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Social isolation shortens lifespan through oxidative stress in ants

Author

Listed:
  • Akiko Koto

    (National Institute of Advanced Industrial Science and Technology
    National Institute of Advanced Industrial Science and Technology)

  • Makoto Tamura

    (Mitsubishi Tanabe Pharma America)

  • Pui Shan Wong

    (National Institute of Advanced Industrial Science and Technology)

  • Sachiyo Aburatani

    (National Institute of Advanced Industrial Science and Technology
    National Institute of Advanced Industrial Science and Technology)

  • Eyal Privman

    (University of Haifa, Institute of Evolution, Department of Evolutionary and Environmental Biology)

  • Céline Stoffel

    (University of Lausanne, Department of Ecology and Evolution)

  • Alessandro Crespi

    (Ecole Polytechnique Fédérale de Lausanne)

  • Sean Keane McKenzie

    (University of Lausanne, Department of Ecology and Evolution)

  • Christine Mendola

    (University of Lausanne, Department of Ecology and Evolution)

  • Tomas Kay

    (University of Lausanne, Department of Ecology and Evolution)

  • Laurent Keller

    (University of Lausanne, Department of Ecology and Evolution
    Social Evolution Unit, Cornuit 8, BP 855)

Abstract

Social isolation negatively affects health, induces detrimental behaviors, and shortens lifespan in social species. Little is known about the mechanisms underpinning these effects because model species are typically short-lived and non-social. Using colonies of the carpenter ant Camponotus fellah, we show that social isolation induces hyperactivity, alters space-use, and reduces lifespan via changes in the expression of genes with key roles in oxidation-reduction and an associated accumulation of reactive oxygen species. These physiological effects are localized to the fat body and oenocytes, which perform liver-like functions in insects. We use pharmacological manipulations to demonstrate that the oxidation-reduction pathway causally underpins the detrimental effects of social isolation on behavior and lifespan. These findings have important implications for our understanding of how social isolation affects behavior and lifespan in general.

Suggested Citation

  • Akiko Koto & Makoto Tamura & Pui Shan Wong & Sachiyo Aburatani & Eyal Privman & Céline Stoffel & Alessandro Crespi & Sean Keane McKenzie & Christine Mendola & Tomas Kay & Laurent Keller, 2023. "Social isolation shortens lifespan through oxidative stress in ants," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41140-w
    DOI: 10.1038/s41467-023-41140-w
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    References listed on IDEAS

    as
    1. Zhang Bin & Horvath Steve, 2005. "A General Framework for Weighted Gene Co-Expression Network Analysis," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 4(1), pages 1-45, August.
    2. Julianne Holt-Lunstad & Timothy B Smith & J Bradley Layton, 2010. "Social Relationships and Mortality Risk: A Meta-analytic Review," PLOS Medicine, Public Library of Science, vol. 7(7), pages 1-1, July.
    3. Eugenio Gutierrez & David Wiggins & Barbara Fielding & Alex P. Gould, 2007. "Specialized hepatocyte-like cells regulate Drosophila lipid metabolism," Nature, Nature, vol. 445(7125), pages 275-280, January.
    4. Kerui Huang & Ting Miao & Kai Chang & Jinoh Kim & Ping Kang & Qiuhan Jiang & Andrew J. Simmonds & Francesca Di Cara & Hua Bai, 2020. "Impaired peroxisomal import in Drosophila oenocytes causes cardiac dysfunction by inducing upd3 as a peroxikine," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    5. Wanhe Li & Zikun Wang & Sheyum Syed & Cheng Lyu & Samantha Lincoln & Jenna O’Neil & Andrew D. Nguyen & Irena Feng & Michael W. Young, 2021. "Chronic social isolation signals starvation and reduces sleep in Drosophila," Nature, Nature, vol. 597(7875), pages 239-244, September.
    6. Laurent Keller & Michel Genoud, 1997. "Extraordinary lifespans in ants: a test of evolutionary theories of ageing," Nature, Nature, vol. 389(6654), pages 958-960, October.
    7. Toren Finkel & Nikki J. Holbrook, 2000. "Oxidants, oxidative stress and the biology of ageing," Nature, Nature, vol. 408(6809), pages 239-247, November.
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