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{"title"=>"Functional significance of allelic variation at methuselah, an aging gene in Drosophila", "type"=>"journal", "authors"=>[{"first_name"=>"Annalise B.", "last_name"=>"Paaby", "scopus_author_id"=>"8980624600"}, {"first_name"=>"Paul S.", "last_name"=>"Schmidt", "scopus_author_id"=>"7403630402"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"18414670", "sgr"=>"44849103119", "doi"=>"10.1371/journal.pone.0001987", "scopus"=>"2-s2.0-44849103119", "pui"=>"352003400", "isbn"=>"1932-6203", "issn"=>"19326203"}, "id"=>"a90fb49d-4318-3fc4-9112-e15b90564811", "abstract"=>"BACKGROUND: Longevity and age-specific patterns of mortality are complex traits that vary within and among taxa. Multiple candidate genes for aging have been identified in model systems by extended longevity mutant phenotypes, including the G-protein coupled receptor methuselah (mth) in D. melanogaster. These genes offer important insights into the mechanisms of lifespan determination and have been major targets of interest in the biology of aging. However, it is largely unknown whether these genes contribute to genetic variance for lifespan in natural populations, and consequently contribute to lifespan evolution. METHODOLOGY/PRINCIPLE FINDINGS: For a gene to contribute to genetic variance for a particular trait, it must meet two criteria: natural allelic variation and functional differences among variants. Previous work showed that mth varies significantly among wild populations; here we assess the functional significance of wild-derived mth alleles on lifespan, fecundity and stress resistance using a quantitative complementation scheme. Our results demonstrate that mth alleles segregating in nature have a functional effect on all three traits. CONCLUSIONS/SIGNIFICANCE: These results suggest that allelic variation at mth contributes to observed differences in lifespan and correlated phenotypes in natural populations, and that evaluation of genetic diversity at candidate genes for aging can be a fruitful approach to identifying loci contributing to lifespan evolution.", "link"=>"http://www.mendeley.com/research/functional-significance-allelic-variation-methuselah-aging-gene-drosophila", "reader_count"=>42, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>12, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>12, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>36, "Medicine and Dentistry"=>2, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>36}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Romania"=>1, "United States"=>4, "United Kingdom"=>2, "South Africa"=>1, "Switzerland"=>2, "India"=>1, "Spain"=>1}, "group_count"=>1}

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• http://doi.org/10.1534/g3.114.010629
• http://doi.org/10.1111/jeb.13310
• http://doi.org/10.1111/j.1365-294X.2009.04508.x
• http://doi.org/10.1371/journal.pone.0011229
• http://doi.org/10.3390/genes7100091
• http://doi.org/10.1186/s12915-018-0562-z
• http://doi.org/10.1111/j.1474-9726.2008.00415.x
• http://doi.org/10.1098/rstb.2009.0265
• http://doi.org/10.1371/journal.pone.0057214
• http://doi.org/10.1007/s10068-017-0180-5
• http://doi.org/10.1016/j.exger.2016.06.006
• http://doi.org/10.1371/journal.pone.0160069
• http://doi.org/10.1111/jeb.12690
• http://doi.org/10.1016/j.exger.2009.09.004
• http://doi.org/10.1534/genetics.119.300160
• http://doi.org/10.1371/journal.pgen.1002631
• http://doi.org/10.1093/molbev/msv061
• http://doi.org/10.1111/mec.12353
• http://doi.org/10.1111/evo.12546
• http://doi.org/10.1007/s11357-013-9568-1
• http://doi.org/10.1016/j.exger.2015.06.021
• http://doi.org/10.1016/j.bbagen.2009.07.010
• http://doi.org/10.1038/ncomms5338
• http://doi.org/10.1002/evl3.143
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• http://doi.org/10.1007/s12041-017-0814-7
• http://doi.org/10.1038/s41598-018-34267-0
• http://doi.org/10.1111/j.1558-5646.2011.01486.x
• http://doi.org/10.1007/s10522-016-9653-9
• http://doi.org/10.1111/jeb.12847
• http://doi.org/10.1007/s00239-019-09923-2
• http://doi.org/10.1002/jez.b.22453
