Dispose the disposable soma theory?

Reproduction does not have lasting effects on survival in mice
Dispose the disposable soma theory?
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The disposable soma theory (DST), first proposed by biologist Thomas Kirkwood in 1977, suggested that organisms face a trade-off between the energy invested in maintaining their bodies (or soma) and the energy devoted to reproduction [1-4]. The body was viewed as "disposable" because, from an evolutionary standpoint, once an organism has reproduced and passed on its genes, maintaining the body became less of a priority. As a result, the theory predicts decreasing investments in somatic maintenance after reproductive events which accumulates and explains the gradual decline in physiological functions over time, offering insight into the aging process from an evolutionary perspective. 

Reproduction is a costly process, and animals that allocate a portion of their energy budget to reproduction may face an accelerated decline in physiological homeostasis [5]. This reduction in energy available for maintaining the body leads to faster aging and a higher risk of mortality as the organism ages. Therefore, according to the disposable soma theory (DST), the significant energy trade-off between body maintenance and reproduction implies that animals that have reproduced are likely to experience increased mortality later in life.

We set out to test this prediction using over 120 breeding and non-breeding mice. To ascertain whether the DST prediction of increased mortality post-reproduction was confirmed, we took comprehensive biological and physiological inventories of the experimental individuals’ reproductive outputs, body composition, daily energy expenditure, oxidative stress as well as lifespan. 

We found that reproduction was not inconsequential: there was an immediate negative effect on survival due to problems during birthing for some females. However, contrary to the predictions of the DST, there was no evidence of a residual effect on survival once breeding females stopped reproducing, indicating no trade-off with somatic maintenance (see below snapshot of figure 2 in the paper). Thus, higher mortality appears to be a direct consequence of reproduction, but reproduction alone does not incur long-term physiological costs [6].

Fig 1

Does this new evidence suggest we should dispose the disposable soma theory? Not yet. But it does show that reproduction and survival are life-histories which interact in much more complex ways. In fact, studies have shown that the trade-off between reproduction and survival can be decoupled through dietary interventions [7-8]. Future work will uncover the extent to which the DST holds across species and will inform us the mechanisms through which physiological demands during reproduction revert after individuals ceased to reproduce. 

References cited

  • Kirkwood, T. B. L. (1977). Evolution of ageing. Nature, 270(5635), 301-304. https://doi.org/10.1038/270301a0
  • Kirkwood, T. B. L., & Holliday, R. (1979). The evolution of ageing and longevity. Proceedings of the Royal Society of London. Series B. Biological Sciences, 205(1161), 531-546. https://doi.org/10.1098/rspb.1979.0083
  • Kirkwood, T. B. L. (2005). Understanding the odd science of aging. Cell, 120(4), 437-447. https://doi.org/10.1016/j.cell.2005.01.027
  • Kirkwood, T. B. L. (1999). Time of Our Lives: The Science of Human Aging. Oxford University Press.
  • Speakman, J. R. (2008). The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B: Biological Sciences363(1490), 375-398.
  • Mitchell, S. E., Simpson, M., Coulet, L., Gouedard, S., Hambly, C., Morimoto, J., Allison, D. B., & Speakman, J. R. (2024). Reproduction has immediate effects on female mortality, but no discernible lasting physiological impacts: A test of the disposable soma theory. PNAS https://doi.org/10.1073/pnas.240868212
  1.    Grandison, R. C., Piper, M. D., & Partridge, L. (2009). Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature462(7276), 1061-1064.

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