Abstract
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.
Highlights
Aging is a ubiquitous feature of living organisms but does it have any biological function? Several contemporaries of Charles Darwin proposed that it does: according to August Weismann and Alfred Russel Wallace, aging serves to remove worn out individuals, thereby increasing food availability for the benefit of the species (Rose, 1991)
A full understanding of C. elegans biology should include an account of how it optimizes fitness, but how should fitness be understood? We have proposed that C. elegans life history has evolved to maximize colony fitness, measurable in terms of number of dauer colony propagules
Our findings suggest the importance of three types of futile food consumption: first, as initially proposed, food consumption
Summary
Aging (senescence) is a ubiquitous feature of living organisms but does it have any biological function? Several contemporaries of Charles Darwin proposed that it does: according to August Weismann and Alfred Russel Wallace, aging serves to remove worn out individuals, thereby increasing food availability for the benefit of the species (Rose, 1991). Modern evolutionary theory, supported by population genetic analysis, indicates that extreme altruism of this type will not be favored by natural selection, at least not in organisms that exist as dispersed, outbred populations (Hamilton, 1964; Maynard Smith, 1976; Williams, 1966). This is because of the vulnerability of suicidal altruists to exploitation by nonsuicidal, nonaltruists (egoists; Figure 1a). Death of postreproductive adults in viscous populations could benefit isogenic larvae and reproductive adults by increasing food availability, an example of consumer sacrifice adaptive death (Lohr et al, 2019)
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