Context-dependent genetic architecture of Drosophila life span
Understanding the genetic basis of variation in life span is a major challenge that is difficult to address in human populations. Evolutionary theory predicts that alleles affecting natural variation in life span will have properties that enable them to persist in populations at intermediate frequen...
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| creator | Huang, Wen Campbell, Terry Carbone, Mary Anna Jones, W Elizabeth Unselt, Desiree Anholt, Robert R H Mackay, Trudy F C |
| description | Understanding the genetic basis of variation in life span is a major challenge that is difficult to address in human populations. Evolutionary theory predicts that alleles affecting natural variation in life span will have properties that enable them to persist in populations at intermediate frequencies, such as late-life-specific deleterious effects, antagonistic pleiotropic effects on early and late-age fitness components, and/or sex- and environment-specific or antagonistic effects. Here, we quantified variation in life span in males and females reared in 3 thermal environments for the sequenced, inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and an advanced intercross outbred population derived from a subset of DGRP lines. Quantitative genetic analyses of life span and the micro-environmental variance of life span in the DGRP revealed significant genetic variance for both traits within each sex and environment, as well as significant genotype-by-sex interaction (GSI) and genotype-by-environment interaction (GEI). Genome-wide association (GWA) mapping in both populations implicates over 2,000 candidate genes with sex- and environment-specific or antagonistic pleiotropic allelic effects. Over 1,000 of these genes are associated with variation in life span in other D. melanogaster populations. We functionally assessed the effects of 15 candidate genes using RNA interference (RNAi): all affected life span and/or micro-environmental variance of life span in at least one sex and environment and exhibited sex-and environment-specific effects. Our results implicate novel candidate genes affecting life span and suggest that variation for life span may be maintained by variable allelic effects in heterogeneous environments. |
| doi_str_mv | 10.1371/journal.pbio.3000645 |
| format | Article |
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Evolutionary theory predicts that alleles affecting natural variation in life span will have properties that enable them to persist in populations at intermediate frequencies, such as late-life-specific deleterious effects, antagonistic pleiotropic effects on early and late-age fitness components, and/or sex- and environment-specific or antagonistic effects. Here, we quantified variation in life span in males and females reared in 3 thermal environments for the sequenced, inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and an advanced intercross outbred population derived from a subset of DGRP lines. Quantitative genetic analyses of life span and the micro-environmental variance of life span in the DGRP revealed significant genetic variance for both traits within each sex and environment, as well as significant genotype-by-sex interaction (GSI) and genotype-by-environment interaction (GEI). Genome-wide association (GWA) mapping in both populations implicates over 2,000 candidate genes with sex- and environment-specific or antagonistic pleiotropic allelic effects. Over 1,000 of these genes are associated with variation in life span in other D. melanogaster populations. We functionally assessed the effects of 15 candidate genes using RNA interference (RNAi): all affected life span and/or micro-environmental variance of life span in at least one sex and environment and exhibited sex-and environment-specific effects. Our results implicate novel candidate genes affecting life span and suggest that variation for life span may be maintained by variable allelic effects in heterogeneous environments.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3000645</identifier><identifier>PMID: 32134916</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Age ; Analysis ; Animals ; Biochemistry ; Biology ; Biology and Life Sciences ; Drosophila ; Drosophila melanogaster - genetics ; Drosophila melanogaster - physiology ; Drosophila Proteins - genetics ; Environmental effects ; Evolution ; Female ; Gene expression ; Gene mapping ; Gene-Environment Interaction ; Genes ; Genetic analysis ; Genetic aspects ; Genetic diversity ; Genetic research ; Genetic variance ; Genetic Variation ; Genome-Wide Association Study ; Genomes ; Genomics ; Genotype & phenotype ; Genotype-environment interactions ; Genotypes ; Human populations ; Inbreeding ; Life span ; Longevity - genetics ; Male ; Mapping ; Mutation ; Population genetics ; Populations ; Quantitative