title: Does the degree of endocrine dyscrasia post-reproduction dictate post-reproductive lifespan? Lessons from semelparous and iteroparous species.
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.
authors.affiliation: 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. csa@medicine.wisc.edu.|Geriatric Research, Education and Clinical Center, Veterans Administration Hospital, Madison, WI, 53705, USA. csa@medicine.wisc.edu.|School of Exercise, Biomedical and Health Sciences, Edith Cowan University, Joondalup, WA, 6027, Australia. csa@medicine.wisc.edu.
authors.forename: Craig S
authors.initials: CS
authors.lastname: Atwood
authors.affiliation: 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.
authors.forename: Kentaro
authors.initials: K
authors.lastname: Hayashi
authors.affiliation: 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.
authors.forename: Sivan Vadakkadath
authors.initials: SV
authors.lastname: Meethal
authors.affiliation: 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.
authors.forename: Tina
authors.initials: T
authors.lastname: Gonzales
authors.affiliation: Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, USA.
authors.forename: Richard L
authors.initials: RL
authors.lastname: Bowen
mesh_terms: D000818:Animals; D004703:Endocrine System / Q000378:metabolism* / Q000502:physiology; D005260:Female; D005640:Follicle Stimulating Hormone / Q000378:metabolism*; D012739:Gonadal Steroid Hormones / Q000378:metabolism*; D008136:Longevity; D008297:Male; D008394:Marsupialia / Q000378:metabolism; D012098:Reproduction / Q000502:physiology; D012474:Salmon / Q000378:metabolism; D012741:Sexual Maturation / Q000502:physiology; D013739:Testosterone / Q000378:metabolism*
chemical_list: D012739:Gonadal Steroid Hormones; D013739:Testosterone; D005640:Follicle Stimulating Hormone
keywords: Iteroparous; Menopause; Post-reproductive lifespan; Salmon; Semelparous; Sex hormones