• http://doi.org/10.1534/g3.120.401041
• http://doi.org/10.1016/j.ibmb.2010.05.005

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• {"url"=>"http%3A%2F%2Fjournals.plos.org%2Fplosone%2Farticle%3Fid%3D10.1371%252Fjournal.pone.0001987", "share_count"=>0, "like_count"=>0, "comment_count"=>0, "click_count"=>0, "total_count"=>0}

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• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/7a5e6bc9-f443-45a1-b79e-9a5cd1abbbbd", "title"=>"Referee Comments: Referee 2", "body"=>"Referee 2's Review:\n\n**********\nN.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication the manuscript has been revised in light of these comments and to address other editorial requirements.\n**********\n\nThe manuscript describes functional characterization of natural Mth alleles using quantitative complementation tests. To my knowledge, this is the first evidence that one of the well-known candidate \"aging\" genes is functionally relevant to lifespan variation among natural populations. Therefore, the novelty and importance of the data is high.\n\nTechnically, the experiments appear to have been carefully conducted and the data analysis is generally appropriate. Quantitative complementation tests are sometimes controversial, but I think the authors have chosen the most appropriate method to measure life history effects of a moderate number of naturally occurring alleles. Precise allele replacement experiments might be the gold standard for such tests, but they are too laborious to extend to the number of different alleles (8) that are compared here. \n\nThe manuscript is well written and appropriately summarizes the background information.\n\nI have some suggestions to improve the clarity of the manuscript in places. Overall, however, I am quite enthusiastic about this study.\n\nGeneral Comment:\n\nI think it would be useful to have a table reporting the phenotype means for each genotype, perhaps as Supplementary Information.\n\nSpecific Comments:\n\np. 6. States that flies derived from natural populations were made isogenic for the 3rd chromosome. Were the remainder of the chromosomes (X, 2 and 4) co-isogenic across different lines? If so, this alleviates some of the concern about potential genetic background effects.\n\np.7 states that the 8 experimental lines were chosen on the basis of haplotype identity and nucleotide diversity at remaining sites. I would like to see more information here. What, exactly were these criteria (the 'nucleotide diversity' criterion is especially obscure)? Perhaps the authors could provide a table that summarizes the differences among genotypes.\n\np. 7 (bottom) Was CO2 anesthesia used in transfers?\n\np. 8. In the linear statistical model that is shown, which terms were fixed and which random? I'm guessing that all terms were fixed except for R(LxA), but this should be stated explicitly. Also it would improve clarity if it were stated here that \"Line\" refers to the lab strains (mutant versus wild type) and \"Allele\" refers to the wild strains.\n\np. 8 (bottom) I don't really trust JMP for analyses of mixed linear models (this applies to the fecundity analyses, not the lifespan analyses). I would prefer to see those tests implemented in SAS or some other software (like R) that appropriately handles mixed models. That said, the results appear to be so robust that I doubt that these analyses would change any of the main conclusions of the paper.\n", "isRemoved"=>false, "created"=>"2008-04-17T18:09:50Z", "lastModified"=>"2008-04-17T18:09:50Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001987", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-04-17T18:09:50Z", "replies"=>[]}
• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/60bf3569-db32-4ad6-a588-cf9c8fc5b648", "title"=>"Kim Hughes' evaluation of this article at the Faculty of 1000 Biology", "body"=>"Kim Hughes (University of Illinois at Urbana-Champaign, United States of America) has commented on this article at the Faculty of 1000 Biology. Her/his comments are as under:\r\n\r\n\"This paper describes the first evidence that one of the well-known candidate “aging” genes (methuselah) is functionally relevant to lifespan variation in nature. Quantitative complementation tests show that alleles derived from different natural populations differ in their effects on lifespan, oxidative stress resistance, and fecundity, and the natural alleles often have sex-specific effects. Consistent with other studies, lifespan and stress resistance effects are positively correlated. Somewhat surprisingly, mth mutants did not have generally elevated lifespan, although one of two mutants did show elevated oxidative stress resistance and elevated fecundity compared to a wild type allele\".\r\n\r\nReference:\r\n\r\n1) Kim Hughes: Faculty of 1000 Biology, 1 May 2008 http://www.f1000biology.com/article/id/1108073/evaluation\r\n\r\nTo refer to this and other PLoS ONE evaluations at F1000B follow this boolean search: \r\n\r\n[http://www.f1000biology.com/search/results.asp?txtSearch1=%22PLoS%22+%5BTA%5D+NOT+Biol+%5BTA%5D+NOT+Pathog+%5BTA%5D+NOT+Med+%5BTA%5D+NOT+Genet+%5BTA%5D+NOT+Biology+%5BTA%5D+NOT+Genetics+%5BTA%5D+NOT+Pathogens+%5BTA%5D&drpFromDate=0&drpToDate=0&drpAddedInLast=0&drpArticleType=&drpAbstract=no+abstract&drpPerPage=20&drpOrderBy=by+date&jou_id=9002&strSearchBoxType=f1000_boolean_results&strSavedArxIDs=&strPeerReview=&drpClassification=&drpPicked=1&drpListBy=newest&drpF1000Rated=1&chkChangesPractice=&Search.x=10]\r\n\r\nBest,\r\n\r\nNiyaz Ahmed\r\nSection Editor, PLoS ONE\r\nFaculty Member, F1000Biology and F1000Medicine\r\n__________\r\n\r\nPS: F1000 Biology (Medicine Reports Ltd.) has the rights for not making available this evaluation publicly but to the registered subscribers of the service. Kindly refer to the web service (www.f1000biology.com) to see full evaluations with rating, F1000 Factors and the threads representing repeated evaluations / refutations etc. The material posted above is carried for general information and with the intent of fair use.\r\n\r\n\r\n\r\n", "isRemoved"=>false, "created"=>"2008-06-29T08:50:49Z", "lastModified"=>"2008-06-29T08:50:49Z", "creator"=>{"userId"=>"60235"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0001987", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-06-29T08:50:49Z", "replies"=>[]}

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/933629"], "description"=>"<p>The comparisons using <i>mth^Δ6</i> are on the left (A and C); the comparisons using <i>mth¹</i> are on the right (B and D). Females are above (A and B), males below (C and D). Positive ratios indicate greater risk of death, so the positive ratios for <i>BF51</i> females (A and B) mean that this line showed lower expected lifespan over the <i>mth</i> mutants than over the <i>mth</i> wild-type allele. The heterogeneity in the magnitude and direction of relative risk represents the functional diversity in lifespan among the wild <i>mth</i> lines. Error bars show 95% confidence. Error bars which do not cross the y-axis signify a failure to complement in that line.</p>", "links"=>[], "tags"=>["ratios", "mutants"], "article_id"=>604081, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987.g002", "stats"=>{"downloads"=>2, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Risk_ratios_for_each_line_over_one_of_the_mth_mutants_relative_to_that_line_over_mth_R3_/604081", "title"=>"Risk ratios for each line over one of the <i>mth</i> mutants relative to that line over <i>mth^R3</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-04-16 01:08:01"}
• {"files"=>["https://ndownloader.figshare.com/files/933749"], "description"=>"<p>The comparison using <i>mth^Δ6</i> is on the left (A); the comparison using <i>mth¹</i> is on the right (B). Positive ratios indicate greater risk of death. The heterogeneity in the magnitude and direction of relative odds represents the functional diversity in stress resistance among the wild <i>mth</i> lines. Error bars show 95% confidence. Error bars which do not cross the y-axis signify a failure to complement in that line.</p>", "links"=>[], "tags"=>["ratios", "mutants"], "article_id"=>604202, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Odds_ratios_for_each_line_over_one_of_the_mth_mutants_mth_916_6_or_mth_1_relative_to_the_line_over_mth_R3_/604202", "title"=>"Odds ratios for each line over one of the <i>mth</i> mutants (<i>mth^Δ6</i> or <i>mth¹</i>) relative to the line over <i>mth^R3</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-04-16 01:10:02"}