genetics ; Research and Analysis Methods ; RNA Interference ; RNA-mediated interference ; Sex ; Sexes ; Temperature ; Thermal environments ; Variance ; Variation</subject><ispartof>PLoS biology, 2020-03, Vol.18 (3), p.e3000645-e3000645</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Huang 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>2020 Huang et al 2020 Huang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c746t-ad846b6e83388079c7dd40a3aa47a6545d576f6107602e1d4faad1d5553cacad3</citedby><cites>FETCH-LOGICAL-c746t-ad846b6e83388079c7dd40a3aa47a6545d576f6107602e1d4faad1d5553cacad3</cites><orcidid>0000-0002-2312-7245 ; 0000-0003-2134-0787 ; 0000-0003-1489-8854</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/PMC7077879/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7077879/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32134916$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Barton, Nick H.</contributor><creatorcontrib>Huang, Wen</creatorcontrib><creatorcontrib>Campbell, Terry</creatorcontrib><creatorcontrib>Carbone, Mary Anna</creatorcontrib><creatorcontrib>Jones, W Elizabeth</creatorcontrib><creatorcontrib>Unselt, Desiree</creatorcontrib><creatorcontrib>Anholt, Robert R H</creatorcontrib><creatorcontrib>Mackay, Trudy F C</creatorcontrib><title>Context-dependent genetic architecture of Drosophila life span</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Understanding the genetic basis of variation in life span is a major challenge that is difficult to address in human populations. Evolutionary theory predicts that alleles affecting natural variation in life span will have properties that enable them to persist in populations at intermediate frequencies, such as late-life-specific deleterious effects, antagonistic pleiotropic effects on early and late-age fitness components, and/or sex- and environment-specific or antagonistic effects. Here, we quantified variation in life span in males and females reared in 3 thermal environments for the sequenced, inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and an advanced intercross outbred population derived from a subset of DGRP lines. Quantitative genetic analyses of life span and the micro-environmental variance of life span in the DGRP revealed significant genetic variance for both traits within each sex and environment, as well as significant genotype-by-sex interaction (GSI) and genotype-by-environment interaction (GEI). Genome-wide association (GWA) mapping in both populations implicates over 2,000 candidate genes with sex- and environment-specific or antagonistic pleiotropic allelic effects. Over 1,000 of these genes are associated with variation in life span in other D. melanogaster populations. We functionally assessed the effects of 15 candidate genes using RNA interference (RNAi): all affected life span and/or micro-environmental variance of life span in at least one sex and environment and exhibited sex-and environment-specific effects. Our results implicate novel candidate genes affecting life span and suggest that variation for life span may be maintained by variable allelic effects in heterogeneous environments.</description><subject>Age</subject><subject>Analysis</subject><subject>Animals</subject><subject>Biochemistry</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - physiology</subject><subject>Drosophila Proteins - genetics</subject><subject>Environmental effects</subject><subject>Evolution</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Gene-Environment Interaction</subject><subject>Genes</subject><subject>Genetic analysis</subject><subject>Genetic aspects</subject><subject>Genetic diversity</subject><subject>Genetic research</subject><subject>Genetic variance</subject><subject>Genetic Variation</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotype & phenotype</subject><subject>Genotype-environment interactions</subject><subject>Genotypes</subject><subject>Human populations</subject><subject>Inbreeding</subject><subject>Life span</subject><subject>Longevity - genetics</subject><subject>Male</subject><subject>Mapping</subject><subject>Mutation</subject><subject>Population genetics</subject><subject>Populations</subject><subject>Quantitative genetics</subject><subject>Research and Analysis Methods</subject><subject>RNA Interference</subject><subject>RNA-mediated interference</subject><subject>Sex</subject><subject>Sexes</subject><subject>Temperature</subject><subject>Thermal