C. eleganshermaphrodites undergo semelparous reproductive death

Abstract

Ageing in the nematode Caenorhabditis elegans is unusual in terms of the severity and early onset of senescent pathology, particularly affecting organs involved in reproduction (Ezcurra et al., 2018; Garigan et al., 2002; Herndon et al., 2002). In post-reproductive C. elegans hermaphrodites, intestinal biomass is converted into yolk leading to intestinal atrophy and yolk steatosis (Ezcurra et al., 2018; Sornda et al., 2019). We recently showed that post-reproductive mothers vent yolk which functions as a milk (yolk milk), supporting larval growth that is consumed by larvae (Kern et al., 2020). This form of massive reproductive effort involving biomass repurposing leading to organ degeneration is characteristic of semelparous organisms (i.e. that exhibit only a single reproductive episode) ranging from monocarpic plants to Pacific salmon where it leads to rapid death (reproductive death) (Finch, 1990; Gems et al., 2020). Removal of the germline greatly increases lifespan in both C. elegans and Pacific salmon, in the latter case by suppressing semelparous reproductive death (Hsin and Kenyon, 1999; Robertson, 1961). Here we present evidence that reproductive death occurs in C. elegans, and that it is suppressed by germline removal, leading to extension of lifespan. Comparing three Caenorhabditis sibling species pairs with hermaphrodites and females, we show that lactation and massive early pathology only occurs in the former. In each case, hermaphrodites are shorter lived and only in hermaphrodites does germline removal markedly increase lifespan. Semelparous reproductive death has previously been viewed as distinct from ageing; however, drawing on recent theories of ageing (Blagosklonny, 2006; de Magalhães and Church, 2005; Maklakov and Chapman, 2019), we argue that it involves exaggerated versions of programmatic mechanisms that to a smaller extent contribute to ageing in non-semelparous species. Thus, despite the presence of reproductive death, mechanisms of ageing in C. elegans are informative about ageing in general.

Reproductive Suicide: Similar Mechanisms of Aging in C. elegans and Pacific Salmon

“…Moreover, for all three sibling species pairs, hermaphrodites vent yolk and lay unfertilized oocytes, while females do not. However, senescent degeneration was seen in females after mating (Kern et al, 2020). Taken together, these results suggest that after the appearance of hermaphroditism in each instance, reproductive death evolved from being facultative (mating induced) to constitutive.…”

“…Could germline ablation in C. elegans hermaphrodites extend lifespan by preventing reproductive death? Supporting this, intestinal atrophy is suppressed by germline removal (Ezcurra et al, 2018;Kern et al, 2020). Moreover, the DAF-16/FOXO transcription factor is required for both life extension (Hsin and Kenyon, 1999) and suppression of intestinal atrophy (Ezcurra et al, 2018) by germline removal.…”

“…We recently examined the pattern of senescent pathology in two additional Caenorhabditis species that are, like C. elegans, androdioecious (with hermaphrodites and males), C. briggsae and C. tropicalis, and found them to be similar to C. elegans, suggesting the occurrence of reproductive death in these species too (Kern et al, 2020). The majority of Caenorhabditis species are gonochoristic (with females and males), and C. elegans, C. briggsae and C. tropicalis represent three independent occurrences of the evolution of androdioecy (Kiontke et al, 2011).…”

“…We recently proposed that two forms of programmatic aging are major determinants of C. elegans lifespan: adaptive death, which promotes fitness (i.e., provides a fitness benefit) in a manner similar to apoptosis (Lohr et al, 2019;Gems, 2020, 2021), and reproductive death (Kern et al, 2020(Kern et al, , 2021. In this essay, we explore further the possibility that C. elegans undergoes semelparous reproductive death by comparing it with other organisms known to undergo reproductive death.…”

C. elegansprovide milk for their young

“…4d). This conclusion is supported by comparative analysis of other Caenorhabditis species which shows that reproductive death is promoted by the germline in hermaphrodites but absent in unmated females (Kern et al, 2020), and by comparison with other organisms that exhibit reproductive death (Gems et al, 2020). We have argued elsewhere that reproductive death can facilitate the evolution of programmed adaptive death, which further shortens lifespan (Galimov and Gems, 2020; Lohr et al, 2019).…”