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C. elegans ageing is accelerated by a self-destructive reproductive programme

Author

Listed:
  • Carina C. Kern

    (University College London)

  • Shivangi Srivastava

    (University College London)

  • Marina Ezcurra

    (University College London
    University of Kent, Canterbury)

  • Kuei Ching Hsiung

    (University College London)

  • Nancy Hui

    (University College London)

  • StJohn Townsend

    (University College London
    The Francis Crick Institute)

  • Dominik Maczik

    (University College London)

  • Bruce Zhang

    (University College London)

  • Victoria Tse

    (University College London)

  • Viktoras Konstantellos

    (University College London)

  • Jürg Bähler

    (University College London)

  • David Gems

    (University College London)

Abstract

In post-reproductive C. elegans, destructive somatic biomass repurposing supports production of yolk which, it was recently shown, is vented and can serve as a foodstuff for larval progeny. This is reminiscent of the suicidal reproductive effort (reproductive death) typical of semelparous organisms such as Pacific salmon. To explore the possibility that C. elegans exhibits reproductive death, we have compared sibling species pairs of the genera Caenorhabditis and Pristionchus with hermaphrodites and females. We report that yolk venting and constitutive, early pathology involving major anatomical changes occur only in hermaphrodites, which are also shorter lived. Moreover, only in hermaphrodites does germline removal suppress senescent pathology and markedly increase lifespan. This is consistent with the hypothesis that C. elegans exhibit reproductive death that is suppressed by germline ablation. If correct, this would imply a major difference in the ageing process between C. elegans and most higher organisms, and potentially explain the exceptional plasticity in C. elegans ageing.

Suggested Citation

  • Carina C. Kern & Shivangi Srivastava & Marina Ezcurra & Kuei Ching Hsiung & Nancy Hui & StJohn Townsend & Dominik Maczik & Bruce Zhang & Victoria Tse & Viktoras Konstantellos & Jürg Bähler & David Gem, 2023. "C. elegans ageing is accelerated by a self-destructive reproductive programme," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40088-1
    DOI: 10.1038/s41467-023-40088-1
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    References listed on IDEAS

    as
    1. Carina C. Kern & StJohn Townsend & Antoine Salzmann & Nigel B. Rendell & Graham W. Taylor & Ruxandra M. Comisel & Lazaros C. Foukas & Jürg Bähler & David Gems, 2021. "C. elegans feed yolk to their young in a form of primitive lactation," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    2. Honor Hsin & Cynthia Kenyon, 1999. "Signals from the reproductive system regulate the lifespan of C. elegans," Nature, Nature, vol. 399(6734), pages 362-366, May.
    3. Natsumi Kanzaki & Isheng J. Tsai & Ryusei Tanaka & Vicky L. Hunt & Dang Liu & Kenji Tsuyama & Yasunobu Maeda & Satoshi Namai & Ryohei Kumagai & Alan Tracey & Nancy Holroyd & Stephen R. Doyle & Gavin C, 2018. "Biology and genome of a newly discovered sibling species of Caenorhabditis elegans," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. Yuan Zhao & Ann F. Gilliat & Matthias Ziehm & Mark Turmaine & Hongyuan Wang & Marina Ezcurra & Chenhao Yang & George Phillips & David McBay & William B. Zhang & Linda Partridge & Zachary Pincus & Davi, 2017. "Two forms of death in ageing Caenorhabditis elegans," Nature Communications, Nature, vol. 8(1), pages 1-8, August.
    5. Qing Wei & Yanmei Zhao & Yiqing Guo & Julie Stomel & Ryan Stires & Ronald E. Ellis, 2014. "Co-option of alternate sperm activation programs in the evolution of self-fertile nematodes," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
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