environments</subject><subject>Variance</subject><subject>Variation</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVkstu1DAUhiMEoqXwBggisYFFBju-ZlOpGm4jVVTitrVObGfGo0wc7ATB2-MwadWgLmBly_7Of25_lj3FaIWJwK_3fgwdtKu-dn5FEEKcsnvZKWaUFUJKdv_W_SR7FOMeobKsSvkwOyElJrTC_DQ7X_tusD-HwtjedsZ2Q761nR2cziHonRusHsZgc9_kb4KPvt-5FvLWNTaPPXSPswcNtNE-mc-z7Ou7t1_WH4rLq_eb9cVloQXlQwFGUl5zKwmREolKC2MoAgJABfBUpWGCNxwjwVFpsaENgMGGMUY0aDDkLHt-1O1bH9XcelQlqZDAshQsEZsjYTzsVR_cAcIv5cGpPw8-bBWE1FZrVV2SmkMDgglJSwsVkpJjYYTRiEo9aZ3P2cb6YI1OUwnQLkSXP53bqa3_oQQSQooqCbycBYL_Pto4qIOL2rYtdNaPU92CEiYRlwl98Rd6d3cztYXUgOsan_LqSVRdcFxhkpY_Uas7qGmA9uC072zj0vsi4NUiQB_NsIUxRrX5_Ok_2I__zl59W7L0yOrkrxhsczNnjNTk9OuBqMnpanZ6Cnt2e0c3QdfWJr8B8VL3fA</recordid><startdate>20200305</startdate><enddate>20200305</enddate><creator>Huang, Wen</creator><creator>Campbell, Terry</creator><creator>Carbone, Mary Anna</creator><creator>Jones, W Elizabeth</creator><creator>Unselt, Desiree</creator><creator>Anholt, Robert R H</creator><creator>Mackay, Trudy F C</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope><orcidid>https://orcid.org/0000-0002-2312-7245</orcidid><orcidid>https://orcid.org/0000-0003-2134-0787</orcidid><orcidid>https://orcid.org/0000-0003-1489-8854</orcidid></search><sort><creationdate>20200305</creationdate><title>Context-dependent genetic architecture of Drosophila life span</title><author>Huang, Wen ; Campbell, Terry ; Carbone, Mary Anna ; Jones, W Elizabeth ; Unselt, Desiree ; Anholt, Robert R H ; Mackay, Trudy F C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c746t-ad846b6e83388079c7dd40a3aa47a6545d576f6107602e1d4faad1d5553cacad3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Age</topic><topic>Analysis</topic><topic>Animals</topic><topic>Biochemistry</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Huang, Wen</au><au>Campbell, Terry</au><au>Carbone, Mary Anna</au><au>Jones, W Elizabeth</au><au>Unselt, Desiree</au><au>Anholt, Robert R H</au><au>Mackay, Trudy F C</au><au>Barton, Nick H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Context-dependent genetic architecture of Drosophila life span</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2020-03-05</date><risdate>2020</risdate><volume>18</volume><issue>3</issue><spage>e3000645</spage><epage>e3000645</epage><pages>e3000645-e3000645</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Understanding the genetic basis of variation in life span is a major challenge that is difficult to address in human populations. Evolutionary theory predicts that alleles affecting natural variation in life span will have properties that enable them to persist in populations at intermediate frequencies, such as late-life-specific deleterious effects, antagonistic pleiotropic effects on early and late-age fitness components, and/or sex- and environment-specific or antagonistic effects. Here, we quantified variation in life span in males and females reared in 3 thermal environments for the sequenced, inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and an advanced intercross outbred population derived from a subset of DGRP lines. Quantitative genetic analyses of life span and the micro-environmental variance of life span in the DGRP revealed significant genetic variance for both traits within each sex and environment, as well as significant genotype-by-sex interaction (GSI) and genotype-by-environment interaction (GEI). Genome-wide association (GWA) mapping in both populations implicates over 2,000 candidate genes with sex- and environment-specific or antagonistic pleiotropic allelic effects. Over 1,000 of these genes are associated with variation in life span in other D. melanogaster populations. We functionally assessed the effects of 15 candidate genes using RNA interference (RNAi): all affected life span and/or micro-environmental variance of life span in at least one sex and environment and exhibited sex-and environment-specific effects. Our results implicate novel candidate genes affecting life span and suggest that variation for life span may be maintained by variable allelic effects in heterogeneous environments.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32134916</pmid><doi>10.1371/journal.pbio.3000645</doi><orcidid>https://orcid.org/0000-0002-2312-7245</orcidid><orcidid>https://orcid.org/0000-0003-2134-0787</orcidid><orcidid>https://orcid.org/0000-0003-1489-8854</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Age Analysis Animals Biochemistry Biology Biology and Life Sciences Drosophila Drosophila melanogaster - genetics Drosophila melanogaster - physiology Drosophila Proteins - genetics Environmental effects Evolution Female Gene expression Gene mapping Gene-Environment Interaction Genes Genetic analysis Genetic aspects Genetic diversity Genetic research Genetic variance Genetic Variation Genome-Wide Association Study Genomes Genomics Genotype & phenotype Genotype-environment interactions Genotypes Human populations Inbreeding Life span Longevity - genetics Male Mapping Mutation Population genetics Populations Quantitative genetics Research and Analysis Methods RNA Interference RNA-mediated interference Sex Sexes Temperature Thermal environments Variance Variation |
| title | Context-dependent genetic architecture of Drosophila life span |
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