Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in the Heliconius melpomene Clade
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{"title"=>"Genomic Hotspots for Adaptation : The Population ¨ llerian Mimicry in the Heliconius Genetics of Mu melpomene Clade", "type"=>"journal", "authors"=>[{"first_name"=>"Simon W.", "last_name"=>"Baxter"}, {"first_name"=>"Nicola J", "last_name"=>"Nadeau"}, {"first_name"=>"Luana S", "last_name"=>"Maroja"}, {"first_name"=>"Paul", "last_name"=>"Wilkinson"}, {"first_name"=>"Brian A.", "last_name"=>"Counterman"}, {"first_name"=>"Margarita", "last_name"=>"Beltran"}, {"first_name"=>"Silvia", "last_name"=>"Perez-espona"}, {"first_name"=>"Nicola", "last_name"=>"Chamberlain"}, {"first_name"=>"Laura", "last_name"=>"Ferguson"}, {"first_name"=>"Claire", "last_name"=>"Davidson"}, {"first_name"=>"Rebecca", "last_name"=>"Glithero"}, {"first_name"=>"James", "last_name"=>"Mallet"}, {"first_name"=>"W Owen", "last_name"=>"Mcmillan"}, {"first_name"=>"Marcus", "last_name"=>"Kronforst"}, {"first_name"=>"Mathieu", "last_name"=>"Joron"}, {"first_name"=>"H", "last_name"=>"Richard"}, {"first_name"=>"Chris D.", "last_name"=>"Jiggins"}], "year"=>2010, "source"=>"Genetics", "identifiers"=>{"issn"=>"1553-7404", "doi"=>"10.1371/journal.pgen.1000794", "pmid"=>"20140188", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)"}, "id"=>"2d92ddc6-0137-3bb2-912c-da0662ac701c", "abstract"=>"Wing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are \"hotspots\" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by approximately 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.", "link"=>"http://www.mendeley.com/research/genomic-hotspots-adaptation-population-llerian-mimicry-heliconius-genetics-mu-melpomene-clade", "reader_count"=>92, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>25, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>7, "Student > Master"=>12, "Other"=>4, "Student > Bachelor"=>7, "Lecturer"=>2, "Professor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>25, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>7, "Student > Master"=>12, "Other"=>4, "Student > Bachelor"=>7, "Lecturer"=>2, "Professor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>82, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>82}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Austria"=>1, "United States"=>2, "United Kingdom"=>3, "Mexico"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/864595"], "description"=>"<p>Sequenced <i>H. melpomene</i> BAC clones across the 721 kb <i>HmB</i> locus and the 330 kb <i>HmYb</i> locus as defined by recombination mapping. In total 24 predicted genes were identified in the <i>HmB</i> region and 20 in the <i>HmYb</i> region. AEHM-22C5 and AEHM-7G5 are overlapping clones from different fingerprinted contigs, and both contain part of the <i>Mad</i> gene. Also see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000794#pgen.1000794.s005\" target=\"_blank\">Table S1</a> for <i>HmB</i> annotation and ref. 65 for <i>HmYb</i> annotation.</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary biology/animal genetics", "evolutionary biology/bioinformatics", "evolutionary biology/developmental evolution", "evolutionary biology/evolutionary and comparative genetics", "evolutionary biology/genomics", "evolutionary biology/pattern formation"], "article_id"=>535020, "categories"=>["Evolutionary Biology"], "users"=>["Simon W. Baxter", "Nicola J. Nadeau", "Luana S. Maroja", "Paul Wilkinson", "Brian A. Counterman", "Anna Dawson", "Margarita Beltrán", "Silvia Perez-Espona", "Nicola Chamberlain", "Laura Ferguson", "Richard Clark", "Claire Davidson", "Rebecca Glithero", "James Mallet", "W. Owen McMillan", "Marcus Kronforst", "Mathieu Joron", "Richard H. ffrench-Constant", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000794.g001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Annotation_of_the_HmB_and_HmYb_gene_regions_/535020", "title"=>"Annotation of the <i>HmB</i> and <i>HmYb</i> gene regions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:23:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/865169"], "description"=>"<p>Values are the mean F<i><sub>ST</sub></i> values across all the sequenced loci ± standard deviations; n indicates the number of loci included in the analysis.