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{"title"=>"Why men matter: Mating patterns drive evolution of human lifespan", "type"=>"journal", "authors"=>[{"first_name"=>"Shripad D.", "last_name"=>"Tuljapurkar", "scopus_author_id"=>"7003415922"}, {"first_name"=>"Cedric O.", "last_name"=>"Puleston", "scopus_author_id"=>"23976541300"}, {"first_name"=>"Michael D.", "last_name"=>"Gurven", "scopus_author_id"=>"6602909086"}], "year"=>2007, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-39649098724", "pui"=>"351386022", "doi"=>"10.1371/journal.pone.0000785", "isbn"=>"1932-6203", "sgr"=>"39649098724", "pmid"=>"17726515"}, "id"=>"9b640a02-e8ea-37d2-8fbb-8541d8645d33", "abstract"=>"Evolutionary theory predicts that senescence, a decline in survival rates with age, is the consequence of stronger selection on alleles that affect fertility or mortality earlier rather than later in life. Hamilton quantified this argument by showing that a rare mutation reducing survival is opposed by a selective force that declines with age over reproductive life. He used a female-only demographic model, predicting that female menopause at age ca. 50 yrs should be followed by a sharp increase in mortality, a “wall of death.” Human lives obviously do not display such a wall. Explanations of the evolution of lifespan beyond the age of female menopause have proven difficult to describe as explicit genetic models. Here we argue that the inclusion of males and mating patterns extends Hamilton's theory and predicts the pattern of human senescence. We analyze a general two-sex model to show that selection favors survival for as long as men reproduce. Male fertility can only result from matings with fertile females, and we present a range of data showing that males much older than 50 yrs have substantial realized fertility through matings with younger females, a pattern that was likely typical among early humans. Thus old-age male fertility provides a selective force against autosomal deleterious mutations at ages far past female menopause with no sharp upper age limit, eliminating the wall of death. Our findings illustrate the evolutionary importance of males and mating preferences, and show that one-sex demographic models are insufficient to describe the forces that shape human senescence.", "link"=>"http://www.mendeley.com/research/men-matter-mating-patterns-drive-evolution-human-lifespan", "reader_count"=>129, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>10, "Researcher"=>36, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>2, "Student > Master"=>11, "Other"=>7, "Student > Bachelor"=>8, "Lecturer"=>3, "Professor"=>16}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>10, "Researcher"=>36, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>2, "Student > Master"=>11, "Other"=>7, "Student > Bachelor"=>8, "Lecturer"=>3, "Professor"=>16}, "reader_count_by_subject_area"=>{"Unspecified"=>9, "Agricultural and Biological Sciences"=>64, "Arts and Humanities"=>6, "Philosophy"=>2, "Business, Management and Accounting"=>1, "Decision Sciences"=>1, "Economics, Econometrics and Finance"=>2, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>3, "Mathematics"=>1, "Medicine and Dentistry"=>7, "Physics and Astronomy"=>2, "Psychology"=>3, "Social Sciences"=>23, "Immunology and Microbiology"=>1, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Social Sciences"=>{"Social Sciences"=>23}, "Decision Sciences"=>{"Decision Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Psychology"=>{"Psychology"=>3}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>9}, "Environmental Science"=>{"Environmental Science"=>3}, "Arts and Humanities"=>{"Arts and Humanities"=>6}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>64}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Philosophy"=>{"Philosophy"=>2}}, "reader_count_by_country"=>{"Austria"=>1, "Netherlands"=>1, "United States"=>5, "Egypt"=>1, "United Kingdom"=>3, "Mexico"=>1, "France"=>2, "Chile"=>1, "Germany"=>1}, "group_count"=>1}

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• {"referral"=>"http://www.npr.org/sections/health-shots/2016/09/21/494567746/flabby-and-fertile-why-how-men-age-matters-for-the-rest-of-us", "language"=>"English", "title"=>"As Men Age, Putting On Pudge May Aid Survival Of The Species : Shots - Health News : NPR", "type"=>"News", "publication"=>"NPR.org", "published_on"=>"", "link_state"=>"APPROVED", "id"=>59185, "created"=>"2016-09-22T07:23:48.000Z", "crowdsourced"=>false, "article"=>{"id"=>19498, "doi"=>"10.1371/journal.pone.0000785", "title"=>"Why Men Matter: Mating Patterns Drive Evolution of Human Lifespan", "published_on"=>"2007-08-29T00:00:00.000Z"}}