• {"files"=>["https://ndownloader.figshare.com/files/933798"], "description"=>"<p>Statistical results for the oxidative stress resistance assay.</p>", "links"=>[], "tags"=>["oxidative"], "article_id"=>604248, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987.t003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistical_results_for_the_oxidative_stress_resistance_assay_/604248", "title"=>"Statistical results for the oxidative stress resistance assay.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-04-16 01:10:48"}
• {"files"=>["https://ndownloader.figshare.com/files/933855"], "description"=>"<p>Statistical results for the lifespan assay.</p>", "links"=>[], "tags"=>["lifespan"], "article_id"=>604304, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987.t001", "stats"=>{"downloads"=>5, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistical_results_for_the_lifespan_assay_/604304", "title"=>"Statistical results for the lifespan assay.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-04-16 01:11:44"}
• {"files"=>["https://ndownloader.figshare.com/files/933567"], "description"=>"<p>Males from lines <i>BF54</i> and <i>S97</i> show differences in survivorship, as <i>BF54</i> over <i>mth^Δ6</i> survived the same as <i>BF54</i> over <i>mth^R3,</i> while <i>S97</i> over <i>mth^Δ6</i> survived more poorly than <i>S97</i> over <i>mth^R3</i> (A). These lines also exhibit differences in mortality rate: <i>BF54</i> shows the same mortality rate when paired with <i>mth^Δ6</i> as when paired with <i>mth^R3</i> (B), while <i>S97</i> shows a higher mortality rate when paired with <i>mth^Δ6</i> than when paired with <i>mth^R3</i> (C).</p>", "links"=>[], "tags"=>["paired", "survivorship", "curves", "rates"], "article_id"=>604017, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987.g001", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_sample_comparison_of_paired_survivorship_curves_and_paired_mortality_rates_for_two_wild_lines_/604017", "title"=>"A sample comparison of paired survivorship curves and paired mortality rates for two wild lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-04-16 01:06:57"}
• {"files"=>["https://ndownloader.figshare.com/files/933823"], "description"=>"<p>Statistical results for the fecundity assay.</p>", "links"=>[], "tags"=>["fecundity"], "article_id"=>604276, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987.t002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistical_results_for_the_fecundity_assay_/604276", "title"=>"Statistical results for the fecundity assay.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-04-16 01:11:16"}
• {"files"=>["https://ndownloader.figshare.com/files/459913"], "description"=>"<div><h3>Background</h3><p>Longevity and age-specific patterns of mortality are complex traits that vary within and among taxa. Multiple candidate genes for aging have been identified in model systems by extended longevity mutant phenotypes, including the G-protein coupled receptor <em>methuselah</em> (<em>mth</em>) in <em>D. melanogaster</em>. These genes offer important insights into the mechanisms of lifespan determination and have been major targets of interest in the biology of aging. However, it is largely unknown whether these genes contribute to genetic variance for lifespan in natural populations, and consequently contribute to lifespan evolution.</p><h3>Methodology/Principle Findings</h3><p>For a gene to contribute to genetic variance for a particular trait, it must meet two criteria: natural allelic variation and functional differences among variants. Previous work showed that <em>mth</em> varies significantly among wild populations; here we assess the functional significance of wild-derived <em>mth</em> alleles on lifespan, fecundity and stress resistance using a quantitative complementation scheme. Our results demonstrate that <em>mth</em> alleles segregating in nature have a functional effect on all three traits.