The Evolutionary Origin of Somatic Cells under the Dirty Work Hypothesis
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{"title"=>"The Evolutionary Origin of Somatic Cells under the Dirty Work Hypothesis", "type"=>"journal", "authors"=>[{"first_name"=>"Heather J.", "last_name"=>"Goldsby", "scopus_author_id"=>"15044261900"}, {"first_name"=>"David B.", "last_name"=>"Knoester", "scopus_author_id"=>"19639083400"}, {"first_name"=>"Charles", "last_name"=>"Ofria", "scopus_author_id"=>"8110205600"}, {"first_name"=>"Benjamin", "last_name"=>"Kerr", "scopus_author_id"=>"7102378874"}], "year"=>2014, "source"=>"PLoS Biology", "identifiers"=>{"isbn"=>"1545-7885", "issn"=>"15457885", "pui"=>"373181622", "sgr"=>"84901459020", "pmid"=>"24823361", "scopus"=>"2-s2.0-84901459020", "doi"=>"10.1371/journal.pbio.1001858"}, "id"=>"b7339c4d-7d08-3e7d-b2ab-4253961f733f", "abstract"=>"Reproductive division of labor is a hallmark of multicellular organisms. However, the evolutionary pressures that give rise to delineated germ and somatic cells remain unclear. Here we propose a hypothesis that the mutagenic consequences associated with performing metabolic work favor such differentiation. We present evidence in support of this hypothesis gathered using a computational form of experimental evolution. Our digital organisms begin each experiment as undifferentiated multicellular individuals, and can evolve computational functions that improve their rate of reproduction. When such functions are associated with moderate mutagenic effects, we observe the evolution of reproductive division of labor within our multicellular organisms. Specifically, a fraction of the cells remove themselves from consideration as propagules for multicellular offspring, while simultaneously performing a disproportionately large amount of mutagenic work, and are thus classified as soma. As a consequence, other cells are able to take on the role of germ, remaining quiescent and thus protecting their genetic information. We analyze the lineages of multicellular organisms that successfully differentiate and discover that they display unforeseen evolutionary trajectories: cells first exhibit developmental patterns that concentrate metabolic work into a subset of germ cells (which we call \"pseudo-somatic cells\") and later evolve to eliminate the reproductive potential of these cells and thus convert them to actual soma. We also demonstrate that the evolution of somatic cells enables phenotypic strategies that are otherwise not easily accessible to undifferentiated organisms, though expression of these new phenotypic traits typically includes negative side effects such as aging.", "link"=>"http://www.mendeley.com/research/evolutionary-origin-somatic-cells-under-dirty-work-hypothesis", "reader_count"=>85, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Student > Doctoral Student"=>4, "Researcher"=>23, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>3, "Student > Master"=>6, "Other"=>4, "Student > Bachelor"=>8, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Student > Doctoral Student"=>4, "Researcher"=>23, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>3, "Student > Master"=>6, "Other"=>4, "Student > Bachelor"=>8, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Agricultural and Biological Sciences"=>60, "Philosophy"=>1, "Chemistry"=>1, "Computer Science"=>3, "Earth and Planetary Sciences"=>1, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Mathematics"=>1, "Medicine and Dentistry"=>2, "Physics and Astronomy"=>2, "Psychology"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Psychology"=>{"Psychology"=>1}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}, "Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>60}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Netherlands"=>2, "Sweden"=>1, "United States"=>7, "Japan"=>2, "China"=>1, "United Kingdom"=>2, "Australia"=>1, "France"=>1, "Germany"=>2, "Spain"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1495599"], "description"=>"<p>Each row represents a digital multicell along a study lineage. Circles signify propagule-eligible germ cells. Squares signify propagule-ineligible cells. Color intensity represents the number of mutagenic functions performed by propagule-eligible cells (blue) and propagule-ineligible cells (red). Within this lineage, the ancestral multicell began with all the cells in a pristine state. After (<b>a</b>), the propagule-eligible cells evolved to perform a variety of mutagenic functions and then to segregate their workload, thus producing pseudo-somatic cells (<b>b</b>). Eventually, these pseudo-somatic cells became ineligible to be used as propagules. At this point, they became true somatic cells (<b>c</b>). After this point, the somatic cells continued to perform mutagenic functions at a high level, while the germ cells remained quiescent. The mean propagule-eligible workload is correlated with the number of mutations that would be passed on to an offspring digital multicell. Notably, when germ–soma differentiation occurred (<b>c</b>), the mean propagule-eligible workload decreased, thus protecting the multicell's propagule from mutational damage.</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary theory", "evolutionary", "trajectory"], "article_id"=>1024986, "categories"=>["Biological Sciences"], "users"=>["Heather J. Goldsby", "David B. Knoester", "Charles Ofria", "Benjamin Kerr"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001858.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_evolutionary_trajectory_of_an_example_digital_multicell_/1024986", "title"=>"The evolutionary trajectory of an example digital multicell.