Unexpected sex‐specific post‐reproductive lifespan in the free‐living nematodePristionchus exspectatus

Abstract

Patterns of senescence (or aging) can vary among life history traits and between the sexes, providing an opportunity to study variation in the aging process within a single species. We previously found that females of the nematode Pristionchus exspectatus outlive males by a substantial margin under laboratory conditions. Here, we show that sex-specific reproductive senescence unfolds in the opposite direction in this species, resulting in a prolonged period of female-specific post-reproductive survival: females lost the ability to reproduce at approximately 4.7 weeks despite a median lifespan of about 12.3 weeks under lab conditions, whereas males lost the ability to reproduce at approximately 6.6 weeks, roughly in line with their median lifespan of around 7.6 weeks. Interestingly, somatic senescence (declining crawling speed) only explained reproductive senescence in males, whereas females lost the ability to reproduce regardless of condition. However, we found that housing females with males significantly increased their mortality rate, indicating that female-specific post-reproductive survival is unlikely to occur in the wild. We discuss our results in light of evolutionary theories of post-reproductive survival and previous studies of nematode behavioral ecology, arguing that premature reproductive senescence may stem from sex-specific condition-dependent survival during the reproductive period. Given the proven lab tractability of Prisitonchus nematodes, our findings provide a foundation for integrative research that combines evolutionary ecology and molecular genetics in the study of sex-specific senescence and post-reproductive survival.

Hybrid crosses and the genetic basis of interspecific divergence in lifespan inPristionchusnematodes

“…The simplest phylogenetic interpretation of our findings is that long lifespan is the ancestral state and that recessive lifespan‐shortening alleles arose and fixed independently in P. pacificus and P. arcanus . However, the phylogenetic pattern uncovered by our previous work argues against this simple scenario: the long lifespan of P. exspectatus females appears to be an evolutionarily recent phenomenon, as does the particularly short lifespan of P. pacificus hermaphrodites, whereas the intermediate lifespan of P. arcanus females is roughly in line with that of females from most other dioecious species studied to date (Weadick & Sommer, , b). Elucidating the molecular genetics of lifespan variation in the P. pacificus species complex will be necessary before we can fully reconstruct the evolutionary timing of key substitutions in this group (e.g.…”

“…). Given the evolutionary relationships within this group, these findings indicate that variation in female/hermaphrodite longevity stems from both a reduction along the hermaphroditic P. pacificus lineage and an increase along the P. exspectatus lineage (Weadick & Sommer, , b). However, the genetic basis of lifespan differences among these closely related species remains unaddressed.…”

No time to die: Evolution of a post‐reproductive life stage

“…However, extended parental care occurs in many mammalian species. Mammals are characterized by low frequencies of bi-parental care (Stockley & Hobson, 2016), with fathers contributing in Alberts et al, 2013;Atwood et al, 2017;Auld, 2018;Austad, 1994;Chapman, Jackson, et al, 2019;Cohen, 2004;Croft et al, 2015;Ellis, Franks, Nattrass, Currie, et al, 2018;Finch & Holmes, 2010;Foote, 2008;Foster et al, 2012;Jervis et al, 1994;Kasuya et al, 1988;Kern et al, 2021;Klepsatel et al, 2013;Lahdenper€ a et al, 2014;Levitis et al, 2013;Levitis & Lackey, 2011;Nichols et al, 2016;Reznick et al, 2005;Uematsu et al, 2010); Walker & Herndon, 2008;Weadick & Sommer, 2016. just 10% of known mammalian genera. It is possible that a decline in the ability of females to provide an adequate level care to offspring later in life may be part of the picture for those mammals showing PRLS.…”

“…Phylogenetic tree of 52 species showing Post‐reproductive Representation (PrR) values above 0.10 coloured by their captivity status (wild = Pink, semi‐captive = Green, human = Black, and captive = Blue). Significant PrR values (discussed in the Appendix S1) are found in Elephas maximus , Orcinus orca , Monodon monoceros , Delphinapterus leucas , Globicephala macrorhynchus , and Homo sapiens (References: Alberts et al., 2013; Atwood et al., 2017; Auld, 2018; Austad, 1994; Chapman, Jackson, et al., 2019; Cohen, 2004; Croft et al., 2015; Ellis, Franks, Nattrass, Cant, et al., 2018; Ellis, Franks, Nattrass, Currie, et al., 2018; Finch & Holmes, 2010; Foote, 2008; Foster et al., 2012; Jervis et al., 1994; Kasuya et al., 1988; Kern et al., 2021; Klepsatel et al., 2013; Lahdenperä et al., 2014; Levitis et al., 2013; Levitis & Lackey, 2011; Nichols et al., 2016; Reznick et al., 2005; Uematsu et al., 2010); Walker & Herndon, 2008; Weadick & Sommer, 2016.…”