Complex adaptations can drive the evolution of the capacitor [PSI], even with realistic rates of yeast sex

The [PSI(+)] prion may enhance evolvability by revealing previously cryptic genetic variation, but it is unclear whether such evolvability properties could be favored by natural selection. Sex inhibits the evolution of other putative evolvability mechanisms, such as mutator alleles. This paper explo...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:PLoS genetics 2009-06, Vol.5 (6), p.e1000517-e1000517
Hauptverfasser: Griswold, Cortland K, Masel, Joanna
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page e1000517
container_issue 6
container_start_page e1000517
container_title PLoS genetics
container_volume 5
creator Griswold, Cortland K
Masel, Joanna
description The [PSI(+)] prion may enhance evolvability by revealing previously cryptic genetic variation, but it is unclear whether such evolvability properties could be favored by natural selection. Sex inhibits the evolution of other putative evolvability mechanisms, such as mutator alleles. This paper explores whether sex also prevents natural selection from favoring modifier alleles that facilitate [PSI(+)] formation. Sex may permit the spread of "cheater" alleles that acquire the benefits of [PSI(+)] through mating without incurring the cost of producing [PSI(+)] at times when it is not adaptive. Using recent quantitative estimates of the frequency of sex in Saccharomyces paradoxus, we calculate that natural selection for evolvability can drive the evolution of the [PSI(+)] system, so long as yeast populations occasionally require complex adaptations involving synergistic epistasis between two loci. If adaptations are always simple and require substitution at only a single locus, then the [PSI(+)] system is not favored by natural selection. Obligate sex might inhibit the evolution of [PSI(+)]-like systems in other species.
doi_str_mv 10.1371/journal.pgen.1000517
format Article
fullrecord <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_1313501065</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A203232058</galeid><doaj_id>oai_doaj_org_article_f7e26a1ec39a4e3f8b9500d049b31c62</doaj_id><sourcerecordid>A203232058</sourcerecordid><originalsourceid>FETCH-LOGICAL-c696t-a01a4042d1a93686493f0c6cea1bf3498f93b47b123824b8f26e9c84a1c84c0a3</originalsourceid><addsrcrecordid>eNqVk12L1DAUhoso7rr6D0QLwoLgjEnTps2NsAx-DCyuuOqNSDhNT2cytE1N0nH235vZqToFL5RAEk6e983Jx4mix5TMKcvpy40ZbAfNvF9hN6eEkIzmd6JTmmVslqckvXs0P4keOLchhGWFyO9HJ1RkCU2FOI02C9P2De5iqKD34LXpXKygiyurtxj7Nca4Nc2wX4hNfRtQ0IPS3tj464fr5bcXgcAu_qH9OrYIjXZeq9iCR7dX3CA4HzvcPYzu1dA4fDSOZ9HnN68_Ld7NLq_eLhcXlzPFBfczIBRCyklFQTBe8FSwmiiuEGhZs1QUtWBlmpc0YUWSlkWdcBSqSIGGThFgZ9HTg2_fGCfHa3KSMsoyQgnPArE8EJWBjeytbsHeSANa3gaMXUmw4RANyjrHhANFxQSkyOqiFBkhFUlFyajiSfB6Ne42lC1WCjtvoZmYTlc6vZYrs5VJOBvlLBicjwbWfB_Qedlqp7BpoEMzOMlzFlLmIoDPDuAKQmK6q03wU3tYXiSEJSwhWRGo-V-o0CpstTId1jrEJ4LnE0FgPO78Cgbn5PL643-w7_-dvfoyZc-P2HX4RH7txl_npmB6AJU1zlmsf180JXJfFr_eW-7LQo5lEWRPjh_pj2isA_YTqKEG8g</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>67365369</pqid></control><display><type>article</type><title>Complex adaptations can drive the evolution of the capacitor [PSI], even with realistic rates of yeast sex</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Public Library of Science (PLoS) Journals Open Access</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Griswold, Cortland K ; Masel, Joanna</creator><contributor>Úbeda, Francisco</contributor><creatorcontrib>Griswold, Cortland K ; Masel, Joanna ; Úbeda, Francisco</creatorcontrib><description>The [PSI(+)] prion may enhance evolvability by revealing previously cryptic genetic variation, but it is unclear whether such evolvability properties could be favored by natural selection. Sex inhibits the evolution of other putative evolvability mechanisms, such as mutator alleles. This paper explores whether sex also prevents natural selection from favoring modifier alleles that facilitate [PSI(+)] formation. Sex may permit the spread of "cheater" alleles that acquire the benefits of [PSI(+)] through mating without incurring the cost of producing [PSI(+)] at times when it is not adaptive. Using recent quantitative estimates of the frequency of sex in Saccharomyces paradoxus, we calculate that natural selection for evolvability can drive the evolution of the [PSI(+)] system, so long as yeast populations occasionally require complex adaptations involving synergistic epistasis between two loci. If adaptations are always simple and require substitution at only a single locus, then the [PSI(+)] system is not favored by natural selection. Obligate sex might inhibit the evolution of [PSI(+)]-like systems in other species.