The Rise and Fall of an Evolutionary Innovation: Contrasting Strategies of Venom Evolution in Ancient and Young Animals
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{"title"=>"The Rise and Fall of an Evolutionary Innovation: Contrasting Strategies of Venom Evolution in Ancient and Young Animals", "type"=>"journal", "authors"=>[{"first_name"=>"Kartik", "last_name"=>"Sunagar", "scopus_author_id"=>"35273686900"}, {"first_name"=>"Yehu", "last_name"=>"Moran", "scopus_author_id"=>"14045793600"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"606841531", "sgr"=>"84946592944", "scopus"=>"2-s2.0-84946592944", "issn"=>"15537404", "isbn"=>"1553-7404", "doi"=>"10.1371/journal.pgen.1005596", "pmid"=>"26492532"}, "id"=>"29e6e6f5-4e8b-3235-917d-cc71e23feb22", "abstract"=>"Animal venoms are theorized to evolve under the significant influence of positive Darwinian selection in a chemical arms race scenario, where the evolution of venom resistance in prey and the invention of potent venom in the secreting animal exert reciprocal selection pressures. Venom research to date has mainly focused on evolutionarily younger lineages, such as snakes and cone snails, while mostly neglecting ancient clades (e.g., cnidarians, coleoids, spiders and centipedes). By examining genome, venom-gland transcriptome and sequences from the public repositories, we report the molecular evolutionary regimes of several centipede and spider toxin families, which surprisingly accumulated low-levels of sequence variations, despite their long evolutionary histories. Molecular evolutionary assessment of over 3500 nucleotide sequences from 85 toxin families spanning the breadth of the animal kingdom has unraveled a contrasting evolutionary strategy employed by ancient and evolutionarily young clades. We show that the venoms of ancient lineages remarkably evolve under the heavy constraints of negative selection, while toxin families in lineages that originated relatively recently rapidly diversify under the influence of positive selection. We propose that animal venoms mostly employ a 'two-speed' mode of evolution, where the major influence of diversifying selection accompanies the earlier stages of ecological specialization (e.g., diet and range expansion) in the evolutionary history of the species-the period of expansion, resulting in the rapid diversification of the venom arsenal, followed by longer periods of purifying selection that preserve the potent toxin pharmacopeia-the period of purification and fixation. However, species in the period of purification may re-enter the period of expansion upon experiencing a major shift in ecology or environment. Thus, we highlight for the first time the significant roles of purifying and episodic selections in shaping animal venoms.", "link"=>"http://www.mendeley.com/research/rise-fall-evolutionary-innovation-contrasting-strategies-venom-evolution-ancient-young-animals", "reader_count"=>54, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>12, "Student > Bachelor"=>9, "Professor"=>5}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>12, "Student > Bachelor"=>9, "Professor"=>5}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>42, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Chemistry"=>2, "Immunology and Microbiology"=>2, "Economics, Econometrics and Finance"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>42}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"Turkey"=>1, "United States"=>4, "Brazil"=>2}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2369445"], "description"=>"<p><b>a:</b> Fast Unconstrained Bayesian AppRoximation</p><p><b>b:</b> Sites detected as experiencing episodic diversifying selection (0.05 significance) by the Mixed Effects Model Evolution (MEME)</p><p><b>c:</b> Positively selected sites detected by the Bayes Empirical Bayes approach implemented in M8. Sites detected at 0.99 and 0.95 significance are indicated in the parenthesis</p><p><b>d:</b> number of sites under pervasive diversifying selection at the posterior probability ≥0.9 (FUBAR)</p><p><b>e:</b> Number of sites under pervasive purifying selection at the posterior probability ≥0.9 (FUBAR)</p><p><b>ω:</b> mean dN/dS</p><p>Molecular evolution of centipede novel putative toxin families.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582942, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.t003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_centipede_novel_putative_toxin_families_/1582942", "title"=>"Molecular evolution of centipede novel putative toxin families.