Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling
Publication Date
January 15, 2016
Journal
PLOS Biology
Authors
Richard W. R. Wallbank, Simon W. Baxter, Carolina Pardo Diaz, Joseph J. Hanly, et al
Volume
14
Issue
1
Pages
e1002353
DOI
https://dx.plos.org/10.1371/journal.pbio.1002353
Publisher URL
http://journals.plos.org/plosbiology/article?id=10.1371%2Fjournal.pbio.1002353
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/26771987
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4714872
Europe PMC
http://europepmc.org/abstract/MED/26771987
Web of Science
000371882900020
Scopus
84961055477
Mendeley
http://www.mendeley.com/research/evolutionary-novelty-butterfly-wing-pattern-through-enhancer-shuffling
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Mendeley | Further Information

{"title"=>"Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling", "type"=>"journal", "authors"=>[{"first_name"=>"Richard W.R.", "last_name"=>"Wallbank", "scopus_author_id"=>"55484856700"}, {"first_name"=>"Simon W.", "last_name"=>"Baxter", "scopus_author_id"=>"8600199700"}, {"first_name"=>"Carolina", "last_name"=>"Pardo-Diaz", "scopus_author_id"=>"36178306900"}, {"first_name"=>"Joseph J.", "last_name"=>"Hanly", "scopus_author_id"=>"56715333700"}, {"first_name"=>"Simon H.", "last_name"=>"Martin", "scopus_author_id"=>"37102428400"}, {"first_name"=>"James", "last_name"=>"Mallet", "scopus_author_id"=>"7202284097"}, {"first_name"=>"Kanchon K.", "last_name"=>"Dasmahapatra", "scopus_author_id"=>"6602134403"}, {"first_name"=>"Camilo", "last_name"=>"Salazar", "scopus_author_id"=>"8283928400"}, {"first_name"=>"Mathieu", "last_name"=>"Joron", "scopus_author_id"=>"6602305237"}, {"first_name"=>"Nicola", "last_name"=>"Nadeau", "scopus_author_id"=>"6602449934"}, {"first_name"=>"W. Owen", "last_name"=>"McMillan", "scopus_author_id"=>"7004840804"}, {"first_name"=>"Chris D.", "last_name"=>"Jiggins", "scopus_author_id"=>"6603932806"}], "year"=>2016, "source"=>"PLoS Biology", "identifiers"=>{"sgr"=>"84961290731", "pmid"=>"26771987", "pui"=>"607981252", "isbn"=>"1545-7885 (Electronic)\r1544-9173 (Linking)", "scopus"=>"2-s2.0-84961290731", "doi"=>"10.1371/journal.pbio.1002353", "issn"=>"15457885"}, "id"=>"f2672c86-40be-393e-a6c9-61e68f257423", "abstract"=>"An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individu- als across 17 species identified narrow regions associated with two distinct red colour pat- tern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the tim- ing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray origi- nated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.", "link"=>"http://www.mendeley.com/research/evolutionary-novelty-butterfly-wing-pattern-through-enhancer-shuffling", "reader_count"=>158, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>11, "Librarian"=>1, "Researcher"=>30, "Student > Doctoral Student"=>9, "Student > Ph. D. Student"=>48, "Student > Postgraduate"=>5, "Student > Master"=>25, "Other"=>4, "Student > Bachelor"=>11, "Lecturer"=>2, "Professor"=>10}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>11, "Librarian"=>1, "Researcher"=>30, "Student > Doctoral Student"=>9, "Student > Ph. D. 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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2628263"], "description"=>"<p>First row: <i>H</i>. <i>burneyi huebneri</i>, <i>H</i>. <i>aoede auca</i>, and <i>H</i>. <i>xanthocles zamora;</i> second row: <i>H</i>. <i>timareta timareta</i> f. <i>timareta</i>, <i>H</i>. <i>doris doris</i>, and <i>H</i>. <i>demeter ucayalensis;</i> third row: <i>H</i>. <i>melpomene malleti</i>, <i>H</i>. <i>egeria homogena</i>, and <i>H</i>. <i>erato emma</i>; fourth row: <i>H</i>. <i>elevatus pseudocupidineus</i>, <i>Eueides heliconioides eanes</i>, and <i>E</i>. <i>tales calathus</i>; and bottom: <i>Chetone phyleis</i>, a pericopine moth. Stars indicate the three species that are the focus of this study. Butterflies figured are from the Neukirchen Collection, McGuire Centre, Florida. The butterflies are from populations in both Ecuador and Peru.</p>", "links"=>[], "tags"=>["combination", "Butterfly Wing Pattern", "dennis phenotype introgressed", "module", "pattern variation", "Wing Pattern", "region", "Heliconius melpomene", "genome sequence data", "colour pattern elements", "evolutionary novelty", "Amazonian Heliconius butterflies", "Phylogenetic analysis", "ray introgressed", "Enhancer Shuffling", "adaptive radiation", "diversification", "17 species", "control expression", "Enhancer elements", "142 individuals", "novel adaptive", "recombination", "transcription factor optix"], "article_id"=>1638146, "categories"=>["Biological Sciences"], "users"=>["Richard W. R. Wallbank", "Simon W. Baxter", "Carolina Pardo-Diaz", "Joseph J. Hanly", "Simon H. Martin", "James Mallet", "Kanchon K. Dasmahapatra", "Camilo Salazar", "Mathieu Joron", "Nicola Nadeau", "W. Owen McMillan", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002353.g001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Diversity_of_the_Amazonian_dennis_ray_mimicry_ring_/1638146", "title"=>"Diversity of the Amazonian dennis-ray mimicry ring.