Minor variations in multicellular life cycles have major effects on adaptation

Multicellularity has evolved several independent times over the past hundreds of millions of years and given rise to a wide diversity of complex life. Recent studies have found that large differences in the fundamental structure of early multicellular life cycles can affect fitness and influence mul...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:PLoS computational biology 2023-04, Vol.19 (4), p.e1010698-e1010698
Hauptverfasser: Isaksson, Hanna, Brännström, Åke, Libby, Eric
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page e1010698
container_issue 4
container_start_page e1010698
container_title PLoS computational biology
container_volume 19
creator Isaksson, Hanna
Brännström, Åke
Libby, Eric
description Multicellularity has evolved several independent times over the past hundreds of millions of years and given rise to a wide diversity of complex life. Recent studies have found that large differences in the fundamental structure of early multicellular life cycles can affect fitness and influence multicellular adaptation. Yet, there is an underlying assumption that at some scale or categorization multicellular life cycles are similar in terms of their adaptive potential. Here, we consider this possibility by exploring adaptation in a class of simple multicellular life cycles of filamentous organisms that only differ in one respect, how many daughter filaments are produced. We use mathematical models and evolutionary simulations to show that despite the similarities, qualitatively different mutations fix. In particular, we find that mutations with a tradeoff between cell growth and group survival, i.e. "selfish" or "altruistic" traits, spread differently. Specifically, altruistic mutations more readily spread in life cycles that produce few daughters while in life cycles producing many daughters either type of mutation can spread depending on the environment. Our results show that subtle changes in multicellular life cycles can fundamentally alter adaptation.
doi_str_mv 10.1371/journal.pcbi.1010698
format Article
fullrecord <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_2814443796</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A748728906</galeid><doaj_id>oai_doaj_org_article_3efc14b0c6e44136bface5c5eea95dc1</doaj_id><sourcerecordid>A748728906</sourcerecordid><originalsourceid>FETCH-LOGICAL-c621t-915a97f5c16d048cc46c5e2c19e98e0d2b0777f5c6a2f124dad91a64cb0cc86a3</originalsourceid><addsrcrecordid>eNqVksuO0zAUhiMEYobCGyCIxAYWLXbiS7xCo-FWaRgkblvrxDnpuHLiYieFeXuctjOaIjbIC1v29_8-tyx7SsmClpK-Xvsx9OAWG1PbBSWUCFXdy04p5-Vclry6f-d8kj2KcU1IOirxMDspJalKIflpdvnJ9j7kWwgWBuv7mNs-70Y3WIPOjQ5C7myLubk2DmN-BVvMO1gnCbYtmiHmvs-hgc2wkz_OHrTgIj457LPs-_t3384_zi8-f1ien13MjSjoMFeUg5ItN1Q0hFXGMGE4FoYqVBWSpqiJlNO7gKKlBWugURQEMzUxphJQzrLne9-N81EfShF1UVHGWCmVSMRyTzQe1noTbAfhWnuwenfhw0pDSFk61CW2hrJkLZAxWoq6BYM8BYSgeGNo8prvveIv3Iz1kdtb--Ns5zZ2oy6IKiqW-DeH6Ma6w8ZgPwRwR7Ljl95e6ZXf6tRGLgiXyeHlwSH4nyPGQXc2Th2BHv04JUo4KSlPLZ1lL_5C_12OxZ5aQcrY9q1PH5u0Guys8T22Nt2fSVbJolJkErw6EiRmwN_DCsYY9fLrl_9gL49ZtmdN8DEGbG_LQomeBvsmfD0Ntj4MdpI9u1vSW9HNJJd_AOr-9fs</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2814443796</pqid></control><display><type>article</type><title>Minor variations in multicellular life cycles have major effects on adaptation</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central</source><source>SWEPUB Freely available online</source><source>Public Library of Science (PLoS)</source><creator>Isaksson, Hanna ; Brännström, Åke ; Libby, Eric</creator><creatorcontrib>Isaksson, Hanna ; Brännström, Åke ; Libby, Eric</creatorcontrib><description>Multicellularity has evolved several independent times over the past hundreds of millions of years and given rise to a wide diversity of complex life. Recent studies have found that large differences in the fundamental structure of early multicellular life cycles can affect fitness and influence multicellular adaptation. Yet, there is an underlying assumption that at some scale or categorization multicellular life cycles are similar in terms of their adaptive potential. Here, we consider this possibility by exploring adaptation in a class of simple multicellular life cycles of filamentous organisms that only differ in one respect, how many daughter filaments are produced. We use mathematical models and evolutionary simulations to show that despite the similarities, qualitatively different mutations fix. In particular, we find that mutations with a tradeoff between cell growth and group survival, i.e. "selfish" or "altruistic" traits, spread differently. Specifically, altruistic mutations more readily spread in life cycles that produce few daughters while in life cycles producing many daughters either type of mutation can spread depending on the environment. Our results show that subtle changes in multicellular life cycles can fundamentally alter adaptation.