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369442"], "description"=>"<p>Divergence times of lineages examined in this study (labels indicated in red) have been indicated. Pie charts depict the proportion of synonymous (dS), non-synonymous (dN) mutations and the number of significantly detected positively selected sites (#PS) in the venom-encoding genes of the respective lineage. Depicted phylogenetic relationships are based on Ref. [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005596#pgen.1005596.ref013\" target=\"_blank\">13</a>].</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582939, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_tree_of_life_depicts_the_evolution_of_venom_in_animals_where_blue_red_and_orange_colored_lines_represent_lineages_that_utilize_venom_for_defense_predation_or_intraspecific_needs_respectively_/1582939", "title"=>"Schematic tree of life depicts the evolution of venom in animals, where blue, red and orange colored lines represent lineages that utilize venom for defense, predation or intraspecific needs, respectively.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369436"], "description"=>"<p>A plot of site-specific ω against amino acid positions for various coleoid toxin types is presented. The red horizontal line represents the line of neutrality: points above and below this line indicate positive and negative selection, respectively. Bar plot color codes: 1) Serine Protease; 2) PLA<sub>2</sub>; 3) Pacifestin and 4) CAP.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582933, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_venom_in_coleoids_/1582933", "title"=>"Molecular evolution of venom in coleoids.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369449", "https://ndownloader.figshare.com/files/2369450", "https://ndownloader.figshare.com/files/2369451", "https://ndownloader.figshare.com/files/2369452", "https://ndownloader.figshare.com/files/2369453", "https://ndownloader.figshare.com/files/2369454"], "description"=>"<div><p>Animal venoms are theorized to evolve under the significant influence of positive Darwinian selection in a chemical arms race scenario, where the evolution of venom resistance in prey and the invention of potent venom in the secreting animal exert reciprocal selection pressures. Venom research to date has mainly focused on evolutionarily younger lineages, such as snakes and cone snails, while mostly neglecting ancient clades (e.g., cnidarians, coleoids, spiders and centipedes). By examining genome, venom-gland transcriptome and sequences from the public repositories, we report the molecular evolutionary regimes of several centipede and spider toxin families, which surprisingly accumulated low-levels of sequence variations, despite their long evolutionary histories. Molecular evolutionary assessment of over 3500 nucleotide sequences from 85 toxin families spanning the breadth of the animal kingdom has unraveled a contrasting evolutionary strategy employed by ancient and evolutionarily young clades. We show that the venoms of ancient lineages remarkably evolve under the heavy constraints of negative selection, while toxin families in lineages that originated relatively recently rapidly diversify under the influence of positive selection. We propose that animal venoms mostly employ a ‘two-speed’ mode of evolution, where the major influence of diversifying selection accompanies the earlier stages of ecological specialization (e.g., diet and range expansion) in the evolutionary history of the species–the period of expansion, resulting in the rapid diversification of the venom arsenal, followed by longer periods of purifying selection that preserve the potent toxin pharmacopeia–the period of purification and fixation. However, species in the period of purification may re-enter the period of expansion upon experiencing a major shift in ecology or environment. Thus, we highlight for the first time the significant roles of purifying and episodic selections in shaping animal venoms.</p></div>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582946, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1005596.s001", "https://dx.doi.org/10.1371/journal.pgen.1005596.s002", "https://dx.doi.org/10.1371/journal.pgen.1005596.s003", "https://dx.doi.org/10.1371/journal.pgen.1005596.s004", "https://dx.doi.org/10.1371/journal.pgen.1005596.s005", "https://dx.doi.org/10.1371/journal.pgen.1005596.s006"], "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Rise_and_Fall_of_an_Evolutionary_Innovation_Contrasting_Strategies_of_Venom_Evolution_in_Ancient_and_Young_Animals_/1582946", "title"=>"The Rise and Fall of an Evolutionary Innovation: Contrasting Strategies of Venom Evolution in Ancient and Young Animals", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369431"], "description"=>"<p>A plot of site-specific ω against amino acid positions for various centipede and spider venom-encoding genes is presented in panel A and B, respectively. Significantly detected positively selected sites (model 8; Bayes Empirical Bayes