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• {"url"=>"http%3A%2F%2Fjournals.plos.org%2Fplosone%2Farticle%3Fid%3D10.1371%252Fjournal.pone.0000785", "share_count"=>1, "like_count"=>0, "comment_count"=>0, "click_count"=>0, "total_count"=>1}

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• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/ec65f2a5-e12b-4925-add3-f0c955c1dc25", "title"=>"Much needed addition to an important topic", "body"=>"This is a fascinating model. In my own work I had seen the genetic correlation between male and female longevity (in insects) as a constraint on optimisation of separate life-histories. This paper has entirely changed my thinking about the evolutioanry relationships between sex and longevity.", "isRemoved"=>false, "created"=>"2007-08-31T00:50:05Z", "lastModified"=>"2007-08-31T00:50:05Z", "creator"=>{"userId"=>"55245"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000785", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2007-08-31T00:50:05Z", "replies"=>[]}
• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/52f72dfc-8aa3-4081-b942-65af7d535d00", "title"=>"Referee Comments: Referee 2 (Conrad Istock)", "body"=>"Reviewer 2's Review (Conrad Istock)\n\n“Initial comments and observations after reading the Abstract. \n\nIt is likely that most men and women in early human populations did not live to the age of 50. Some group leader males may have lived much longer and reproduced, but would likely have many deleterious mutations in their sperm, probably reducing the viability and survival of offspring. There is also the possibility that selection in these early populations might have favored longer, post-menopausal, survival of some women who performed behavioral roles that enhanced group survival. Such has been claimed for post reproductive female elk who guide their groups over routes they know will efficiently move them between summer and winter habitats. This is akin to the \"grandmother\" scenario cited in the introduction. At some point we will also have to face the fact that traditionally women live longer then men on average, though the gap is closing. \n\nGeneral comments. \n\nI like the problem addressed here and the approach is intriguing. It is truly provocative and for that reason alone I hope it will be published.\n \nI wonder how realistic the stability assumptions, for example p. 11, are. Early humans may have experienced incessant fluctuations in their demography. They, like the more recent analogues, probably lived in small groups innocent of stable age distributions and so on. \n\nI found the jumping back and forth between this new approach and Hamilton's awkward. Why not just give the Hamilton review early on with figure 1 and S=0 and then move on logically (unbroken) with the two sex development? Returning once more to the contrast in the discussion. \n\nWhy do females come with a finite supply of eggs?”\n\nN.B. These are the general comments made by the reviewer when reviewing this paper in light of which the manuscript was revised. Specific points addressed during revision of the paper are not shown.\n", "isRemoved"=>false, "created"=>"2007-09-04T10:56:38Z", "lastModified"=>"2007-09-04T10:56:38Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000785", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2007-09-04T10:56:38Z", "replies"=>[]}
• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/b3766beb-6047-4ead-866b-33ceb7738121", "title"=>"The next questions...", "body"=>"This is a nice paper and makes an important point. Still, there are several questions it cannot answer:\n\n1) Why doesn't the age of menopause increase to parallel male lifespan? I.e., the cost or trade-offs involved must be different for the reproductive aging and somatic aging.\n\n2) Why do female mammals live longer than males?\n\n3) In the other species with the clearest female post-reproductive lifespan, Short-finned Pilot Whales, the oldest fertile female observed was 39, the oldest living female was 63, and the oldest living male was 43, so for this species it seems impossible that a similar explanation could apply. Why the differences?\n\nI have no answers to these questions at the moment, but believe that we must understand the physiology of reproductive and somatic aging in order to address them. For example, there is still no good explanation for why most oocytes are produced before birth in most mammals - it is the decline in these oocytes that results in female reproductive aging.", "isRemoved"=>false, "created"=>"2007-10-23T19:08:04Z", "lastModified"=>"2007-10-23T19:08:04Z", "creator"=>{"userId"=>"164005"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000785", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2007-10-23T19:08:04Z", "replies"=>[]}
• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/5a2b5d22-f05e-4e35-a813-43a9ac9ce8e5", "title"=>"Media Coverage of this Article", "body"=>"The following article represents some of the media coverage that has occurred for this paper:\n\nPublication: LA Times \nTitle: “Did menopause arise because men prefer younger women? - latimes.com”\nhttp://www.latimes.com/news/science/sciencenow/la-sci-sn-menopause-evolution-20130613,0,5275115.story\n\nIf you see any additional coverage of this paper in the press or blogosphere, please reply to this thread and add the link to the article. \n", "isRemoved"=>false, "created"=>"2013-06-14T23:15:54Z", "lastModified"=>"2013-06-14T23:15:54Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>true, "hasCompetingInterests"=>true, "body"=>"PLoS ONE staff"}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000785", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2013-06-14T23:15:54Z", "replies"=>[]}