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-01-28 12:37:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2628352", "https://ndownloader.figshare.com/files/2628353", "https://ndownloader.figshare.com/files/2628354", "https://ndownloader.figshare.com/files/2628355", "https://ndownloader.figshare.com/files/2628356", "https://ndownloader.figshare.com/files/2628357", "https://ndownloader.figshare.com/files/2628358"], "description"=>"<div><p>An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian <i>Heliconius</i> butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, <i>dennis</i> and <i>ray</i>. We hypothesise that these modules in non-coding sequence represent distinct <i>cis</i>-regulatory loci that control expression of the transcription factor <i>optix</i>, which in turn controls red pattern variation across <i>Heliconius</i>. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these <i>cis</i>-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into <i>Heliconius melpomene</i> at about the same time that ray originated in this group, while ray introgressed back into <i>H</i>. <i>elevatus</i> much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.</p></div>", "links"=>[], "tags"=>["combination", "Butterfly Wing Pattern", "dennis phenotype introgressed", "module", "pattern variation", "Wing Pattern", "region", "Heliconius melpomene", "genome sequence data", "colour pattern elements", "evolutionary novelty", "Amazonian Heliconius butterflies", "Phylogenetic analysis", "ray introgressed", "Enhancer Shuffling", "adaptive radiation", "diversification", "17 species", "control expression", "Enhancer elements", "142 individuals", "novel adaptive", "recombination", "transcription factor optix"], "article_id"=>1638182, "categories"=>["Biological Sciences"], "users"=>["Richard W. R. Wallbank", "Simon W. Baxter", "Carolina Pardo-Diaz", "Joseph J. Hanly", "Simon H. Martin", "James Mallet", "Kanchon K. Dasmahapatra", "Camilo Salazar", "Mathieu Joron", "Nicola Nadeau", "W. Owen McMillan", "Chris D. Jiggins"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1002353.s001", "https://dx.doi.org/10.1371/journal.pbio.1002353.s002", "https://dx.doi.org/10.1371/journal.pbio.1002353.s003", "https://dx.doi.org/10.1371/journal.pbio.1002353.s004", "https://dx.doi.org/10.1371/journal.pbio.1002353.s005", "https://dx.doi.org/10.1371/journal.pbio.1002353.s006", "https://dx.doi.org/10.1371/journal.pbio.1002353.s007"], "stats"=>{"downloads"=>6, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_Novelty_in_a_Butterfly_Wing_Pattern_through_Enhancer_Shuffling_/1638182", "title"=>"Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2016-01-28 12:37:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/2628265"], "description"=>"<p>(A) Examples of the principal red wing patterns: dennis-ray <i>H</i>. <i>e</i>. <i>pseudocupidineus</i> and <i>H</i>. <i>m</i>. <i>malleti</i>, dennis-only <i>H</i>. <i>m</i>. <i>meriana</i>, ray-only <i>H</i>. <i>t</i>. <i>timareta</i> f. <i>contigua</i>, and band <i>H</i>. <i>m</i>. <i>rosina</i>. (B) Association analysis across 96 genomes showing statistical association for the dennis (red dots) and ray phenotypes (orange dots). The horizontal black line represents significance after Bonferroni correction. Boxes show exon positions. (C) Sliding window analysis of fixed differences between specific comparisons to identify dennis- and ray-associated sites (orange and red lines—see also <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.s001\" target=\"_blank\">S1 Fig</a> and <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.s004\" target=\"_blank\">S1 Table</a>). (D) Recombination breakpoints allowed separate isolation of regions fully associated with dennis and ray phenotypes. Informative haplotypes are shown (<i>H</i>. <i>elevatus</i>, <i>H</i>. <i>m</i>. <i>malleti</i>, <i>H</i>. <i>t</i>. <i>timareta</i> f. <i>contigua</i>, <i>H</i>. <i>m</i>. <i>meriana</i>, and <i>H</i>. <i>m</i>. <i>rosina</i>, phenotypes shown above). Genotypes are indicated as D/d for <i>dennis</i> present/absent and R/r for <i>ray</i> present/absent. A <i>H</i>. <i>melpomene</i> recombinant hybrid was heterozygous in the <i>dennis</i> region and homozygous for <i>ray</i>-absent, as expected, but was not informative for precise breakpoint delineation because of missing data. See Dryad depository for plot data [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.ref032\" target=\"_blank\">32</a>].