The Evolution of Sex Is Favoured During Adaptation to New Environments
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{"title"=>"The evolution of sex is favoured during adaptation to new environments", "type"=>"journal", "authors"=>[{"first_name"=>"Lutz", "last_name"=>"Becks", "scopus_author_id"=>"8565263400"}, {"first_name"=>"Aneil F.", "last_name"=>"Agrawal", "scopus_author_id"=>"7202771681"}], "year"=>2012, "source"=>"PLoS Biology", "identifiers"=>{"sgr"=>"84861566860", "doi"=>"10.1371/journal.pbio.1001317", "pui"=>"364901029", "pmid"=>"22563299", "scopus"=>"2-s2.0-84861566860", "issn"=>"15449173", "isbn"=>"1545-7885"}, "id"=>"fbbeb9c4-f19b-3f1e-89ce-43eaede2805e", "abstract"=>"Both theory and experiments have demonstrated that sex can facilitate adaptation, potentially yielding a group-level advantage to sex. However, it is unclear whether this process can help solve the more difficult problem of the maintenance of sex within populations. Using experimental populations of the facultatively sexual rotifer Brachionus calyciflorus, we show that rates of sex evolve to higher levels during adaptation but then decline as fitness plateaus. To assess the fitness consequences of genetic mixing, we directly compare the fitnesses of sexually and asexually derived genotypes that naturally occur in our experimental populations. Sexually derived genotypes are more fit than asexually derived genotypes when adaptive pressures are strong, but this pattern reverses as the pace of adaptation slows, matching the pattern of evolutionary change in the rate of sex. These fitness assays test the net effect of sex but cannot be used to disentangle whether selection on sex arises because highly sexual lineages become associated with different allele combinations or with different allele frequencies than less sexual lineages (i.e., \"short-\" or \"long-term\" effects, respectively). We infer which of these mechanisms provides an advantage to sex by performing additional manipulations to obtain fitness distributions of sexual and asexual progeny arrays from unbiased parents (rather than from naturally occurring, and thereby evolutionarily biased, parents). We find evidence that sex breaks down adaptive gene combinations, resulting in lower average fitness of sexual progeny (i.e., a short-term disadvantage to sex). As predicted by theory, the advantage to sex arises because sexually derived progeny are more variable in fitness, allowing for faster adaptation. This \"long-term advantage\" builds over multiple generations, eventually resulting in higher fitness of sexual types.", "link"=>"http://www.mendeley.com/research/evolution-sex-favoured-during-adaptation-new-environments", "reader_count"=>231, "reader_count_by_academic_status"=>{"Unspecified"=>7, "Professor > Associate Professor"=>13, "Librarian"=>1, "Student > Doctoral Student"=>4, "Researcher"=>52, "Student > Ph. D. Student"=>65, "Student > Postgraduate"=>8, "Student > Master"=>40, "Other"=>2, "Student > Bachelor"=>23, "Lecturer"=>4, "Lecturer > Senior Lecturer"=>2, "Professor"=>10}, "reader_count_by_user_role"=>{"Unspecified"=>7, "Professor > Associate Professor"=>13, "Librarian"=>1, "Student > Doctoral Student"=>4, "Researcher"=>52, "Student > Ph. D. Student"=>65, "Student > Postgraduate"=>8, "Student > Master"=>40, "Other"=>2, "Student > Bachelor"=>23, "Lecturer"=>4, "Lecturer > Senior Lecturer"=>2, "Professor"=>10}, "reader_count_by_subject_area"=>{"Unspecified"=>9, "Agricultural and Biological Sciences"=>173, "Philosophy"=>1, "Chemistry"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>2, "Engineering"=>1, "Environmental Science"=>15, "Biochemistry, Genetics and Molecular Biology"=>16, "Mathematics"=>2, "Medicine and Dentistry"=>4, "Neuroscience"=>3, "Social Sciences"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Social Sciences"=>{"Social Sciences"=>2}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>9}, "Environmental Science"=>{"Environmental Science"=>15}, "Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Neuroscience"=>{"Neuroscience"=>3}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>173}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>16}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "Romania"=>1, "United States"=>11, "Japan"=>1, "United Kingdom"=>6, "Portugal"=>2, "Switzerland"=>1, "Spain"=>3, "India"=>2, "Canada"=>4, "Latvia"=>1, "Sweden"=>3, "Netherlands"=>1, "Austria"=>1, "Poland"=>1, "Brazil"=>3, "Italy"=>2, "Mexico"=>1, "France"=>2, "Chile"=>1, "Peru"=>1, "Germany"=>5}, "group_count"=>7}