</p>", "links"=>[], "tags"=>["differentiation", "locus", "compared", "unlinked", "loci", "races"], "article_id"=>535605, "categories"=>["Evolutionary Biology"], "users"=>["Simon W. Baxter", "Nicola J. Nadeau", "Luana S. Maroja", "Paul Wilkinson", "Brian A. Counterman", "Anna Dawson", "Margarita Beltrán", "Silvia Perez-Espona", "Nicola Chamberlain", "Laura Ferguson", "Richard Clark", "Claire Davidson", "Rebecca Glithero", "James Mallet", "W. Owen McMillan", "Marcus Kronforst", "Mathieu Joron", "Richard H. ffrench-Constant", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000794.t001", "stats"=>{"downloads"=>3, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_population_differentiation_at_the_HmYb_locus_compared_to_unlinked_loci_between_species_and_between_races_of_Heliconius_/535605", "title"=>"Comparison of population differentiation at the <i>HmYb</i> locus compared to unlinked loci between species and between races of <i>Heliconius</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-02-05 01:33:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/864836"], "description"=>"<p>(A) The <i>HmYb</i> region between <i>H. m. melpomene</i> and <i>H. m. rosina</i> (triangles) and between <i>H. m. aglaope</i> and <i>H. m. amaryllis</i> (circles), (B) The <i>HmYb</i> region between <i>H. pachinus</i> and <i>H. cydno</i>, and (C) the <i>HmB</i> region between <i>H. m. aglaope</i> and <i>H. m. amaryllis</i>. Significance cut-off was calculated using the Bonferroni correction, applied across all 866 SNPs tested.</p>", "links"=>[], "tags"=>["associations", "phenotypic"], "article_id"=>535266, "categories"=>["Evolutionary Biology"], "users"=>["Simon W. Baxter", "Nicola J. Nadeau", "Luana S. Maroja", "Paul Wilkinson", "Brian A. Counterman", "Anna Dawson", "Margarita Beltrán", "Silvia Perez-Espona", "Nicola Chamberlain", "Laura Ferguson", "Richard Clark", "Claire Davidson", "Rebecca Glithero", "James Mallet", "W. Owen McMillan", "Marcus Kronforst", "Mathieu Joron", "Richard H. ffrench-Constant", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000794.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genotype_by_phenotype_associations_across_three_phenotypic_comparisons_/535266", "title"=>"Genotype-by-phenotype associations across three phenotypic comparisons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:27:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/865062"], "description"=>"<p>For the ‘Between wing segments’ experiment, <i>H. melpomene cythera</i> forewings were dissected into P (proximal), B (band) and D (distal) segments of three pupal developmental stages; EP (early pupae), PO (pre-omochrome) and OO (only omochrome). For the “Between Races” experiment, forewings (Fw) and hindwings (Hw) of <i>H. m. malleti</i> (left side) and <i>H. m. cythera</i> (right side), were dissected from Larvae (5<sup>th</sup> instar) and EP (early pupae).</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary biology/animal genetics", "evolutionary biology/bioinformatics", "evolutionary biology/developmental evolution", "evolutionary biology/evolutionary and comparative genetics", "evolutionary biology/genomics", "evolutionary biology/pattern formation"], "article_id"=>535485, "categories"=>["Evolutionary Biology"], "users"=>["Simon W. Baxter", "Nicola J. Nadeau", "Luana S. Maroja", "Paul Wilkinson", "Brian A. Counterman", "Anna Dawson", "Margarita Beltrán", "Silvia Perez-Espona", "Nicola Chamberlain", "Laura Ferguson", "Richard Clark", "Claire Davidson", "Rebecca Glithero", "James Mallet", "W. Owen McMillan", "Marcus Kronforst", "Mathieu Joron", "Richard H. ffrench-Constant", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000794.g005", "stats"=>{"downloads"=>3, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mean_and_standard_error_of_relative_gene_expression_for_Mad_Slu7_Kinesin_and_GPCR_/535485", "title"=>"Mean and standard error of relative gene expression for <i>Mad</i>, <i>Slu7</i>, <i>Kinesin</i>, and <i>GPCR</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:31:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/864703"], "description"=>"<p><i>H.m. rosina</i>, <i>H.m. melpomene</i>, and <i>H.m. amaryllis</i> display the medial red forewing band controlled by a dominant allele at <i>HmB</i>. In addition, <i>H. pachinus</i>, <i>H.m. rosina</i>, and <i>H.m. amaryllis</i> display the yellow hindwing bar controlled by a recessive allele at <i>HmYb</i>.</p>", "links"=>[], "tags"=>["samples"], "article_id"=>535147, "categories"=>["Evolutionary Biology"], "users"=>["Simon W. Baxter", "Nicola J. Nadeau", "Luana S. Maroja", "Paul Wilkinson", "Brian A. Counterman", "Anna Dawson", "Margarita Beltrán", "Silvia Perez-Espona", "Nicola Chamberlain", "Laura Ferguson", "Richard Clark", "Claire Davidson", "Rebecca Glithero", "James Mallet", "W. Owen McMillan", "Marcus Kronforst", "Mathieu Joron", "Richard H. ffrench-Constant", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000794.