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C. elegans provide milk for their young

Carina C. Kern, StJohn Townsend, Antoine Salzmann, Nigel B. Rendell, Graham W. Taylor, Ruxandra M. Comisel, Lazaros C. Foukas, View ORCID ProfileJürg Bähler, David Gems
doi: https://doi.org/10.1101/2020.11.15.380253
Carina C. Kern
1Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK
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StJohn Townsend
1Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK
2Molecular Biology of Metabolism Laboratory, The Francis Crick Institute, London NW1 1AT, UK
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Antoine Salzmann
1Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK
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Nigel B. Rendell
3Wolfson Drug Discovery Unit, Centre for Amyloidosis and Acute Phase Proteins, Division of Medicine, University College London, London NW3 2PF, UK
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Graham W. Taylor
3Wolfson Drug Discovery Unit, Centre for Amyloidosis and Acute Phase Proteins, Division of Medicine, University College London, London NW3 2PF, UK
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Ruxandra M. Comisel
1Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK
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Lazaros C. Foukas
1Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK
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Jürg Bähler
1Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK
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  • ORCID record for Jürg Bähler
David Gems
1Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK
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  • For correspondence: david.gems@ucl.ac.uk
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Abstract

Adult C. elegans hermaphrodites exhibit severe senescent pathology that begins to develop within days of reaching sexual maturity (Ezcurra et al., 2018; Garigan et al., 2002; Herndon et al., 2002; Wang et al., 2018). For example, after depletion of self-sperm, intestinal biomass is converted into yolk leading to intestinal atrophy and yolk steatosis (pseudocoelomic lipoprotein pools, PLPs) (Ezcurra et al., 2018; Garigan et al., 2002; Herndon et al., 2002; Sornda et al., 2019). These senescent pathologies are promoted by insulin/IGF-1 signalling (IIS), which also shortens lifespan (Ezcurra et al., 2018; Kenyon, 2010). This pattern of rapid and severe pathology in organs linked to reproduction is reminiscent of semelparous organisms where massive reproductive effort leads to rapid death (reproductive death) as in Pacific salmon (Finch, 1990; Gems et al., 2020). Moreover, destructive conversion of somatic biomass to support reproduction is a hallmark of reproductive death (Gems et al., 2020). Yet arguing against the occurrence of reproductive death in C. elegans is the apparent futility of post-reproductive yolk production. Here we show that this effort is not futile, since post-reproductive mothers vent yolk through their vulva, which is consumed by progeny and supports their growth; thus vented yolk functions as a milk, and C. elegans mothers exhibit a form of lactation. Moreover, IIS promotes lactation, thereby effecting a costly process of resource transfer from postreproductive mothers to offspring. These results support the view that C. elegans hermaphrodites exhibit reproductive death involving a self-destructive process of lactation that is promoted by IIS. They also provide new insight into how the strongly life-shortening effects of IIS in C. elegans evolved.

Competing Interest Statement

The authors have declared no competing interest.

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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 4.0 International license.
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Posted November 15, 2020.
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C. elegans provide milk for their young
Carina C. Kern, StJohn Townsend, Antoine Salzmann, Nigel B. Rendell, Graham W. Taylor, Ruxandra M. Comisel, Lazaros C. Foukas, Jürg Bähler, David Gems
bioRxiv 2020.11.15.380253; doi: https://doi.org/10.1101/2020.11.15.380253
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C. elegans provide milk for their young
Carina C. Kern, StJohn Townsend, Antoine Salzmann, Nigel B. Rendell, Graham W. Taylor, Ruxandra M. Comisel, Lazaros C. Foukas, Jürg Bähler, David Gems
bioRxiv 2020.11.15.380253; doi: https://doi.org/10.1101/2020.11.15.380253

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