</p>", "links"=>[], "tags"=>["combination", "Butterfly Wing Pattern", "dennis phenotype introgressed", "module", "pattern variation", "Wing Pattern", "region", "Heliconius melpomene", "genome sequence data", "colour pattern elements", "evolutionary novelty", "Amazonian Heliconius butterflies", "Phylogenetic analysis", "ray introgressed", "Enhancer Shuffling", "adaptive radiation", "diversification", "17 species", "control expression", "Enhancer elements", "142 individuals", "novel adaptive", "recombination", "transcription factor optix"], "article_id"=>1638148, "categories"=>["Biological Sciences"], "users"=>["Richard W. R. Wallbank", "Simon W. Baxter", "Carolina Pardo-Diaz", "Joseph J. Hanly", "Simon H. Martin", "James Mallet", "Kanchon K. Dasmahapatra", "Camilo Salazar", "Mathieu Joron", "Nicola Nadeau", "W. Owen McMillan", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002353.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genotype_by_phenotype_association_analyses_and_mapping_of_dennis_and_ray_regions_/1638148", "title"=>"Genotype-by-phenotype association analyses and mapping of <i>dennis</i> and <i>ray</i> regions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-01-28 12:37:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/2628266"], "description"=>"<p>Each group of alleles is characterised by a complex structure of insertion and deletion variation. Horizontal bars represent aligned allele sequences for the outgroups (A), silvaniforms (B), <i>H</i>. <i>elevatus</i> (C), dennis morph melpomene/timareta (D), non-dennis morph melpomene/timareta (E), and the cydno/heurippa/pachinus clade (F). There are three general forms of the region: an “outgroup” allele (X) with many indels and lacking large sections of sequence; a silvaniform/dennis allele (Y), which possesses indel 1 and lacks indel 2; and a non-dennis/cydno allele (Z), which lacks indel 1 and possesses indel 2. Dotted lines and blue colouration indicate the point where dennis-morph melpomene/timareta alleles become silvaniform like (left) and where the dennis-only morph, <i>H</i>. <i>m</i>. <i>meriana</i>, recombines with the other non-rayed melpomene (right). Fixed SNPs in perfect association with the dennis phenotype are indicated by yellow asterisks and form two clusters. See Dryad depository for alignment [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.ref032\" target=\"_blank\">32</a>].</p>", "links"=>[], "tags"=>["combination", "Butterfly Wing Pattern", "dennis phenotype introgressed", "module", "pattern variation", "Wing Pattern", "region", "Heliconius melpomene", "genome sequence data", "colour pattern elements", "evolutionary novelty", "Amazonian Heliconius butterflies", "Phylogenetic analysis", "ray introgressed", "Enhancer Shuffling", "adaptive radiation", "diversification", "17 species", "control expression", "Enhancer elements", "142 individuals", "novel adaptive", "recombination", "transcription factor optix"], "article_id"=>1638149, "categories"=>["Biological Sciences"], "users"=>["Richard W. R. Wallbank", "Simon W. Baxter", "Carolina Pardo-Diaz", "Joseph J. Hanly", "Simon H. Martin", "James Mallet", "Kanchon K. Dasmahapatra", "Camilo Salazar", "Mathieu Joron", "Nicola Nadeau", "W. Owen McMillan", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002353.g003", "stats"=>{"downloads"=>2, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_overview_of_the_dennis_region_alignment_architecture_/1638149", "title"=>"Schematic overview of the <i>dennis</i> region alignment architecture.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-01-28 12:55:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/2628267"], "description"=>"<p>(A) The phylogeny of species used in this study (left, from [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.ref014\" target=\"_blank\">14</a>]) and their respective combinations of <i>dennis</i> and <i>ray</i> haplotypes (right). Note that although genetic data for <i>Heliconius elevatus roraima</i> are not analysed here or included in our alignment, this taxon is shown for completeness. Representative butterfly phenotypes are shown with their respective subspecies or form names. <i>H</i>. <i>e</i>. <i>pseudocupidineus</i> is abbreviated to pseudoc. (B) ML trees with bootstraps (generated using de