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• {"id"=>"656109701449543680", "text"=>"This week's journal club's paper: Why Men Matter: Mating Patterns Drive Evolution of Human Lifespan. http://t.co/MM9SP3hVi3 #EvolTheoPloen", "created_at"=>"2015-10-19T14:08:37Z", "user"=>"jorgeapenas", "user_name"=>"Jorge Peña", "user_profile_image"=>"http://pbs.twimg.com/profile_images/490889312238440449/_nYrfWps_normal.jpeg"}
• {"id"=>"919944840439361537", "text"=>"(Fue propuesta inicialmente por Tuljapurkar & al en este p?iper de 2007:)\nhttps://t.co/IGUNX2l9yg", "created_at"=>"2017-10-16T15:15:16Z", "user"=>"SimonPerera", "user_name"=>"Sim?n Perera ??", "user_profile_image"=>"http://pbs.twimg.com/profile_images/899790851068571649/wfNJskSE_normal.jpg"}
• {"id"=>"919958587832664064", "text"=>"RT @SimonPerera: (Fue propuesta inicialmente por Tuljapurkar & al en este p?iper de 2007:)\nhttps://t.co/IGUNX2l9yg", "created_at"=>"2017-10-16T16:09:54Z", "user"=>"pepxabiagen", "user_name"=>"Pep", "user_profile_image"=>"http://pbs.twimg.com/profile_images/593004862507462656/9TVYttlS_normal.jpg"}