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  • {"files"=>["https://ndownloader.figshare.com/files/643790"], "description"=>"<p>Replicated rotifer populations were kept for 80 d either in the environment to which they were previously adapted (non-adapting controls, A and B) or moved to a novel environment after 10 d (C and D). (A) Control populations for Environment A, (B) control populations for Environment B, (C) experimental populations adapting to Environment A (B→A); (D) experimental populations adapting to Environment B (A→B). Female density is shown as triangles for populations originating from Environment A (A and D) and as circles for populations originating from Environment B (B and C); points in red (black) represent measurements made in Environment A (B). The percentage of eggs produced by mixis is shown as diamonds for populations originating from Environment A (C and D) and as squares for populations originating from Environment B (B and C); points in brown (grey) represent measurements made in Environment A (B). Error bars denote ±1 standard error. In both environments, investment in sex (measured as percent fertilized mictic eggs) increases and then declines over time for adapting populations (quadratic term: B→A, χ<sup>2</sup> = 106.66, <i>df</i> = 1, <i>p</i><2.2×10<sup>−16</sup>; A→B, χ<sup>2</sup> = 115.58, <i>df</i> = 1, <i>p</i><2.2×10<sup>−16</sup>); there is no such pattern for control populations. Dotted vertical lines mark the time points at which the fertilized mictic and amictic eggs were sampled to compare the fitness of sexual and asexual genotypes (<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001317#pbio-1001317-g002\" target=\"_blank\">Figure 2</a>) and to measure the propensity of sex (<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001317#pbio-1001317-g003\" target=\"_blank\">Figure 3</a>).</p>", "links"=>[], "tags"=>["adapting"], "article_id"=>314289, "categories"=>["Evolutionary Biology"], "users"=>["Lutz Becks", "Aneil F. Agrawal"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001317.g001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Female_density_and_sexual_investment_in_adapting_and_control_populations_/314289", "title"=>"Female density and sexual investment in adapting and control populations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-01 01:11:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/644217"], "description"=>"<p>Comparisons in the distributions of lifetime reproduction between sexually and asexually produced offspring from random sets of parents. Distributions are based on genotypic values, each measured as the mean of five clonal replicates. For the first set of adapting populations, distributions are measured at day 33 and 67; for the second set of adapting populations, distributions are measured at day 53 and 67, corresponding to 16 and 30 d after their initiation, as shown in parentheses. Control populations are measured at each time. (A, B) Ratio (± standard error) of average fitness of sexually produced offspring to that of asexually produced offspring. (C, D) Ratio of variance in fitness of sexually produced genotypes to that of asexually produced genotypes. Variance is calculated as the variance among genotypic means. (E, F) Ratio of the mean fitness of the top 10% of sexually produced genotypes to that of asexually produced genotypes.</p>", "links"=>[], "tags"=>["Evolutionary biology"], "article_id"=>314714, "categories"=>["Evolutionary Biology"], "users"=>["Lutz Becks", "Aneil F. Agrawal"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001317.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Short_and_long_term_effects_of_sex_/314714", "title"=>"Short- and long-term effects of sex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-01 01:18:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/332219", "https://ndownloader.figshare.com/files/332269", "https://ndownloader.figshare.com/files/332347", "https://ndownloader.figshare.com/files/332435", "https://ndownloader.figshare.com/files/332502", "https://ndownloader.figshare.com/files/332560", "https://ndownloader.figshare.com/files/332613"], "description"=>"<div><p>Both theory and experiments have demonstrated that sex can facilitate adaptation, potentially yielding a group-level advantage to sex. However, it is unclear whether this process can help solve the more difficult problem of the maintenance of sex within populations. Using experimental populations of the facultatively sexual rotifer <em>Brachionus calyciflorus</em>, we show that rates of sex evolve to higher levels during adaptation but then decline as fitness plateaus. To assess the fitness consequences of genetic mixing, we directly compare the fitnesses of sexually and asexually derived genotypes that naturally occur in our experimental populations. Sexually derived genotypes are more fit than asexually derived genotypes when adaptive pressures are strong, but this pattern reverses as the pace of adaptation slows, matching the pattern of evolutionary change in the rate of sex. These fitness assays test the net effect of sex but cannot be used to disentangle whether selection on sex arises because highly sexual lineages become associated with different allele combinations or with different allele frequencies than less sexual lineages (i.e., “short-” or “long-term” effects, respectively). We infer which of these mechanisms provides an advantage to sex by performing additional manipulations to obtain fitness distributions of sexual and asexual progeny arrays from unbiased parents (rather than from naturally occurring, and thereby evolutionarily biased, parents). We find evidence that sex breaks down adaptive gene combinations, resulting in lower average fitness of sexual progeny (i.e., a short-term disadvantage to sex). As predicted by theory, the advantage to sex arises because sexually derived progeny are more variable in fitness, allowing for faster adaptation. This “long-term advantage” builds over multiple generations, eventually resulting in higher fitness of sexual types.