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-13 03:09:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1495594"], "description"=>"<p>Each histogram depicts the results for a specified FML with values ranging from 0.0 to 0.075 per-site probability. Each bar specifies the number of replicates (out of 30) that evolved a given proportion of propagule-ineligible cells. The vertical dashed line is the mean. In the absence of mutagenic effects (FML = 0.0) or at very high levels, propagule-ineligible cells failed to become abundant. At intermediate FMLs, peaking at 0.00075, propagule-ineligible cells evolved. Notably, these propagule-ineligible cells perform a disproportionately large amount of the mutagenic work of the multicell (e.g., propagule-ineligible cells within the 0.000075 and 0.00075 treatments evolved to perform 88.67% and 99.01% of the mutagenic work, respectively). Thus, we consider these propagule-ineligible cells to be soma.</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary theory", "mutagenic", "functions", "somatic"], "article_id"=>1024981, "categories"=>["Biological Sciences"], "users"=>["Heather J. Goldsby", "David B. Knoester", "Charles Ofria", "Benjamin Kerr"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001858.g002", "stats"=>{"downloads"=>5, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_mutagenic_functions_on_the_evolution_of_somatic_cells_/1024981", "title"=>"The effect of mutagenic functions on the evolution of somatic cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-13 03:09:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1495602"], "description"=>"<p>Within this study, cells have access via mutation to a variety of instructions that enable them to self-replicate, perform functions, coordinate their behavior, and set their propagation status. In this table, we describe several of the instructions that, when executed, enable a cell to coordinate its behavior with other cells (i.e., <i>get_xy, send_message, retrieve_message, broadcast_message</i>), remove itself from consideration as a propagule (i.e., <i>block_propagation</i>), and conditionally execute instructions within its genome (i.e., <i>if_propagule_eligible, if_propagule_ineligible, if_label, if_less, mov_head</i>).</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary theory", "instructions"], "article_id"=>1024989, "categories"=>["Biological Sciences"], "users"=>["Heather J. Goldsby", "David B. Knoester", "Charles Ofria", "Benjamin Kerr"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001858.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Avida_instructions_used_to_coordinate_behavior_and_differentiate_/1024989", "title"=>"Avida instructions used to coordinate behavior and differentiate.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-05-13 03:09:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1495601"], "description"=>"<p>Over evolutionary time (<b>A</b>), a digital multicell evolves to consume resources more rapidly when young (resources consumed 0–1,000 updates of its lifetime; red line; circles) and relatively much more slowly when old (ratio of resources consumed late within its lifetime [9,000–10,000 updates], as compared with early in its lifetime [0–1,000 updates], blue line; triangles). The black dashed vertical line is the time point at which propagule-ineligible cells evolved. (<b>B</b>) At the beginning of the evolutionary run (the first step along the line of descent), the resource acquisition rate of a digital multicell remains constant throughout its lifetime (0–10,000 updates). (<b>C</b>) At the end of the evolutionary run (the final step along the line of descent), the resource acquisition rate of a digital multicell sharply decreases throughout its lifetime (0–10,000 updates). These results demonstrate antagonistic pleiotropy between resource consumption early in life and aging later in life.</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary theory", "multicell", "aging", "evolutionary"], "article_id"=>1024988, "categories"=>["Biological Sciences"], "users"=>["Heather J. Goldsby", "David B. Knoester", "Charles Ofria", "Benjamin Kerr"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001858.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Measurements_of_digital_multicell_aging_over_evolutionary_time_/1024988", "title"=>"Measurements of digital multicell aging over evolutionary time.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-13 03:09:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1495607", "https://ndownloader.figshare.com/files/1495608", "https://ndownloader.figshare.com/files/1495609", "https://ndownloader.figshare.com/files/1495610", "https://ndownloader.figshare.com/files/1495611", "https://ndownloader.figshare.com/files/1495612", "https://ndownloader.figshare.com/files/1495613", "https://ndownloader.figshare.com/files/1495614", "https://ndownloader.figshare.com/files/1495615", "https://ndownloader.figshare.com/files/1495616", "https://ndownloader.figshare.com/files/1495617", "https://ndownloader.figshare.com/files/1495618"], "description"=>"<div><p>Reproductive division of labor is a hallmark of multicellular organisms. However, the evolutionary pressures that give rise to delineated germ and somatic cells remain unclear. Here we propose a hypothesis that the mutagenic consequences associated with performing metabolic work favor such differentiation. We present evidence in support of this hypothesis gathered using a computational form of