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Correlated evolution of social organization and lifespan in mammals

Author

Listed:
  • Pingfen Zhu

    (Institute of Zoology)

  • Weiqiang Liu

    (Institute of Zoology
    University of Chinese Academy of Sciences)

  • Xiaoxiao Zhang

    (Institute of Zoology
    University of Chinese Academy of Sciences)

  • Meng Li

    (Institute of Zoology)

  • Gaoming Liu

    (Institute of Zoology)

  • Yang Yu

    (Institute of Zoology
    University of Science and Technology of China)

  • Zihao Li

    (Institute of Zoology
    University of Chinese Academy of Sciences)

  • Xuanjing Li

    (Institute of Zoology
    University of Chinese Academy of Sciences)

  • Juan Du

    (Institute of Zoology
    University of Chinese Academy of Sciences)

  • Xiao Wang

    (Institute of Zoology)

  • Cyril C. Grueter

    (The University of Western Australia
    The University of Western Australia
    Dali University)

  • Ming Li

    (Institute of Zoology
    Chinese Academy of Sciences)

  • Xuming Zhou

    (Institute of Zoology)

Abstract

Discerning the relationship between sociality and longevity would permit a deeper understanding of how animal life history evolved. Here, we perform a phylogenetic comparative analysis of ~1000 mammalian species on three states of social organization (solitary, pair-living, and group-living) and longevity. We show that group-living species generally live longer than solitary species, and that the transition rate from a short-lived state to a long-lived state is higher in group-living than non-group-living species, altogether supporting the correlated evolution of social organization and longevity. The comparative brain transcriptomes of 94 mammalian species identify 31 genes, hormones and immunity-related pathways broadly involved in the association between social organization and longevity. Further selection features reveal twenty overlapping pathways under selection for both social organization and longevity. These results underscore a molecular basis for the influence of the social organization on longevity.

Suggested Citation

  • Pingfen Zhu & Weiqiang Liu & Xiaoxiao Zhang & Meng Li & Gaoming Liu & Yang Yu & Zihao Li & Xuanjing Li & Juan Du & Xiao Wang & Cyril C. Grueter & Ming Li & Xuming Zhou, 2023. "Correlated evolution of social organization and lifespan in mammals," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35869-7
    DOI: 10.1038/s41467-023-35869-7
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    References listed on IDEAS

    as
    1. van Buuren, Stef & Groothuis-Oudshoorn, Karin, 2011. "mice: Multivariate Imputation by Chained Equations in R," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 45(i03).
    2. Georg Petkau & Twm J. Mitchell & Krishnendu Chakraborty & Sarah E. Bell & Vanessa D´Angeli & Louise Matheson & David J. Turner & Alexander Saveliev & Ozge Gizlenci & Fiamma Salerno & Peter D. Katsikis, 2022. "The timing of differentiation and potency of CD8 effector function is set by RNA binding proteins," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Mark Pagel, 1999. "Inferring the historical patterns of biological evolution," Nature, Nature, vol. 401(6756), pages 877-884, October.
    4. Miranda M. Lim & Zuoxin Wang & Daniel E. Olazábal & Xianghui Ren & Ernest F. Terwilliger & Larry J. Young, 2004. "Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene," Nature, Nature, vol. 429(6993), pages 754-757, June.
    5. Daniel M. Rosenbaum & Søren G. F. Rasmussen & Brian K. Kobilka, 2009. "The structure and function of G-protein-coupled receptors," Nature, Nature, vol. 459(7245), pages 356-363, May.
    6. David Brawand & Magali Soumillon & Anamaria Necsulea & Philippe Julien & Gábor Csárdi & Patrick Harrigan & Manuela Weier & Angélica Liechti & Ayinuer Aximu-Petri & Martin Kircher & Frank W. Albert & U, 2011. "The evolution of gene expression levels in mammalian organs," Nature, Nature, vol. 478(7369), pages 343-348, October.
    7. Andres Bendesky & Young-Mi Kwon & Jean-Marc Lassance & Caitlin L. Lewarch & Shenqin Yao & Brant K. Peterson & Meng Xiao He & Catherine Dulac & Hopi E. Hoekstra, 2017. "The genetic basis of parental care evolution in monogamous mice," Nature, Nature, vol. 544(7651), pages 434-439, April.
    8. Martin A. Nowak & Corina E. Tarnita & Edward O. Wilson, 2010. "The evolution of eusociality," Nature, Nature, vol. 466(7310), pages 1057-1062, August.
    9. Francesco N. Carelli & Angélica Liechti & Jean Halbert & Maria Warnefors & Henrik Kaessmann, 2018. "Repurposing of promoters and enhancers during mammalian evolution," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    10. Ravi K Patel & Mukesh Jain, 2012. "NGS QC Toolkit: A Toolkit for Quality Control of Next Generation Sequencing Data," PLOS ONE, Public Library of Science, vol. 7(2), pages 1-7, February.
    11. Susanne Shultz & Christopher Opie & Quentin D. Atkinson, 2011. "Stepwise evolution of stable sociality in primates," Nature, Nature, vol. 479(7372), pages 219-222, November.
    12. Jeong-Tae Kwon & Changhyeon Ryu & Hyeseung Lee & Alec Sheffield & Jingxuan Fan & Daniel H. Cho & Shivani Bigler & Heather A. Sullivan & Han Kyung Choe & Ian R. Wickersham & Myriam Heiman & Gloria B. C, 2021. "An amygdala circuit that suppresses social engagement," Nature, Nature, vol. 593(7857), pages 114-118, May.
    13. Michael Douglas Reed & Yeong Shin Yim & Ralf D. Wimmer & Hyunju Kim & Changhyeon Ryu & Gwyneth Margaret Welch & Matias Andina & Hunter Oren King & Ari Waisman & Michael M. Halassa & Jun R. Huh & Glori, 2020. "IL-17a promotes sociability in mouse models of neurodevelopmental disorders," Nature, Nature, vol. 577(7789), pages 249-253, January.
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