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1000517</identifier><identifier>PMID: 19521499</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptation ; Adaptation, Biological ; Computational Biology/Evolutionary Modeling ; Evolution, Molecular ; Evolutionary Biology/Microbial Evolution and Genomics ; Genes ; Genetic aspects ; Genetic variation ; Models, Genetic ; Mutation ; Natural selection ; Peptide Termination Factors - genetics ; Peptide Termination Factors - metabolism ; Physiological aspects ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae - physiology ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Selection, Genetic ; Yeast ; Yeast fungi</subject><ispartof>PLoS genetics, 2009-06, Vol.5 (6), p.e1000517-e1000517</ispartof><rights>COPYRIGHT 2009 Public Library of Science</rights><rights>Griswold, Masel. 2009</rights><rights>2009 Griswold, Masel. 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: Griswold CK, Masel J (2009) Complex Adaptations Can Drive the Evolution of the Capacitor [PSI+], Even with Realistic Rates of Yeast Sex. PLoS Genet 5(6): e1000517. doi:10.1371/journal.pgen.1000517</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c696t-a01a4042d1a93686493f0c6cea1bf3498f93b47b123824b8f26e9c84a1c84c0a3</citedby><cites>FETCH-LOGICAL-c696t-a01a4042d1a93686493f0c6cea1bf3498f93b47b123824b8f26e9c84a1c84c0a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2686163/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2686163/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19521499$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Úbeda, Francisco</contributor><creatorcontrib>Griswold, Cortland K</creatorcontrib><creatorcontrib>Masel, Joanna</creatorcontrib><title>Complex adaptations can drive the evolution of the capacitor [PSI], even with realistic rates of yeast sex</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The [PSI(+)] prion may enhance evolvability by revealing previously cryptic genetic variation, but it is unclear whether such evolvability properties could be favored by natural selection. Sex inhibits the evolution of other putative evolvability mechanisms, such as mutator alleles. This paper explores whether sex also prevents natural selection from favoring modifier alleles that facilitate [PSI(+)] formation. Sex may permit the spread of "cheater" alleles that acquire the benefits of [PSI(+)] through mating without incurring the cost of producing [PSI(+)] at times when it is not adaptive. Using recent quantitative estimates of the frequency of sex in Saccharomyces paradoxus, we calculate that natural selection for evolvability can drive the evolution of the [PSI(+)] system, so long as yeast populations occasionally require complex adaptations involving synergistic epistasis between two loci. If adaptations are always simple and require substitution at only a single locus, then the [PSI(+)] system is not favored by natural selection. Obligate sex might inhibit the evolution of [PSI(+)]-like systems in other species.</description><subject>Adaptation</subject><subject>Adaptation, Biological</subject><subject>Computational Biology/Evolutionary Modeling</subject><subject>Evolution, Molecular</subject><subject>Evolutionary Biology/Microbial Evolution and Genomics</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic variation</subject><subject>Models, Genetic</subject><subject>Mutation</subject><subject>Natural selection</subject><subject>Peptide Termination Factors - genetics</subject><subject>Peptide Termination Factors - metabolism</subject><subject>Physiological aspects</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae - physiology</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Selection, Genetic</subject><subject>Yeast</subject><subject>Yeast fungi</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk12L1DAUhoso7rr6D0QLwoLgjEnTps2NsAx-DCyuuOqNSDhNT2cytE1N0nH235vZqToFL5RAEk6e983Jx4mix5TMKcvpy40ZbAfNvF9hN6eEkIzmd6JTmmVslqckvXs0P4keOLchhGWFyO9HJ1RkCU2FOI02C9P2De5iqKD34LXpXKygiyurtxj7Nca4Nc2wX4hNfRtQ0IPS3tj464fr5bcXgcAu_qH9OrYIjXZeq9iCR7dX3CA4HzvcPYzu1dA4fDSOZ9HnN68_Ld7NLq_eLhcXlzPFBfczIBRCyklFQTBe8FSwmiiuEGhZs1QUtWBlmpc0YUWSlkWdcBSqSIGGThFgZ9HTg2_fGCfHa3KSMsoyQgnPArE8EJWBjeytbsHeSANa3gaMXUmw4RANyjrHhANFxQSkyOqiFBkhFUlFyajiSfB6Ne42lC1WCjtvoZmYTlc6vZYrs5VJOBvlLBicjwbWfB_Qedlqp7BpoEMzOMlzFlLmIoDPDuAKQmK6q03wU3tYXiSEJSwhWRGo-V-o0CpstTId1jrEJ4LnE0FgPO78Cgbn5PL643-w7_-dvfoyZc-P2HX4RH7txl_npmB6AJU1zlmsf180JXJfFr_eW-7LQo5lEWRPjh_pj2isA_YTqKEG8g</recordid><startdate>20090601</startdate><enddate>20090601</enddate><creator>Griswold, Cortland K</creator><creator>Masel, Joanna</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20090601</creationdate><title>Complex