Semelparous Death as one Element of Iteroparous Aging Gone Large

Abstract

The aging process in semelparous and iteroparous species is different, but how different? Death in semelparous organisms (e.g., Pacific salmon) results from suicidal reproductive effort (reproductive death). Aging (senescence) in iteroparous organisms such as humans is often viewed as a quite different process. Recent findings suggest that the nematode Caenorhabditis elegans, widely used to study aging, undergoes reproductive death. In post-reproductive C. elegans hermaphrodites, intestinal biomass is repurposed to produce yolk which when vented serves as a milk to support larval growth. This apparent benefit of lactation comes at the cost of intestinal atrophy in the mother. Germline removal and inhibition of insulin/IGF-1 signaling (IIS) suppress C. elegans reproductive pathology and greatly increase lifespan. Blocking sexual maturity, e.g., by gonadectomy, suppresses reproductive death thereby strongly increasing lifespan in semelparous organisms, but typically has little effect on lifespan in iteroparous ones. Similarly, reduced IIS causes relatively modest increases in lifespan in iteroparous organisms. We argue that the more regulated and plastic mechanisms of senescence in semelparous organisms, involving costly resource reallocation under endocrine control, exist as one extreme of an etiological continuum with mechanisms operative in iteroparous organisms. We suggest that reproductive death evolved by exaggeration of mechanisms operative in iteroparous species, where other mechanisms also promote senescence. Thus, knowledge of C. elegans senescence can guide understanding of mechanisms contributing to human aging.

A Year at the Forefront of Proteostasis and Aging

“…This might have significant implications since it increases the chance that interventions that extend worm's lifespan will not translate to higher organisms, and underscores the importance of understanding the evolutionary logic at work in the models used to study aging. The authors of this study further argue that semelparity and iteoparity likely exist on a continuum rather than as fully distinct categories ( Kern and Gems, 2022 ; Kern et al, 2020 preprint). Many researchers view mouse lifespans as the gold standard of a bona fide pro-longevity intervention.…”

“…While these organisms vary in complexity, the rationale for choosing them for lifespan studies is that these animals have fast development and are short-lived. Recent work, however, suggests that C. elegans is a semelparous species, undergoing reproductive death ( Kern and Gems, 2022 ). This might have significant implications since it increases the chance that interventions that extend worm's lifespan will not translate to higher organisms, and underscores the importance of understanding the evolutionary logic at work in the models used to study aging.…”

Forever Young

“…We can also survive the life stage of reproduction by decades. All is not lost, however, as Carina Kern and David Gems explain in a recent review [5] . Strategies like the postreproductive self-destruction of C. elegans may well be evolutionarily related to the more gradual decay in mammalian ageing.…”

Fisher & Salguero-Gomez reproductive death final with tables

“…Dasyurid marsupials in the genera Antechinus, Phascogale, and Dasykaluta are often considered to be the only semelparous terrestrial vertebrates (e.g. Kern and Gems 2022).…”

“…When residual reproductive value (the remaining reproduction expected in an organism's life) is low, unrestrained reproductive effort can maximise fitness. Indeed, terminal investment increases fitness if there is a survival cost of reproduction, and when concentrated investment in breeding kills the parent this is 'reproductive death' (Kern and Gems 2022). Semelparity resulting from reproductive death is thus terminal investment in the first reproductive event.…”