experimental evolution. Our digital organisms begin each experiment as undifferentiated multicellular individuals, and can evolve computational functions that improve their rate of reproduction. When such functions are associated with moderate mutagenic effects, we observe the evolution of reproductive division of labor within our multicellular organisms. Specifically, a fraction of the cells remove themselves from consideration as propagules for multicellular offspring, while simultaneously performing a disproportionately large amount of mutagenic work, and are thus classified as soma. As a consequence, other cells are able to take on the role of germ, remaining quiescent and thus protecting their genetic information. We analyze the lineages of multicellular organisms that successfully differentiate and discover that they display unforeseen evolutionary trajectories: cells first exhibit developmental patterns that concentrate metabolic work into a subset of germ cells (which we call “pseudo-somatic cells”) and later evolve to eliminate the reproductive potential of these cells and thus convert them to actual soma. We also demonstrate that the evolution of somatic cells enables phenotypic strategies that are otherwise not easily accessible to undifferentiated organisms, though expression of these new phenotypic traits typically includes negative side effects such as aging.</p></div>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary theory", "evolutionary", "somatic", "cells"], "article_id"=>1024993, "categories"=>["Biological Sciences"], "users"=>["Heather J. Goldsby", "David B. Knoester", "Charles Ofria", "Benjamin Kerr"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001858.s001", "https://dx.doi.org/10.1371/journal.pbio.1001858.s002", "https://dx.doi.org/10.1371/journal.pbio.1001858.s003", "https://dx.doi.org/10.1371/journal.pbio.1001858.s004", "https://dx.doi.org/10.1371/journal.pbio.1001858.s005", "https://dx.doi.org/10.1371/journal.pbio.1001858.s006", "https://dx.doi.org/10.1371/journal.pbio.1001858.s007", "https://dx.doi.org/10.1371/journal.pbio.1001858.s008", "https://dx.doi.org/10.1371/journal.pbio.1001858.s009", "https://dx.doi.org/10.1371/journal.pbio.1001858.s010", "https://dx.doi.org/10.1371/journal.pbio.1001858.s011", "https://dx.doi.org/10.1371/journal.pbio.1001858.s012"], "stats"=>{"downloads"=>11, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Evolutionary_Origin_of_Somatic_Cells_under_the_Dirty_Work_Hypothesis_/1024993", "title"=>"The Evolutionary Origin of Somatic Cells under the Dirty Work Hypothesis", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-05-13 03:09:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1495591"], "description"=>"<p>Cells are either propagule-eligible (circles) or propagule-ineligible (squares). Deeper shades of color represent increased execution of mutagenic functions and, thus, accumulation of mutations in propagule-eligible cells (blue) and propagule-ineligible cells (red). Each cell contains a genetic program that guides its execution; a genome segment encoding one particular computational function (NOT) is shown. The last two depicted lines of the genome demonstrate how simple instructions can be used to evolve phenotypically plastic cells. In particular, the second to last line (<i>if_less</i>) specifies that the next instruction (<i>block_propagation</i>) should be executed only if the value in the <i>BX</i> register (e.g., 10001110100…) is less than the value in the <i>CX</i> register (e.g., 11110111111…). In this case, because the value in <i>BX</i> is indeed less than the value in <i>CX</i>, the <i>block_propagation</i> instruction is executed and thus the cell enters the propagule-ineligible state. However, if the values in the registers were different, then the cell could have remained eligible to be used as a propagule.</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary theory", "consisting", "multicells", "contains", "25"], "article_id"=>1024978, "categories"=>["Biological Sciences"], "users"=>["Heather J. Goldsby", "David B. Knoester", "Charles Ofria", "Benjamin Kerr"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001858.g001", "stats"=>{"downloads"=>5, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_World_consisting_of_digital_multicells_that_each_contains_up_to_25_cells_/1024978", "title"=>"World consisting of digital multicells that each contains up to 25 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-13 03:09:44"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"9", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"23", "full-text"=>"14", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"0", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
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  • {"unique-ip"=>"13", "full-text"=>"21", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
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  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"11"}
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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
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  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
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  • {"unique-ip"=>"14", "full-text"=>"23", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Computational biology", "average_usage"=>[341, 529]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[285]}, {"subject_area"=>"/Biology and life sciences/Zoology", "average_usage"=>[329]}]}
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