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

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          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.

          Abstract

          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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          The Natural Biotic Environment of Caenorhabditis elegans

          Organisms evolve in response to their natural environment. Consideration of natural ecological parameters are thus of key importance for our understanding of an organism’s biology. Curiously, the natural ecology of the model species Caenorhabditis elegans has long been neglected, even though this nematode has become one of the most intensively studied models in biological research. This lack of interest changed ∼10 yr ago. Since then, an increasing number of studies have focused on the nematode’s natural ecology. Yet many unknowns still remain. Here, we provide an overview of the currently available information on the natural environment of C. elegans. We focus on the biotic environment, which is usually less predictable and thus can create high selective constraints that are likely to have had a strong impact on C. elegans evolution. This nematode is particularly abundant in microbe-rich environments, especially rotting plant matter such as decomposing fruits and stems. In this environment, it is part of a complex interaction network, which is particularly shaped by a species-rich microbial community. These microbes can be food, part of a beneficial gut microbiome, parasites and pathogens, and possibly competitors. C. elegans is additionally confronted with predators; it interacts with vector organisms that facilitate dispersal to new habitats, and also with competitors for similar food environments, including competitors from congeneric and also the same species. Full appreciation of this nematode’s biology warrants further exploration of its natural environment and subsequent integration of this information into the well-established laboratory-based research approaches.
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            A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits

            Background The nematode Caenorhabditis elegans is a major laboratory model in biology. Only ten Caenorhabditis species were available in culture at the onset of this study. Many of them, like C. elegans, were mostly isolated from artificial compost heaps, and their more natural habitat was unknown. Results Caenorhabditis nematodes were found to be proliferating in rotten fruits, flowers and stems. By collecting a large worldwide set of such samples, 16 new Caenorhabditis species were discovered. We performed mating tests to establish biological species status and found some instances of semi-fertile or sterile hybrid progeny. We established barcodes for all species using ITS2 rDNA sequences. By obtaining sequence data for two rRNA and nine protein-coding genes, we determined the likely phylogenetic relationships among the 26 species in culture. The new species are part of two well-resolved sister clades that we call the Elegans super-group and the Drosophilae super-group. We further scored phenotypic characters such as reproductive mode, mating behavior and male tail morphology, and discuss their congruence with the phylogeny. A small space between rays 2 and 3 evolved once in the stem species of the Elegans super-group; a narrow fan and spiral copulation evolved once in the stem species of C. angaria, C. sp. 8 and C. sp. 12. Several other character changes occurred convergently. For example, hermaphroditism evolved three times independently in C. elegans, C. briggsae and C. sp. 11. Several species can co-occur in the same location or even the same fruit. At the global level, some species have a cosmopolitan distribution: C. briggsae is particularly widespread, while C. elegans and C. remanei are found mostly or exclusively in temperate regions, and C. brenneri and C. sp. 11 exclusively in tropical zones. Other species have limited distributions, for example C. sp. 5 appears to be restricted to China, C. sp. 7 to West Africa and C. sp. 8 to the Eastern United States. Conclusions Caenorhabditis are "fruit worms", not soil nematodes. The 16 new species provide a resource and their phylogeny offers a framework for further studies into the evolution of genomic and phenotypic characters.
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              Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans.

              Aging is characterized by progressive, degenerative changes in many tissues. To elucidate the relationships among degenerative changes in Caenorhabditis elegans, we developed methods to measure age-related changes quantitatively and analyzed correlations among these changes by using a longitudinal study. The age-related declines of pharyngeal pumping and body movement were positively correlated with each other and lifespan. These findings suggest that the declines of pharyngeal pumping and body movement cause a decline in survival probability or that a shared regulatory system mediates the declines in pharyngeal pumping, body movement, and survival probability. Furthermore, measurements of these processes can be used to predict lifespan and detect premature aging. The declines of physiological processes were measured in daf-2, age-1, daf-16, eat-2, and clk-1 mutants that have altered lifespans. Each mutant strain displayed changes in one or more age-related declines, but the correlations among age-related changes were similar to WT. These measurements were used to generate a system of four stages that describes the aging process and is useful for the analysis of genetic and environmental effects on aging.
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                Author and article information

                Contributors
                david.gems@ucl.ac.uk
                Journal
                Aging Cell
                Aging Cell
                10.1111/(ISSN)1474-9726
                ACEL
                Aging Cell
                John Wiley and Sons Inc. (Hoboken )
                1474-9718
                1474-9726
                16 April 2020
                May 2020
                : 19
                : 5 ( doiID: 10.1111/acel.v19.5 )
                : e13141
                Affiliations
                [ 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@ 123456ucl.ac.uk

                Author information
                https://orcid.org/0000-0001-8891-3362
                https://orcid.org/0000-0002-6653-4676
                Article
                ACEL13141
                10.1111/acel.13141
                7253062
                32301222
                60f4d55c-2869-4f88-af0d-f9384689e2c5
                © 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 http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 31 October 2019
                : 24 January 2020
                : 20 February 2020
                Page count
                Figures: 6, Tables: 0, Pages: 15, Words: 9615
                Funding
                Funded by: BBSRC equipment grant
                Award ID: BB/R01356X/1
                Funded by: Wellcome Trust Strategic Award
                Award ID: 098565/Z/12/Z
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                May 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.3 mode:remove_FC converted:27.05.2020

                Cell biology
                adaptive death,c. elegans ecology,evolution of aging,evolutionary modelling,inclusive fitness

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