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

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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.


          Caenorhabditis elegans fitness can be viewed at the level of individual animals or of viscous, clonal populations of worms (or colonies). Behavior of an in silico model of C. elegans predicts that early death of postreproductive adults can increase colony fitness (measured as yield of dauer propagules) by reducing futile food consumption. This supports the occurrence of apoptosis‐like programmed organismal death in C. elegans, of the consumer sacrifice type, which limits lifespan.

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          Most cited references 57

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          The genetical evolution of social behaviour. I.

           W.D. Hamilton (1964)
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            The genetics of ageing.

            The nematode Caenorhabditis elegans ages and dies in a few weeks, but humans can live for 100 years or more. Assuming that the ancestor we share with nematodes aged rapidly, this means that over evolutionary time mutations have increased lifespan more than 2,000-fold. Which genes can extend lifespan? Can we augment their activities and live even longer? After centuries of wistful poetry and wild imagination, we are now getting answers, often unexpected ones, to these fundamental questions.
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              Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection.

              From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not. The potential for such semantic confusion is greatest with interdisciplinary research. Our aim here is to address issues of semantic confusion that have arisen with research on the problem of cooperation. In particular, we: (i) discuss confusion over the terms kin selection, mutualism, mutual benefit, cooperation, altruism, reciprocal altruism, weak altruism, altruistic punishment, strong reciprocity, group selection and direct fitness; (ii) emphasize the need to distinguish between proximate (mechanism) and ultimate (survival value) explanations of behaviours. We draw examples from all areas, but especially recent work on humans and microbes.

                Author and article information

                Aging Cell
                Aging Cell
                Aging Cell
                John Wiley and Sons Inc. (Hoboken )
                16 April 2020
                May 2020
                : 19
                : 5 ( doiID: 10.1111/acel.v19.5 )
                [ 1 ] Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment University College London London UK
                Author notes
                [* ] Correspondence

                David Gems, Institute of Healthy Ageing, and Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK.

                Email: david.gems@

                © 2020 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.

                This is an open access article under the terms of the License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 6, Tables: 0, Pages: 15, Words: 9615
                Funded by: BBSRC equipment grant
                Award ID: BB/R01356X/1
                Funded by: Wellcome Trust Strategic Award
                Award ID: 098565/Z/12/Z
                Original Article
                Original Articles
                Custom metadata
                May 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.3 mode:remove_FC converted:27.05.2020


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