</p> </div>", "links"=>[], "tags"=>["favoured", "adaptation", "environments"], "article_id"=>125595, "categories"=>["Evolutionary Biology"], "users"=>["Lutz Becks", "Aneil F. Agrawal"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001317.s001", "https://dx.doi.org/10.1371/journal.pbio.1001317.s002", "https://dx.doi.org/10.1371/journal.pbio.1001317.s003", "https://dx.doi.org/10.1371/journal.pbio.1001317.s004", "https://dx.doi.org/10.1371/journal.pbio.1001317.s005", "https://dx.doi.org/10.1371/journal.pbio.1001317.s006", "https://dx.doi.org/10.1371/journal.pbio.1001317.s007"], "stats"=>{"downloads"=>10, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Evolution_of_Sex_Is_Favoured_During_Adaptation_to_New_Environments/125595", "title"=>"The Evolution of Sex Is Favoured During Adaptation to New Environments", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-05-01 01:33:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/644129"], "description"=>"<p>The propensity for sex is measured as percentage of females induced to sexual reproduction when exposed to a standardized stimulus. Data points represent the mean of five replicate populations per treatment ±1 standard error. The grey horizontal lines represent the initial propensity for sex and are shown for reference (upper line for Set 1; lower line for Set 2). The propensity for sex decreases in the control populations (solid lines) independent of the environment. In populations adapting to new environments (dashed lines), the propensity for sex increases and then declines (quadratic term: B→A χ<sup>2</sup> = 18.5, <i>df</i> = 1, <i>p</i> = 1.7×10<sup>−5</sup>; A→B χ<sup>2</sup> = 30.2, <i>df</i> = 1, <i>p</i><2.2×10<sup>−16</sup>). On day 37, a second set of adapting populations were initiated from the controls. They also show an increase in sex (open symbols). The numbers in parentheses on the time axis denote the number of days since initiation of the second set. Note that colour always depicts the environment from which eggs were isolated and in which the assay was performed (red, Environment A; black, Environment B). Grey vertical lines denote time points when high- and low-density subpopulations were started to test for short- and long-term effects of sex (<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001317#pbio-1001317-g004\" target=\"_blank\">Figure 4</a>).</p>", "links"=>[], "tags"=>["propensity", "adapting", "populations", "standardized"], "article_id"=>314629, "categories"=>["Evolutionary Biology"], "users"=>["Lutz Becks", "Aneil F. Agrawal"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001317.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolution_of_the_propensity_for_sex_in_adapting_and_control_populations_measured_under_standardized_conditions_/314629", "title"=>"Evolution of the propensity for sex in adapting and control populations measured under standardized conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-01 01:17:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/643946"], "description"=>"<p>Naturally occurring sexual and asexual eggs are directly isolated from populations; lifetime reproduction is measured on the third clonal generation in the same environment from which the eggs are isolated (red, Environment A; black, Environment B). (A) Control populations in Environment A; (B) control populations in Environment B; (C) populations adapting to Environment A (B→A); (D) populations adapting to Environment B (A→B); sexual and asexuals were assayed at the same time as each other each week but points have been offset for clarity. Each data point represents the average number of offspring of five clonal individuals per genotype of third generation females that were hatched from eggs isolated from the experimental populations. In adapting populations, sexually derived offspring are significantly more fit than asexually derived offspring during the early stages of adaptation but become significantly less fit after adaptation plateaus (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001317#pbio.1001317.s006\" target=\"_blank\">Table S1</a> for statistics). (E) The ratio of the mean fitness of sexual and asexually produced offspring. Genotypes from sexual eggs are represented by open symbols (dashed lines connect mean fitness of five replicate populations across time points) and genotypes from asexual eggs are represented by filled symbols (solid lines connect mean fitness of five replicate populations across time points).</p>", "links"=>[], "tags"=>["asexually", "derived", "offspring", "adapting"], "article_id"=>314441, "categories"=>["Evolutionary Biology"], "users"=>["Lutz Becks", "Aneil F. Agrawal"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001317.g002", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fitness_of_sexually_and_asexually_derived_offspring_from_adapting_and_control_populations_/314441", "title"=>"Fitness of sexually and asexually derived offspring from adapting and control populations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-01 01:14:01"}

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Relative Metric

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