Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes

Abstract

Sexual interactions have a potent influence on health in several species, including mammals. Previous work in C. elegans identified strategies used by males to accelerate the demise of the opposite sex (hermaphrodites). But whether hermaphrodites evolved counter-strategies against males remains unknown. Here we discover that young C. elegans hermaphrodites are remarkably resistant to brief sexual encounters with males, whereas older hermaphrodites succumb prematurely. Surprisingly, it is not their youthfulness that protects young hermaphrodites, but the fact that they have self-sperm. The beneficial effect of self-sperm is mediated by a sperm-sensing pathway acting on the soma rather than by fertilization. Activation of this pathway in females triggers protection from the negative impact of males. Interestingly, the role of self-sperm in protecting against the detrimental effects of males evolved independently in hermaphroditic nematodes. Endogenous strategies to delay the negative effect of mating may represent a key evolutionary innovation to maximize reproductive success.

Insulin-like peptides and the mTOR-TFEB pathway protect Caenorhabditis elegans hermaphrodites from mating-induced death

“…The presence of self-sperm in young hermaphrodites protects them from brief mating-induced death (Booth et al, 2019; Figure 1A,B). Unlike older hermaphrodites, young hermaphrodites that mate during a brief interaction with males are protected from this mating-induced death (Booth et al, 2019; Figure 1A,B). By contrast, young feminized (i.e.…”

“…By contrast, young feminized (i.e. lacking self-sperm; fog-2(q71), fem-1(hc17) ) worms exhibit significant acceleration of death after brief mating with males (Booth et al, 2019; Figure 1C, Figure 1—figure supplement 1A), suggesting that self-sperm are protective.…”

“…Our transcriptional data revealed that spermless females differ not only in expression of sperm proteins and ins-37 but also in genes whose promoters contain the predicted binding motif for the HLH-30/TFEB transcription factor (Reimand et al, 2007; Grove et al, 2009; Figure 3—figure supplement 1), which has been previously implicated in longevity regulation through its control of lipid metabolism and lysosomal autophagy. Mutants that produce an excess of self-sperm ( fem-3(q20)) (Rosenquist and Kimble, 1988) are protected from brief mating-induced death for a longer period of their lifespan than wild-type hermaphrodites (Booth et al, 2019), and we found that the HLH-30 binding motif is also enriched in promoters of genes that are up-regulated in ( fem-3(q20)) hermaphrodites compared to animals with normal levels of sperm (Figure 3—figure supplement 1; Supplementary file 3).…”

“…We noted previously that mating-induced death occurs only after C. elegans hermaphrodites produce all their progeny (Shi and Murphy, 2014); this delay is necessary for successful reproduction, but the underlying mechanism allowing this balance was previously unknown. In an accompanying manuscript, Booth et al report that self-sperm are protective against short-term mating-induced death specifically in hermaphroditic mothers (Booth et al, 2019). Here, we describe the molecular mechanism that hermaphrodites use to prevent early SF-induced death until self-sperm are depleted.…”

A new defense in the battle of the sexes

“…In one paper Anne Brunet of Stanford University and co-workers – including Lauren Booth as first author with Travis Maures, Robin Yeo, and Cindy Tantilert – report that self-sperm protects C. elegans against aging by activating the 'sperm-sensing' pathway (Booth et al, 2019). Young hermaphrodite worms that mate have normal lifespans, while old worms die soon after mating.…”