Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans
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 t...
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description | 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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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.</description><identifier>ISSN: 1474-9718</identifier><identifier>EISSN: 1474-9726</identifier><identifier>DOI: 10.1111/acel.13141</identifier><identifier>PMID: 32301222</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>adaptive death ; Adults ; Aging ; Altruism ; Animals ; Apoptosis ; C. elegans ecology ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Cellular Senescence - genetics ; Colonies ; Colonies & territories ; Death ; Evolution ; evolution of aging ; evolutionary modelling ; Fecundity ; Fertility - genetics ; Food ; Food availability ; Food consumption ; inclusive fitness ; Larvae ; Life span ; Longevity - genetics ; Nematoda ; Nematodes ; Original ; Population density ; Population growth ; Propagules ; Reproductive fitness ; Senescence ; Sperm ; Worms</subject><ispartof>Aging cell, 2020-05, Vol.19 (5), p.e13141-n/a</ispartof><rights>2020 The Authors. published by the Anatomical Society and John Wiley & Sons Ltd.</rights><rights>2020 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.</rights><rights>COPYRIGHT 2020 John Wiley & Sons, Inc.</rights><rights>2020. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5431-42e20d6aa53f47cbd0a4b9327b5b34911769877f4d15fa152c0e7baade70b48e3</citedby><cites>FETCH-LOGICAL-c5431-42e20d6aa53f47cbd0a4b9327b5b34911769877f4d15fa152c0e7baade70b48e3</cites><orcidid>0000-0002-6653-4676 ; 0000-0001-8891-3362</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7253062/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7253062/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11542,27903,27904,45553,45554,46030,46454,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32301222$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Galimov, Evgeniy R.</creatorcontrib><creatorcontrib>Gems, David</creatorcontrib><title>Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans</title><title>Aging cell</title><addtitle>Aging Cell</addtitle><description>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.</description><subject>adaptive death</subject><subject>Adults</subject><subject>Aging</subject><subject>Altruism</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>C. elegans ecology</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Cellular Senescence - genetics</subject><subject>Colonies</subject><subject>Colonies & territories</subject><subject>Death</subject><subject>Evolution</subject><subject>evolution of aging</subject><subject>evolutionary modelling</subject><subject>Fecundity</subject><subject>Fertility - genetics</subject><subject>Food</subject><subject>Food availability</subject><subject>Food consumption</subject><subject>inclusive fitness</subject><subject>Larvae</subject><subject>Life span</subject><subject>Longevity - genetics</subject><subject>Nematoda</subject><subject>Nematodes</subject><subject>Original</subject><subject>Population density</subject><subject>Population growth</subject><subject>Propagules</subject><subject>Reproductive fitness</subject><subject>Senescence</subject><subject>Sperm</subject><subject>Worms</subject><issn>1474-9718</issn><issn>1474-9726</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kl-PEyEUxYnRuLvVFz-AIfHFbNLKBWaYeTFpmvVP0sQH9RkZuNOymcIKM2v67aV2bXaNWXiAwO-eCyeHkFfAFlDGO2NxWIAACU_IOUgl563i9dPTHpozcpHzNWOgWiaekzPBBQPO-Tn58XUb04iJDr5HaoKjCd1k0dEe7RScH_fUmkB9sAlNRmrjEMOe9n4MmHM5p7c-jZMZ6MpgiGlrulLkM8UBNybkF-RZb4aML-_WGfn-4erb6tN8_eXj59VyPbeVFDCXHDlztTGV6KWynWNGdq3gqqs6IVsAVbeNUr10UPUGKm4Zqs4Yh4p1skExI--PujdTt0NnMYzJDPom-Z1Jex2N1w9vgt_qTbzVileC1bwIvL0TSPHnhHnUO5-Ls4MJGKesuWihVTUUB2fkzT_odZxSKN_TvJJSSFWL6lFKsrptJcA9rY0ZUPvQx_I6e2itl4qpRgBrRKEW_6HKdLjzNgbsfTl_UHB5LLAp5pywPzkBTB9Sow-p0X9SU-DX9707oX9jUgA4Ar9Km_0jUnq5ulofRX8DoDzLRA</recordid><startdate>202005</startdate><enddate>202005</enddate><creator>Galimov, Evgeniy R.</creator><creator>Gems, David</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7TK</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6653-4676</orcidid><orcidid>https://orcid.org/0000-0001-8891-3362</orcidid></search><sort><creationdate>202005</creationdate><title>Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans</title><author>Galimov, Evgeniy R. ; Gems, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5431-42e20d6aa53f47cbd0a4b9327b5b34911769877f4d15fa152c0e7baade70b48e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>adaptive death</topic><topic>Adults</topic><topic>Aging</topic><topic>Altruism</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>C. elegans ecology</topic><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Cellular Senescence - genetics</topic><topic>Colonies</topic><topic>Colonies & territories</topic><topic>Death</topic><topic>Evolution</topic><topic>evolution of aging</topic><topic>evolutionary modelling</topic><topic>Fecundity</topic><topic>Fertility - genetics</topic><topic>Food</topic><topic>Food availability</topic><topic>Food consumption</topic><topic>inclusive fitness</topic><topic>Larvae</topic><topic>Life span</topic><topic>Longevity - genetics</topic><topic>Nematoda</topic><topic>Nematodes</topic><topic>Original</topic><topic>Population density</topic><topic>Population growth</topic><topic>Propagules</topic><topic>Reproductive fitness</topic><topic>Senescence</topic><topic>Sperm</topic><topic>Worms</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Galimov, Evgeniy R.</creatorcontrib><creatorcontrib>Gems, David</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Aging cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Galimov, Evgeniy R.</au><au>Gems, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans</atitle><jtitle>Aging cell</jtitle><addtitle>Aging Cell</addtitle><date>2020-05</date><risdate>2020</risdate><volume>19</volume><issue>5</issue><spage>e13141</spage><epage>n/a</epage><pages>e13141-n/a</pages><issn>1474-9718</issn><eissn>1474-9726</eissn><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.
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.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>32301222</pmid><doi>10.1111/acel.13141</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-6653-4676</orcidid><orcidid>https://orcid.org/0000-0001-8891-3362</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | adaptive death Adults Aging Altruism Animals Apoptosis C. elegans ecology Caenorhabditis elegans Caenorhabditis elegans - genetics Cellular Senescence - genetics Colonies Colonies & territories Death Evolution evolution of aging evolutionary modelling Fecundity Fertility - genetics Food Food availability Food consumption inclusive fitness Larvae Life span Longevity - genetics Nematoda Nematodes Original Population density Population growth Propagules Reproductive fitness Senescence Sperm Worms |
title | Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans |
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