adaptations can drive the evolution of the capacitor [PSI], even with realistic rates of yeast sex</title><author>Griswold, Cortland K ; Masel, Joanna</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c696t-a01a4042d1a93686493f0c6cea1bf3498f93b47b123824b8f26e9c84a1c84c0a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Adaptation</topic><topic>Adaptation, Biological</topic><topic>Computational Biology/Evolutionary Modeling</topic><topic>Evolution, Molecular</topic><topic>Evolutionary Biology/Microbial Evolution and Genomics</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic variation</topic><topic>Models, Genetic</topic><topic>Mutation</topic><topic>Natural selection</topic><topic>Peptide Termination Factors - genetics</topic><topic>Peptide Termination Factors - metabolism</topic><topic>Physiological aspects</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Saccharomyces cerevisiae - physiology</topic><topic>Saccharomyces cerevisiae Proteins - genetics</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Selection, Genetic</topic><topic>Yeast</topic><topic>Yeast fungi</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Griswold, Cortland K</creatorcontrib><creatorcontrib>Masel, Joanna</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: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Griswold, Cortland K</au><au>Masel, Joanna</au><au>Úbeda, Francisco</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Complex adaptations can drive the evolution of the capacitor [PSI], even with realistic rates of yeast sex</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2009-06-01</date><risdate>2009</risdate><volume>5</volume><issue>6</issue><spage>e1000517</spage><epage>e1000517</epage><pages>e1000517-e1000517</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The [PSI(+)] prion may enhance evolvability by revealing previously cryptic genetic variation, but it is unclear whether such evolvability properties could be favored by natural selection. Sex inhibits the evolution of other putative evolvability mechanisms, such as mutator alleles. This paper explores whether sex also prevents natural selection from favoring modifier alleles that facilitate [PSI(+)] formation. Sex may permit the spread of "cheater" alleles that acquire the benefits of [PSI(+)] through mating without incurring the cost of producing [PSI(+)] at times when it is not adaptive. Using recent quantitative estimates of the frequency of sex in Saccharomyces paradoxus, we calculate that natural selection for evolvability can drive the evolution of the [PSI(+)] system, so long as yeast populations occasionally require complex adaptations involving synergistic epistasis between two loci. If adaptations are always simple and require substitution at only a single locus, then the [PSI(+)] system is not favored by natural selection. Obligate sex might inhibit the evolution of [PSI(+)]-like systems in other species.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>19521499</pmid><doi>10.1371/journal.pgen.1000517</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1553-7404
ispartof PLoS genetics, 2009-06, Vol.5 (6), p.e1000517-e1000517
issn 1553-7404
1553-7390
1553-7404
language eng
recordid cdi_plos_journals_1313501065
source MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central
subjects Adaptation
Adaptation, Biological
Computational Biology/Evolutionary Modeling
Evolution, Molecular
Evolutionary Biology/Microbial Evolution and Genomics
Genes
Genetic aspects
Genetic variation
Models, Genetic
Mutation
Natural selection
Peptide Termination Factors - genetics
Peptide Termination Factors - metabolism
Physiological aspects
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae - physiology
Saccharomyces cerevisiae Proteins - genetics
Saccharomyces cerevisiae Proteins - metabolism
Selection, Genetic
Yeast
Yeast fungi
title Complex adaptations can drive the evolution of the capacitor [PSI], even with realistic rates of yeast sex
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-17T13%3A20%3A11IST&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=Complex%20adaptations%20can%20drive%20the%20evolution%20of%20the%20capacitor%20%5BPSI%5D,%20even%20with%20realistic%20rates%20of%20yeast%20sex&rft.jtitle=PLoS%20genetics&rft.au=Griswold,%20Cortland%20K&rft.date=2009-06-01&rft.volume=5&rft.issue=6&rft.spage=e1000517&rft.epage=e1000517&rft.pages=e1000517-e1000517&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1000517&rft_dat=%3Cgale_plos_%3EA203232058%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=67365369&rft_id=info:pmid/19521499&rft_galeid=A203232058&rft_doaj_id=oai_doaj_org_article_f7e26a1ec39a4e3f8b9500d049b31c62&rfr_iscdi=true