novo assembled genomes) show that the <i>dennis</i> alleles cluster with the silvaniform clade (left), whilst the <i>ray</i> alleles cluster with the melpomene/timareta clade (right). Terminal nodes are coloured by silvaniform clade (green, except <i>H</i>. <i>elevatus</i>), dennis/ray (red, <i>H</i>. <i>melpomene/timareta</i>; burgundy, <i>H</i>. <i>elevatus</i>), <i>melpomene/timareta</i> non-dennis/ray forms (blue), and <i>cydno/pachinus/heurippa</i> clade (purple). Outgroup species are in black (see also <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.s002\" target=\"_blank\">S2 Fig</a> for sample labels). <i>H</i>. <i>m</i>. <i>meriana</i> and <i>H</i>. <i>t</i>. <i>timareta</i> f. <i>contigua</i> have dennis-only and ray-only patterns, respectively, and cluster with their expected phenotypes. All trees were rooted to <i>H</i>. <i>aoede</i>. Bootstraps are given as percentages of 1,000 iterations.</p>", "links"=>[], "tags"=>["combination", "Butterfly Wing Pattern", "dennis phenotype introgressed", "module", "pattern variation", "Wing Pattern", "region", "Heliconius melpomene", "genome sequence data", "colour pattern elements", "evolutionary novelty", "Amazonian Heliconius butterflies", "Phylogenetic analysis", "ray introgressed", "Enhancer Shuffling", "adaptive radiation", "diversification", "17 species", "control expression", "Enhancer elements", "142 individuals", "novel adaptive", "recombination", "transcription factor optix"], "article_id"=>1638150, "categories"=>["Biological Sciences"], "users"=>["Richard W. R. Wallbank", "Simon W. Baxter", "Carolina Pardo-Diaz", "Joseph J. Hanly", "Simon H. Martin", "James Mallet", "Kanchon K. Dasmahapatra", "Camilo Salazar", "Mathieu Joron", "Nicola Nadeau", "W. Owen McMillan", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002353.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Modularity_of_dennis_and_ray_and_phylogenetic_relationships_among_alleles_at_both_loci_/1638150", "title"=>"Modularity of <i>dennis</i> and <i>ray</i> and phylogenetic relationships among alleles at both loci.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-01-28 12:37:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2628268"], "description"=>"<p>Key events indicated on the x-axis are (A) introgression of <i>dennis</i> from <i>H</i>. <i>elevatus</i> into <i>H</i>. <i>melpomene</i>, inferred from the coalescence time of alleles sampled from these two species; (B) the origin of <i>ray</i> alleles within <i>H</i>. <i>melpomene</i>, inferred from the coalescence of <i>dennis</i> and non-<i>dennis</i> alleles within <i>H</i>. <i>melpomene</i>; (C) introgression of <i>ray</i> into <i>H</i>. <i>timareta</i>; (D) introgression of ray into <i>H</i>. <i>elevatus</i>, and (E) introgression of <i>dennis</i> into <i>H</i>. <i>timareta</i>. Dating of phylogenies was carried out using BEAST, and full dated trees with support limits are provided in <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.s003\" target=\"_blank\">S3 Fig</a>. The species tree is derived from [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002353#pbio.1002353.ref014\" target=\"_blank\">14</a>].</p>", "links"=>[], "tags"=>["combination", "Butterfly Wing Pattern", "dennis phenotype introgressed", "module", "pattern variation", "Wing Pattern", "region", "Heliconius melpomene", "genome sequence data", "colour pattern elements", "evolutionary novelty", "Amazonian Heliconius butterflies", "Phylogenetic analysis", "ray introgressed", "Enhancer Shuffling", "adaptive radiation", "diversification", "17 species", "control expression", "Enhancer elements", "142 individuals", "novel adaptive", "recombination", "transcription factor optix"], "article_id"=>1638151, "categories"=>["Biological Sciences"], "users"=>["Richard W. R. Wallbank", "Simon W. Baxter", "Carolina Pardo-Diaz", "Joseph J. Hanly", "Simon H. Martin", "James Mallet", "Kanchon K. Dasmahapatra", "Camilo Salazar", "Mathieu Joron", "Nicola Nadeau", "W. Owen McMillan", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002353.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hypothesis_for_the_origins_and_introgression_of_the_dennis_and_ray_regions_inferred_from_dated_trees_/1638151", "title"=>"Hypothesis for the origins and introgression of the <i>dennis</i> and <i>ray</i> regions inferred from dated trees.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2016-01-28 12:37:00"}

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

Relative Metric

{"start_date"=>"2016-01-01T00:00:00Z", "end_date"=>"2016-12-31T00:00:00Z", "subject_areas"=>[]}
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