</p><h3>Conclusions/Significance</h3><p>These results suggest that allelic variation at <em>mth</em> contributes to observed differences in lifespan and correlated phenotypes in natural populations, and that evaluation of genetic diversity at candidate genes for aging can be a fruitful approach to identifying loci contributing to lifespan evolution.</p></div>", "links"=>[], "tags"=>["allelic", "aging"], "article_id"=>150614, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987", "stats"=>{"downloads"=>5, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Functional_Significance_of_Allelic_Variation_at_methuselah_an_Aging_Gene_in_Drosophila_/150614", "title"=>"Functional Significance of Allelic Variation at <em>methuselah</em>, an Aging Gene in <em>Drosophila</em>", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-04-16 00:10:14"}
• {"files"=>["https://ndownloader.figshare.com/files/933702"], "description"=>"<p>Non-parallel slopes between lines in the three lab-derived <i>mth</i> backgrounds indicate the functional variation in lifetime fecundity among the wild lines. The general increase in eggs laid across the x-axis represents a correlation of increasing fecundity with decreasing background <i>mth</i> expression; all lines but <i>T50</i> showed lowest fecundity when paired with the wild-type <i>mth^R3</i> allele. Error bars show 95% confidence.</p>", "links"=>[], "tags"=>["fecundity", "genotypic"], "article_id"=>604152, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Annalise B. Paaby", "Paul S. Schmidt"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001987.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Average_lifetime_fecundity_per_line_for_all_genotypic_combinations_/604152", "title"=>"Average lifetime fecundity per line for all genotypic combinations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-04-16 01:09:12"}

PMC Usage Stats | Further Information

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Relative Metric

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F1000Prime | Further Information

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• {"year"=>2014, "month"=>10, "doi"=>"10.1371/journal.pone.0001987", "f1000_id"=>"1108073", "url"=>"http://f1000.com/prime/1108073", "score"=>2, "classifications"=>["new_finding"], "updated_at"=>"2014-10-27T08:31:12Z"}
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• {"year"=>2014, "month"=>12, "doi"=>"10.1371/journal.pone.0001987", "f1000_id"=>"1108073", "url"=>"http://f1000.com/prime/1108073", "score"=>2, "classifications"=>["new_finding"], "updated_at"=>"2014-12-29T09:40:46Z"}
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• {"year"=>2015, "month"=>7, "doi"=>"10.1371/journal.pone.0001987", "f1000_id"=>"1108073", "url"=>"http://f1000.com/prime/1108073", "score"=>2, "classifications"=>["new_finding"], "updated_at"=>"2015-07-27T08:40:19Z"}
• {"year"=>2015, "month"=>8, "doi"=>"10.1371/journal.pone.0001987", "f1000_id"=>"1108073", "url"=>"http://f1000.com/prime/1108073", "score"=>2, "classifications"=>["new_finding"], "updated_at"=>"2015-08-31T08:40:23Z"}
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• {"year"=>2015, "month"=>11, "doi"=>"10.1371/journal.pone.0001987", "f1000_id"=>"1108073", "url"=>"http://f1000.com/prime/1108073", "score"=>2, "classifications"=>["new_finding"], "updated_at"=>"2015-11-30T09:40:23Z"}
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• {"year"=>2016, "month"=>1, "doi"=>"10.1371/journal.pone.0001987", "f1000_id"=>"1108073", "url"=>"http://f1000.com/prime/1108073", "score"=>2, "classifications"=>["new_finding"], "updated_at"=>"2016-01-25T09:40:26Z"}
• {"year"=>2016, "month"=>2, "doi"=>"10.1371/journal.pone.0001987", "f1000_id"=>"1108073", "url"=>"http://f1000.com/prime/1108073", "score"=>2, "classifications"=>["new_finding"], "updated_at"=>"2016-02-29T09:40:17Z"}
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