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/945983"], "description"=>"<p>This figure shows the force of selection by age, <i>S</i>(<i>x</i>), as a fraction of the force of selection at birth, <i>S</i>(0), as described by Hamilton using female-only demography. (a) Hamilton's one-sex force of selection at age <i>x</i> (shown relative to its value at birth) falls to zero with the decline of remaining survival-weighted female reproduction. b is the inverse of the top panel. In mutation-selection balance, the frequency of deleterious mutant alleles is expected to be proportional to 1/<i>S</i>, where <i>S</i> is the force of selection for a dominant or semi-dominant allele. The inverse of the force of selection is an indicator of age-specific mortality. The rapid increase in mortality at female menopause is the ‘wall of death.’</p>", "links"=>[], "tags"=>["ecology/evolutionary ecology", "ecology/population ecology", "ecology/theoretical ecology", "evolutionary biology/evolutionary ecology", "evolutionary biology/sexual behavior", "genetics and genomics/population genetics", "evolutionary biology/human evolution"], "article_id"=>616337, "categories"=>["Evolutionary Biology", "Ecology", "Genetics"], "users"=>["Shripad D. Tuljapurkar", "Cedric O. Puleston", "Michael D. Gurven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000785.g001", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_wall_of_death_/616337", "title"=>"The wall of death.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-29 01:45:37"}
• {"files"=>["https://ndownloader.figshare.com/files/946236"], "description"=>"<p>In a the dashed red line shows the relative force of selection (as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000785#pone-0000785-g001\" target=\"_blank\">Fig. 1</a>) on a forager population with a life expectancy of 33.5 years using female-only demography. The solid blue line shows the two-sex relative force of selection and reveals an active defense against deleterious mutations into the 65–70 yr age interval. b shows the inverse of the force of selection, which describes the pattern of mortality. The wall of death is replaced by a gradual rise in mortality until very late ages.</p>", "links"=>[], "tags"=>["eliminates"], "article_id"=>616595, "categories"=>["Evolutionary Biology", "Ecology", "Genetics"], "users"=>["Shripad D. Tuljapurkar", "Cedric O. Puleston", "Michael D. Gurven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000785.g004", "stats"=>{"downloads"=>3, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Two_sex_model_eliminates_wall_of_death_/616595", "title"=>"Two-sex model eliminates wall of death.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-29 01:49:55"}
• {"files"=>["https://ndownloader.figshare.com/files/465442"], "description"=>"<div><p>Evolutionary theory predicts that senescence, a decline in survival rates with age, is the consequence of stronger selection on alleles that affect fertility or mortality earlier rather than later in life. Hamilton quantified this argument by showing that a rare mutation reducing survival is opposed by a selective force that declines with age over reproductive life. He used a female-only demographic model, predicting that female menopause at age ca. 50 yrs should be followed by a sharp increase in mortality, a “wall of death.” Human lives obviously do not display such a wall. Explanations of the evolution of lifespan beyond the age of female menopause have proven difficult to describe as explicit genetic models. Here we argue that the inclusion of males and mating patterns extends Hamilton's theory and predicts the pattern of human senescence. We analyze a general two-sex model to show that selection favors survival for as long as men reproduce. Male fertility can only result from matings with fertile females, and we present a range of data showing that males much older than 50 yrs have substantial realized fertility through matings with younger females, a pattern that was likely typical among early humans. Thus old-age male fertility provides a selective force against autosomal deleterious mutations at ages far past female menopause with no sharp upper age limit, eliminating the wall of death. Our findings illustrate the evolutionary importance of males and mating preferences, and show that one-sex demographic models are insufficient to describe the forces that shape human senescence.</p></div>", "links"=>[], "tags"=>["men", "mating", "patterns", "lifespan"], "article_id"=>151756, "categories"=>["Evolutionary Biology", "Ecology", "Genetics"], "users"=>["Shripad D. Tuljapurkar", "Cedric O. Puleston", "Michael D. Gurven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000785", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Why_Men_Matter_Mating_Patterns_Drive_Evolution_of_Human_Lifespan/151756", "title"=>"Why Men Matter: Mating Patterns Drive Evolution of Human Lifespan", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2007-08-29 00:29:16"}
• {"files"=>["https://ndownloader.figshare.com/files/946081"], "description"=>"<p>Fertility distributions (in age-specific fertility rates as a fraction of total fertility rate) for women (dashed red) and men (solid blue) for (a) the hunter-gatherer Dobe !Kung of Botswana, (b) the forest-living Ache, (c) the Amazonian forager-horticulturalist Yanomamo, (d) Bolivian forager-horticulturalists the Tsimane, (e) agricultural Gambian villagers, (f) modern Canada. The blue shaded area represents realized male fertility after the age of last female reproduction.</p>", "links"=>[], "tags"=>["distributions"], "article_id"=>616453, "categories"=>["Evolutionary Biology", "Ecology", "Genetics"], "users"=>["Shripad D. Tuljapurkar", "Cedric O. Puleston", "Michael D. Gurven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000785.g002", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Observed_distributions_of_female_and_male_fertility_/616453", "title"=>"Observed distributions of female and male fertility.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-29 01:47:33"}
• {"files"=>["https://ndownloader.figshare.com/files/946179"], "description"=>"<p>Male fertility in1980 France (black), Pakistan 1984 (blue dots) and Cameroon 1964 (red dashes). Redrawn from Paget and Timaeus <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000785#pone.0000785-Paget1\" target=\"_blank\">[24]</a> Cameroon's distribution is common of high-fertility polygynous societies. The Y-axis shows age-specific fertility rates as a fraction of the total fertility rate.</p>", "links"=>[], "tags"=>["fertility"], "article_id"=>616545, "categories"=>["Evolutionary Biology", "Ecology", "Genetics"], "users"=>["Shripad D. Tuljapurkar", "Cedric O. Puleston", "Michael D. Gurven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000785.g003", "stats"=>{"downloads"=>5, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Three_distinct_male_fertility_distributions_/616545", "title"=>"Three distinct male fertility distributions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-29 01:49:05"}

PMC Usage Stats | Further Information

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Relative Metric

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F1000Prime