Cold shock induces a terminal investment reproductive response in C. elegans

Abstract

Challenges from environmental stressors have a profound impact on many life-history traits of an organism, including reproductive strategy. Examples across multiple taxa have demonstrated that maternal reproductive investment resulting from stress can improve offspring survival; a form of matricidal provisioning when death appears imminent is known as terminal investment. Here we report a reproductive response in the nematode Caenorhabditis elegans upon exposure to acute cold shock at 2C, whereby vitellogenic lipid movement from the soma to the germline appears to be massively upregulated at the expense of parental survival. This response is dependent on functional TAX-2;TAX-4 cGMP-gated channels that are part of canonical thermosensory mechanisms in worms and can be prevented in the presence of activated SKN-1/Nrf2, the master stress regulator. Increased maternal provisioning promotes improved embryonic cold shock survival, which is notably suppressed in animals with impaired vitellogenesis. These findings suggest that cold shock in C. elegans triggers terminal investment to promote progeny fitness at the expense of parental survival and may serve as a tractable model for future studies of stress-induced progeny plasticity.

GPCR signaling promotes severe stress-induced organismic death inC. elegans

“…SOAT converts accessible cholesterol into ester forms for storage in lipid droplets (Luo et al 2020; Sevanian & Peterson 1986). While the biochemical function of OAC-31 remains further characterized, a recent study showed that cold shock can promote lipid movement from the intestine to the germline (Gulyas & Powell 2021). Interestingly, natural aging of C. elegans is accompanied with autophagy-mediated conversion of intestinal biomass into yolk, contributing to late-life aging pathologies and mortality (Ezcurra et al 2018).…”

“…We postulate that genetic programs underlying stress-induced phenoptosis may have evolved because of antagonistic pleiotropic effects and/or “kin selection” at the population level so that the phenoptosis of adult and weak individuals after severe cold-thermal stress would benefit less stressed and reproductively more privileged ones to facilitate the spreading of genes by fit individuals under resource-limiting and high-stress conditions (Jiang et al 2018; Hamilton 1963; Smith 1964). While evolutionary mechanisms and significance of phenoptosis still remain debatable in the field (Galimov et al 2019; Kirkwood & Melov 2011; Longo et al 2005; Sapolsky 2004; Skulachev 2019), many empirical studies suggest that organisms with clonal population structures such as C. elegans may indeed chronically age or die under stresses by mechanisms (terminal investment, antagonistic pleiotropy, consumer sacrifice or disposable soma) that can benefit its progeny or reproductive success of the organism itself (Ezcurra et al 2018; Galimov & Gems 2020; Gulyas & Powell 2021; Wu et al 2022).…”