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Locations_of_field_collected_samples_used_for_population_genetic_analysis_/535147", "title"=>"Locations of field collected samples used for population genetic analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:25:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/429013", "https://ndownloader.figshare.com/files/429024", "https://ndownloader.figshare.com/files/429038", "https://ndownloader.figshare.com/files/429048", "https://ndownloader.figshare.com/files/429066", "https://ndownloader.figshare.com/files/429076", "https://ndownloader.figshare.com/files/429084", "https://ndownloader.figshare.com/files/429096", "https://ndownloader.figshare.com/files/429113", "https://ndownloader.figshare.com/files/429127", "https://ndownloader.figshare.com/files/429131"], "description"=>"<div><p>Wing patterning in <em>Heliconius</em> butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are “hotspots” for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in <em>Heliconius melpomene</em> and relatives. Alleles at <em>HmB</em> control the presence or absence of the red forewing band, while alleles at <em>HmYb</em> control the yellow hindwing bar. Across <em>HmYb</em> two regions, separated by ∼100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at <em>HmB</em> a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both <em>HmYb</em> and <em>HmB</em> there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the <em>HmB</em> locus, the <em>kinesin</em> shows differences in wing disc expression between races that are replicated in the co-mimic, <em>Heliconius erato</em>, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in <em>Heliconius melpomene</em> therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.</p></div>", "links"=>[], "tags"=>["genomic", "hotspots", "genetics", "mimicry", "clade"], "article_id"=>144708, "categories"=>["Evolutionary Biology"], "users"=>["Simon W. Baxter", "Nicola J. Nadeau", "Luana S. Maroja", "Paul Wilkinson", "Brian A. Counterman", "Anna Dawson", "Margarita Beltrán", "Silvia Perez-Espona", "Nicola Chamberlain", "Laura Ferguson", "Richard Clark", "Claire Davidson", "Rebecca Glithero", "James Mallet", "W. Owen McMillan", "Marcus Kronforst", "Mathieu Joron", "Richard H. ffrench-Constant", "Chris D. Jiggins"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000794.s001", "https://dx.doi.org/10.1371/journal.pgen.1000794.s002", "https://dx.doi.org/10.1371/journal.pgen.1000794.s003", "https://dx.doi.org/10.1371/journal.pgen.1000794.s004", "https://dx.doi.org/10.1371/journal.pgen.1000794.s005", "https://dx.doi.org/10.1371/journal.pgen.1000794.s006", "https://dx.doi.org/10.1371/journal.pgen.1000794.s007", "https://dx.doi.org/10.1371/journal.pgen.1000794.s008", "https://dx.doi.org/10.1371/journal.pgen.1000794.s009", "https://dx.doi.org/10.1371/journal.pgen.1000794.s010", "https://dx.doi.org/10.1371/journal.pgen.1000794.s011"], "stats"=>{"downloads"=>24, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Genomic_Hotspots_for_Adaptation_The_Population_Genetics_of_M_llerian_Mimicry_in_the_Heliconius_melpomene_Clade/144708", "title"=>"Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in the <em>Heliconius melpomene</em> Clade", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-02-05 01:18:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/864928"], "description"=>"<p>Pairwise LD between sites across the genomic region is shown as a heatmap, with greyscale indicating estimated r<sup>2</sup> values. Darker colours indicate a stronger correlation between SNP variants at the two sites, across the individuals sampled. The highest LD estimates are all within gene regions, or between closely linked loci. The largest block of LD is across the region with strong genotype-by-phenotype association in the <i>HmB</i> region, across the <i>Slu7</i>, <i>Kinesin</i> and <i>GPCR</i> genes (A, lower left). Comparisons are shown for a) all sites, b) sites associated with phenotype in the <i>HmB</i> locus, and c) sites associated with phenotype in the <i>HmYb</i> locus.</p>", "links"=>[], "tags"=>["disequilibrium"], "article_id"=>535361, "categories"=>["Evolutionary Biology"], "users"=>["Simon W. Baxter", "Nicola J. Nadeau", "Luana S. Maroja", "Paul Wilkinson", "Brian A. Counterman", "Anna Dawson", "Margarita Beltrán", "Silvia Perez-Espona", "Nicola Chamberlain", "Laura Ferguson", "Richard Clark", "Claire Davidson", "Rebecca Glithero", "James Mallet", "W. Owen McMillan", "Marcus Kronforst", "Mathieu Joron", "Richard H. ffrench-Constant", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000794.g004", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Linkage_disequilibrium_LD_for_combined_H_m_aglaope_and_H_m_amaryllis_populations_/535361", "title"=>"Linkage disequilibrium (LD) for combined <i>H. m. aglaope</i> and <i>H. m. amaryllis</i> populations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:29:21"}

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  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"34", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"9", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
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  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"9", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"24", "full-text"=>"16", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"9", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"16", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}

Relative Metric

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