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1010698</identifier><identifier>PMID: 37083675</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acclimatization ; Adaptation ; Adaptation (Biology) ; Altruism ; Analysis ; Animals ; Biological Evolution ; Biology and Life Sciences ; Cell survival ; Cooperation ; Daughters ; Evolution ; Filaments ; Life Cycle Stages ; Life cycles ; Life cycles (Biology) ; Mathematical models ; Models, Theoretical ; Mutation ; Mutation (Biology) ; Phenotype ; Physical Sciences ; Research and Analysis Methods</subject><ispartof>PLoS computational biology, 2023-04, Vol.19 (4), p.e1010698-e1010698</ispartof><rights>Copyright: © 2023 Isaksson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Isaksson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Isaksson et al 2023 Isaksson et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c621t-915a97f5c16d048cc46c5e2c19e98e0d2b0777f5c6a2f124dad91a64cb0cc86a3</cites><orcidid>0000-0002-6569-5793</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/PMC10156057/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10156057/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,550,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37083675$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-209284$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Isaksson, Hanna</creatorcontrib><creatorcontrib>Brännström, Åke</creatorcontrib><creatorcontrib>Libby, Eric</creatorcontrib><title>Minor variations in multicellular life cycles have major effects on adaptation</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>Multicellularity has evolved several independent times over the past hundreds of millions of years and given rise to a wide diversity of complex life. Recent studies have found that large differences in the fundamental structure of early multicellular life cycles can affect fitness and influence multicellular adaptation. Yet, there is an underlying assumption that at some scale or categorization multicellular life cycles are similar in terms of their adaptive potential. Here, we consider this possibility by exploring adaptation in a class of simple multicellular life cycles of filamentous organisms that only differ in one respect, how many daughter filaments are produced. We use mathematical models and evolutionary simulations to show that despite the similarities, qualitatively different mutations fix. In particular, we find that mutations with a tradeoff between cell growth and group survival, i.e. "selfish" or "altruistic" traits, spread differently. Specifically, altruistic mutations more readily spread in life cycles that produce few daughters while in life cycles producing many daughters either type of mutation can spread depending on the environment. Our results show that subtle changes in multicellular life cycles can fundamentally alter adaptation.</description><subject>Acclimatization</subject><subject>Adaptation</subject><subject>Adaptation (Biology)</subject><subject>Altruism</subject><subject>Analysis</subject><subject>Animals</subject><subject>Biological Evolution</subject><subject>Biology and Life Sciences</subject><subject>Cell survival</subject><subject>Cooperation</subject><subject>Daughters</subject><subject>Evolution</subject><subject>Filaments</subject><subject>Life Cycle Stages</subject><subject>Life cycles</subject><subject>Life cycles (Biology)</subject><subject>Mathematical models</subject><subject>Models, Theoretical</subject><subject>Mutation</subject><subject>Mutation (Biology)</subject><subject>Phenotype</subject><subject>Physical Sciences</subject><subject>Research and Analysis Methods</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>D8T</sourceid><sourceid>DOA</sourceid><recordid>eNqVksuO0zAUhiMEYobCGyCIxAYWLXbiS7xCo-FWaRgkblvrxDnpuHLiYieFeXuctjOaIjbIC1v29_8-tyx7SsmClpK-Xvsx9OAWG1PbBSWUCFXdy04p5-Vclry6f-d8kj2KcU1IOirxMDspJalKIflpdvnJ9j7kWwgWBuv7mNs-70Y3WIPOjQ5C7myLubk2DmN-BVvMO1gnCbYtmiHmvs-hgc2wkz_OHrTgIj457LPs-_t3384_zi8-f1ien13MjSjoMFeUg5ItN1Q0hFXGMGE4FoYqVBWSpqiJlNO7gKKlBWugURQEMzUxphJQzrLne9-N81EfShF1UVHGWCmVSMRyTzQe1noTbAfhWnuwenfhw0pDSFk61CW2hrJkLZAxWoq6BYM8BYSgeGNo8prvveIv3Iz1kdtb--Ns5zZ2oy6IKiqW-DeH6Ma6w8ZgPwRwR7Ljl95e6ZXf6tRGLgiXyeHlwSH4nyPGQXc2Th2BHv04JUo4KSlPLZ1lL_5C_12OxZ5aQcrY9q1PH5u0Guys8T22Nt2fSVbJolJkErw6EiRmwN_DCsYY9fLrl_9gL49ZtmdN8DEGbG_LQomeBvsmfD0Ntj4MdpI9u1vSW9HNJJd_AOr-9fs</recordid><startdate>20230401</startdate><enddate>20230401</enddate><creator>Isaksson, Hanna</creator><creator>Brännström, Åke</creator><creator>Libby, Eric</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QO</scope><scope>7QP</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AL</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>JQ2</scope><scope>K7-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0N</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>ADHXS</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>D93</scope><scope>ZZAVC</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-6569-5793</orcidid></search><sort><creationdate>20230401</creationdate><title>Minor variations in multicellular life cycles have major effects on adaptation</title><author>Isaksson, Hanna ; Brännström, Åke ; Libby, Eric</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c621t-915a97f5c16d048cc46c5e2c19e98e0d2b0777f5c6a2f124dad91a64cb0cc86a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Acclimatization</topic><topic>Adaptation</topic><topic>Adaptation (Biology)</topic><topic>Altruism</topic><topic>Analysis</topic><topic>Animals</topic><topic>Biological Evolution</topic><topic>Biology and Life Sciences</topic><topic>Cell survival</topic><topic>Cooperation</topic><topic>Daughters</topic><topic>Evolution</topic><topic>Filaments</topic><topic>Life Cycle Stages</topic><topic>Life cycles</topic><topic>Life cycles (Biology)</topic><topic>Mathematical models</topic><topic>Models, Theoretical</topic><topic>Mutation</topic><topic>Mutation (Biology)</topic><topic>Phenotype</topic><topic>Physical Sciences</topic><topic>Research and Analysis Methods</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Isaksson, Hanna</creatorcontrib><creatorcontrib>Brännström, Åke</creatorcontrib><creatorcontrib>Libby, Eric</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Computing Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Computer Science Collection</collection><collection>Computer Science Database</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Computing Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</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>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SWEPUB Umeå universitet full text</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SWEPUB Umeå universitet</collection><collection>SwePub Articles full text</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Isaksson, Hanna</au><au>Brännström, Åke</au><au>Libby, Eric</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Minor variations in multicellular life cycles have major effects on adaptation</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2023-04-01</date><risdate>2023</risdate><volume>19</volume><issue>4</issue><spage>e1010698</spage><epage>e1010698</epage><pages>e1010698-e1010698</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>Multicellularity has evolved several independent times over the past hundreds of millions of years and given rise to a wide diversity of complex life. Recent studies have found that large differences in the fundamental structure of early multicellular life cycles can affect fitness and influence multicellular adaptation. Yet, there is an underlying assumption that at some scale or categorization multicellular life cycles are similar in terms of their adaptive potential. Here, we consider this possibility by exploring adaptation in a class of simple multicellular life cycles of filamentous organisms that only differ in one respect, how many daughter filaments are produced. We use mathematical models and evolutionary simulations to show that despite the similarities, qualitatively different mutations fix. In particular, we find that mutations with a tradeoff between cell growth and group survival, i.e. "selfish" or "altruistic" traits, spread differently. Specifically, altruistic mutations more readily spread in life cycles that produce few daughters while in life cycles producing many daughters either type of mutation can spread depending on the environment. Our results show that subtle changes in multicellular life cycles can fundamentally alter adaptation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37083675</pmid><doi>10.1371/journal.pcbi.1010698</doi><tpages>e1010698</tpages><orcidid>https://orcid.org/0000-0002-6569-5793</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1553-7358
ispartof PLoS computational biology, 2023-04, Vol.19 (4), p.e1010698-e1010698
issn 1553-7358
1553-734X
1553-7358
language eng
recordid cdi_plos_journals_2814443796
source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; SWEPUB Freely available online; Public Library of Science (PLoS)
subjects Acclimatization
Adaptation
Adaptation (Biology)
Altruism
Analysis
Animals
Biological Evolution
Biology and Life Sciences
Cell survival
Cooperation
Daughters
Evolution
Filaments
Life Cycle Stages
Life cycles
Life cycles (Biology)
Mathematical models
Models, Theoretical
Mutation
Mutation (Biology)
Phenotype
Physical Sciences
Research and Analysis Methods
title Minor variations in multicellular life cycles have major effects on adaptation
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T21%3A15%3A34IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Minor%20variations%20in%20multicellular%20life%20cycles%20have%20major%20effects%20on%20adaptation&rft.jtitle=PLoS%20computational%20biology&rft.au=Isaksson,%20Hanna&rft.date=2023-04-01&rft.volume=19&rft.issue=4&rft.spage=e1010698&rft.epage=e1010698&rft.pages=e1010698-e1010698&rft.issn=1553-7358&rft.eissn=1553-7358&rft_id=info:doi/10.1371/journal.pcbi.1010698&rft_dat=%3Cgale_plos_%3EA748728906%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2814443796&rft_id=info:pmid/37083675&rft_galeid=A748728906&rft_doaj_id=oai_doaj_org_article_3efc14b0c6e44136bface5c5eea95dc1&rfr_iscdi=true