testard@pennmedicine.upenn.edu
Camille Testard
3Department of Neuroscience, University of Pennsylvania, Philadelphia, PA, USA
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  • ORCID record for Camille Testard
  • For correspondence: laura.newman@nyu.edu camille.testard@pennmedicine.upenn.edu
Alex R. DeCasien
4Section on Developmental Neurogenomics, National Institutes of Mental Health, Bethesda, Maryland, USA
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Kenneth L. Chiou
5Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, USA
6School of Life Sciences, Arizona State University, Tempe, Arizona, USA
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  • ORCID record for Kenneth L. Chiou
Marina M. Watowich
5Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, USA
6School of Life Sciences, Arizona State University, Tempe, Arizona, USA
7Department of Biology, University of Washington, Seattle, Washington, USA
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  • ORCID record for Marina M. Watowich
Mareike C. Janiak
1Department of Anthropology, New York University, New York, New York, USA
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  • ORCID record for Mareike C. Janiak
Melissa A. Pavez-Fox
9Centre for Research in Animal Behaviour, University of Exeter, United Kingdom
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Mitchell R. Sanchez Rosado
10Department of Microbiology and Medical Zoology, University of Puerto Rico, San Juan, Puerto Rico
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Eve B. Cooper
1Department of Anthropology, New York University, New York, New York, USA
2The New York Consortium in Evolutionary Primatology (NYCEP), New York, New York, USA
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  • ORCID record for Eve B. Cooper
Christina E. Costa
1Department of Anthropology, New York University, New York, New York, USA
2The New York Consortium in Evolutionary Primatology (NYCEP), New York, New York, USA
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Rachel M. Petersen
11Department of Biological Sciences, Vanderbilt University, Nashville, TN, USA
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  • ORCID record for Rachel M. Petersen
Michael J. Montague
3Department of Neuroscience, University of Pennsylvania, Philadelphia, PA, USA
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Michael L. Platt
3Department of Neuroscience, University of Pennsylvania, Philadelphia, PA, USA
12Department of Psychology, University of Pennsylvania, Philadelphia, PA, USA
13Marketing Department, University of Pennsylvania, Philadelphia, PA, USA
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Lauren J.N. Brent
9Centre for Research in Animal Behaviour, University of Exeter, United Kingdom
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  • ORCID record for Lauren J.N. Brent
Noah Snyder-Mackler
5Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, USA
6School of Life Sciences, Arizona State University, Tempe, Arizona, USA
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James P. Higham
1Department of Anthropology, New York University, New York, New York, USA
2The New York Consortium in Evolutionary Primatology (NYCEP), New York, New York, USA
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Abstract

Social adversity can increase the age-associated risk of disease and death, yet the biological mechanisms that link social adversities to aging remain poorly understood. Long-term naturalistic studies of nonhuman animals are crucial for integrating observations of social behavior throughout an individual’s life with detailed anatomical, physiological, and molecular measurements. Here, we synthesize the body of research from one such naturalistic study system, Cayo Santiago Island, which is home to the world’s longest continuously monitored free-ranging population of rhesus macaques. We review recent studies of age-related variation in morphology, gene regulation, microbiome composition, and immune function. We also discuss ecological and social modifiers of age-markers in this population. In particular, we summarize how a major natural disaster, Hurricane Maria, affected rhesus macaque physiology and social structure and highlight the context-dependent and domain-specific nature of aging modifiers. Finally, we conclude by providing directions for future study, on Cayo Santiago and elsewhere, that will further our understanding of aging across different domains and how social adversity modifies aging processes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵‡ These authors are co-senior authors

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 January 29, 2023.
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The biology of aging in a social world: insights from free-ranging rhesus macaques
Laura E. Newman, Camille Testard, Alex R. DeCasien, Kenneth L. Chiou, Marina M. Watowich, Mareike C. Janiak, Melissa A. Pavez-Fox, Mitchell R. Sanchez Rosado, Eve B. Cooper, Christina E. Costa, Rachel M. Petersen, Michael J. Montague, Michael L. Platt, Lauren J.N. Brent, Noah Snyder-Mackler, James P. Higham
bioRxiv 2023.01.28.525893; doi: https://doi.org/10.1101/2023.01.28.525893
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The biology of aging in a social world: insights from free-ranging rhesus macaques
Laura E. Newman, Camille Testard, Alex R. DeCasien, Kenneth L. Chiou, Marina M. Watowich, Mareike C. Janiak, Melissa A. Pavez-Fox, Mitchell R. Sanchez Rosado, Eve B. Cooper, Christina E. Costa, Rachel M. Petersen, Michael J. Montague, Michael L. Platt, Lauren J.N. Brent, Noah Snyder-Mackler, James P. Higham
bioRxiv 2023.01.28.525893; doi: https://doi.org/10.1101/2023.01.28.525893

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