Does senescence promote fitness in Caenorhabditis elegans by causing death?

Lohr, Jennifer; Galimov, Evgeniy R.; Gems, David

doi:10.1016/j.arr.2019.01.008

Cited by 41 publications

(99 citation statements)

References 154 publications

(230 reference statements)

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“…Each form of futile consumption can be minimized by life history optimization. Futile adult food consumption can be avoided by adaptive death not only in postreproductive adults, as previously proposed (Lohr et al, 2019), but also in adults with continuous reproduction (Figures 3e, and ) since on a dwindling food patch they become postreproductive as far as dauer yield is concerned (Figure 6d). Futile food consumption in postreproductive adults can also be reduced by a programmed age decline in food consumption rate (Huang et al, 2004), which our findings suggest could have evolved to promote colony fitness (Figure ).…”

Section: Discussionsupporting

confidence: 70%

“…In our model, we varied M2 from 0.99 (mean lifespan 12 days) to 0.8 (mean lifespan 2.4 days), see Figure 2f,g. Although under standard laboratory conditions lifespan is 2–3 weeks (Klass, 1977), C. elegans in the wild certainly experience much shorter lifespans to which genetic determinants are likely to contribute (Lohr et al, 2019); thus, though our model tests benefits of programmed aging, we assume that extrinsic factors (especially infection and starvation) will amplify its effects. Available evidence suggests that wild C. elegans colonies typically exist as clonal populations of selfing hermaphrodites with barely any males (Barriere & Felix, 2007; Frezal & Felix, 2015; Petersen et al, 2015; Richaud, Zhang, Lee, Lee, & Félix, 2018).…”

Section: Resultsmentioning

confidence: 99%

“…That early death increases fitness when reproductive span is short is consistent with the occurrence of consumer sacrifice. According to this interpretation, postreproductive parents compete with their progeny for a limited food supply, such that programmed death in older adults increases food availability for progeny, thereby increasing dauer yield (Lohr et al, 2019). To test this further, we limited reproduction to day 1 of adulthood and increased competition between parents and larvae by increasing reproductive output from 2 to up to 50 progeny per worm.…”

Section: Resultsmentioning

confidence: 99%

“…Androdioecy (having hermaphrodites and males) in C. elegans arose by evolution from an ancestor that was gonochoristic (having females and males; Ellis & Lin, 2014; Kiontke et al, 2011; Stewart & Phillips, 2002). This led us previously to suggest that adaptive death in Caenorhabditis species might evolve only after the appearance of hermaphroditism (Lohr et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans

Galimov

Gems

2020

Aging Cell

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In the nematode Caenorhabditis elegans, loss of function of many genes leads to increases in lifespan, sometimes of a very large magnitude. Could this reflect the occurrence of programmed death that, like apoptosis of cells, promotes fitness? The notion that programmed death evolves as a mechanism to remove worn out, old individuals in order to increase food availability for kin is not supported by classic evolutionary theory for most species. However, it may apply in organisms with colonies of closely related individuals such as C. elegans in which largely clonal populations subsist on spatially limited food patches. Here, we ask whether food competition between nonreproductive adults and their clonal progeny could favor programmed death by using an in silico model of C. elegans. Colony fitness was estimated as yield of dauer larva propagules from a limited food patch. Simulations showed that not only shorter lifespan but also shorter reproductive span and reduced adult feeding rate can increase colony fitness, potentially by reducing futile food consumption. Early adult death was particularly beneficial when adult food consumption rate was high. These results imply that programmed, adaptive death could promote colony fitness in C. elegans through a consumer sacrifice mechanism. Thus, C. elegans lifespan may be limited not by aging in the usual sense but rather by apoptosis‐like programmed death.

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Section: Discussionsupporting

confidence: 70%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans

Galimov

Gems

2020

Aging Cell

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“…Work from Haldane, Medawar, Hamilton and others predicts that the declining force of natural selection after reproductive maturation should inevitably lead to the accumulation of deleterious gene variants, resulting in increased mortality later in life (Haldane, 1941; Medawar, 1952; Hamilton, 1966; Charlesworth, 2000). While these mutation-accumuation theories of ageing explain ageing as a fundamentally non-adaptive process, other evolutionary theories of ageing suggest senescence could evolve as an antagonistic side-effect of positively-selected traits (Williams, 1957), or even as a kin- or group-selected adaptation in its own right (Longo et al, 2005; Lohr et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

AEGIS: An In Silico Tool to model Genome Evolution in Age-Structured Populations

Bradshaw

Šajina

Valenzano

2019

Preprint

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9AEGIS (Ageing of Evolving Genomes In Silico) is a versatile population-genetics numerical-simulation tool 10 that enables the evolution of life history trajectories under sexual and asexual reproduction and a wide variety 11 of evolutionary constraints. By encoding age-specific survival and reproduction probabilities as discrete ge-12 nomic elements, AEGIS allows these probabilities to evolve freely and independently over time. Simulation 13 of population evolution with AEGIS demonstrates that ageing-like phenotypes evolve in stable environments 14 under a wide range of conditions, that life history trajectories depend heavily on mutation rates, and that sexual 15 populations are better able to accumulate high levels of beneficial mutations affecting early-life survival and 16 reproduction. AEGIS is free and open-source, and aims to become a standard reference tool in the study of 17 life-history evolution and the evolutionary biology of ageing. 18Species in nature vastly differ in life histories, with dramatic variation in maturation rate, lifespan, and fecun-20 dity. In general, age-dependent mortality increases as a function of age while age-dependent fecundity declines, 21 a phenomenon known as ageing or senescence. However, in some organisms mortality decreases or remains 22 constant through life, while fecundity remains constant or increases (Jones et al., 2014). These difference in 23 demography can have important effects on fitness, giving rise to dramatic differences in lifetime reproductive 24 output between species. 25The evolution of age-dependent changes in mortality and reproduction has been an important object of the-26 oretical investigation since the dawn of population genetics, giving rise to a number of theories to explain the 27 widespread occurrence of senescence in nature. Work from Haldane, Medawar, Hamilton and others predicts 28 that the declining force of natural selection after reproductive maturation should inevitably lead to the accumu-29 lation of deleterious gene variants, resulting in increased mortality later in life (Haldane, 1941; Medawar, 1952; 30 Hamilton, 1966; Charlesworth, 2000). While these mutation-accumuation theories of ageing explain ageing as 31 a fundamentally non-adaptive process, other evolutionary theories of ageing suggest senescence could evolve 32 1 as an antagonistic side-effect of positively-selected traits (Williams, 1957), or even as a kin-or group-selected 33 adaptation in its own right (Longo et al., 2005; Lohr et al., 2019). 34Up to now, the evolution of life-history traits, including age-dependent changes in survival and reproduc-35 tion, has primarily been performed using analytical approaches (Hamilton, 1966; Charlesworth, 1994; Fisher, 36 1930); while some simple numerical models exploring the evolution of ageing have been proposed (Penna, 37 1995; Dzwinel et al., 2005; Werfel et al., 2015), there remains a need for a flexible simulation tool to model the 38 evolution of ageing. In particular, a model which permits independent evolut...

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Natural Ecosystems and Earth’s Habitability: Attempting a Cross-Disciplinary Synthesis

Makarieva

2021

Strategies for Sustainability of the Earth System

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Does senescence promote fitness in Caenorhabditis elegans by causing death?

Cited by 41 publications

References 154 publications

Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans

Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans

AEGIS: An In Silico Tool to model Genome Evolution in Age-Structured Populations

Natural Ecosystems and Earth’s Habitability: Attempting a Cross-Disciplinary Synthesis

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