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Does the degree of endocrine dyscrasia post-reproduction dictate post-reproductive lifespan? Lessons from semelparous and iteroparous species

GeroScience volume 39, pages 103–116 (2017)Cite this article

Abstract

Post-reproductive lifespan varies greatly among species; human post-reproductive lifespan comprises ~30–50% of their total longevity, while semelparous salmon and dasyurid marsupials post-reproductive lifespan comprises <4% of their total longevity. To examine if the magnitude of hypothalamic-pituitary-gonadal (HPG) axis dyscrasia at the time of reproductive senescence determines post-reproductive lifespan, we examined the difference between pre- and post-reproductive (1) circulating sex hormones and (2) the ratio of sex steroids to gonadotropins (e.g., 17β-estradiol/follicle-stimulating hormone (FSH)), an index of the dysregulation of the HPG axis and the level of dyotic (death) signaling post-reproduction. Animals with a shorter post-reproductive lifespan (<4% total longevity) had a more marked decline in circulating sex steroids and corresponding elevation in gonadotropins compared to animals with a longer post-reproductive lifespan (30–60% total longevity). In semelparous female salmon of short post-reproductive lifespan (1%), these divergent changes in circulating hormone concentration post-reproduction equated to a 711-fold decrease in the ratio of 17β-estradiol/FSH between the reproductive and post-reproductive periods. In contrast, the decrease in the ratio of 17β-estradiol/FSH in iteroparous female mammals with long post-reproductive lifespan was significantly less (1.7–34-fold) post-reproduction. Likewise, in male semelparous salmon, the decrease in the ratio of testosterone/FSH (82-fold) was considerably larger than for iteroparous species (1.3–11-fold). These results suggest that (1) organisms with greater reproductive endocrine dyscrasia more rapidly undergo senescence and die, and (2) the contribution post-reproduction by non-gonadal (and perhaps gonadal) tissues to circulating sex hormones dictates post-reproductive tissue health and longevity. In this way, reproduction and longevity are coupled, with the degree of non-gonadal tissue hormone production dictating the rate of somatic tissue demise post-reproduction and the differences in post-reproductive lifespans between species.

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Acknowledgements

This material is the result of work supported with resources at the William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin. The opinions expressed herein are those of the authors. The contents do not represent the views of the Department of Veterans Affairs or the US Government. This is Geriatrics Research, Education and Clinical Center VA paper # 2017–006.

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Affiliations

  1. Division of Geriatrics and Gerontology, Department of Medicine, University of Wisconsin-Madison School of Medicine and Public Health, William S. Middleton Memorial VA (GRECC 11G), 2500 Overlook Terrace, Madison, WI, 53705, USA

    Craig S. Atwood, Kentaro Hayashi, Sivan Vadakkadath Meethal & Tina Gonzales

  2. Geriatric Research, Education and Clinical Center, Veterans Administration Hospital, Madison, WI, 53705, USA

    Craig S. Atwood

  3. School of Exercise, Biomedical and Health Sciences, Edith Cowan University, Joondalup, WA, 6027, Australia

    Craig S. Atwood

  4. Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, USA

    Richard L. Bowen

Authors
  1. Craig S. Atwood
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  2. Kentaro Hayashi
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  3. Sivan Vadakkadath Meethal
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  4. Tina Gonzales
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  5. Richard L. Bowen
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Correspondence to Craig S. Atwood.

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Atwood, C.S., Hayashi, K., Meethal, S.V. et al. Does the degree of endocrine dyscrasia post-reproduction dictate post-reproductive lifespan? Lessons from semelparous and iteroparous species. GeroScience 39, 103–116 (2017). https://doi.org/10.1007/s11357-016-9955-5

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  • DOI: https://doi.org/10.1007/s11357-016-9955-5

Keywords

  • Post-reproductive lifespan
  • Sex hormones
  • Semelparous
  • Iteroparous
  • Menopause
  • Salmon