approach) are presented as large red circles. The red horizontal line represents the line of neutrality: points above and below this line indicate positive and negative selection, respectively. A corresponding bar plot is provided, which shows the computed ω value for the respective toxin class. Bar plot color code: <b>Panel A</b> 1) Novel family (NF) 8; 2) NF 6; 3) NF 4; 4) NF 1; 5) β-PFT; 6) CAP; 7) LDLA; 8) SLPTX 1; 9) SLPTX 4; 10) SLPTX 5; 11) SLPTX 10; 12) SLPTX 11; 13) SLPTX 12; 14) SLPTX 13; 15) SLPTX 15; 16) SLPTX 16; 17) SLPTX 17; <b>Panel B</b> 1) lycotoxins; 2) latrotoxins; 3) magi-1 family; 4) Kunitz toxins; 5) Sphingomyelinase D; 6) Huwentoxin-1 family; 7) κ/ω-hexatoxins; 8) κ-hexatoxins; 9) ω-hexatoxins; 10) Superfamily E ICKs.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582928, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_venom_in_centipedes_A_and_spiders_B_/1582928", "title"=>"Molecular evolution of venom in centipedes (A) and spiders (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369444"], "description"=>"<p><b>a:</b> Fast Unconstrained Bayesian AppRoximation</p><p><b>b:</b> Sites detected as experiencing episodic diversifying selection (0.05 significance) by the Mixed Effects Model Evolution (MEME)</p><p><b>c:</b> Positively selected sites detected by the Bayes Empirical Bayes approach implemented in M8. Sites detected at 0.99 and 0.95 significance are indicated in the parenthesis</p><p><b>d:</b> number of sites under pervasive diversifying selection at the posterior probability ≥0.9 (FUBAR)</p><p><b>e:</b> Number of sites under pervasive purifying selection at the posterior probability ≥0.9 (FUBAR)</p><p><b>ω:</b> mean dN/dS</p><p>Molecular evolution of scoloptoxins.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582941, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_scoloptoxins_/1582941", "title"=>"Molecular evolution of scoloptoxins.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369429"], "description"=>"<p>Sequence alignments of widely separated sea anemone and scorpion neurotoxins are depicted. Sampled locations of these toxins are indicated on the map. Identical positions in sequence alignments are shown in blue, while differing amino acids are shown in brown. Uniprot IDs of sequences are: 1) B1NWR0; 2) P01532; 3) P0C5F4; 4) P29187; 5) E2S062; 6) Q7YXD3; 7) D5HR48; 8) P01484 and 9) D5HR56.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582926, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Remarkable_sequence_conservation_in_distantly_related_toxins_/1582926", "title"=>"Remarkable sequence conservation in distantly related toxins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369443"], "description"=>"<p><b>a:</b> Fast Unconstrained Bayesian AppRoximation</p><p><b>b:</b> Sites detected as experiencing episodic diversifying selection (0.05 significance) by the Mixed Effects Model Evolution (MEME)</p><p><b>c:</b> Positively selected sites detected by the Bayes Empirical Bayes approach implemented in M8. Sites detected at 0.99 and 0.95 significance are indicated in the parenthesis</p><p><b>d:</b> number of sites under pervasive diversifying selection at the posterior probability ≥0.9 (FUBAR)</p><p><b>e:</b> Number of sites under pervasive purifying selection at the posterior probability ≥0.9 (FUBAR)</p><p><b>ω:</b> mean dN/dS</p><p>Molecular evolution of centipede PFT, CAP and LDLA venom proteins.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582940, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.t001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_centipede_PFT_CAP_and_LDLA_venom_proteins_/1582940", "title"=>"Molecular evolution of centipede PFT, CAP and LDLA venom proteins.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369438"], "description"=>"<p>A plot of site-specific ω against amino acid positions for various advanced snake and cone snail venom-encoding genes is presented. Significantly detected positively selected sites (model 8; Bayes Empirical Bayes approach) are presented as large red circles. The red horizontal line represents the line of neutrality: points above and below this line indicate positive and negative selection, respectively. A corresponding bar plot is provided, which shows the computed ω value for the respective toxin class. Bar-plot color code: <b>Panel A</b> 1) β-defensins; 2) Cytotoxins; 3) PII-Disintegrins; 4) Group I PLA<sub>2</sub>s; 5) Group II PLA<sub>2</sub>s; 6) Kallikreins; 7) <i>Psammophis</i> SVMPs; 8) Advanced snake SVMPs; 9) Serine Proteases; 10) Lectins; 11) κ-3FTxs; 12) Type III α-neurotoxins; 13) Type II α-neurotoxins; Type I α-neurotoxins; and 14) CRISPs. <b>Panel B</b><i>Conus marmoreus</i>—> 1) Superfamily M; 2) Superfamily I2; 3) Superfamily T; 4) Superfamily O2; <i>C</i>. <i>geographus</i>—> 5) Superfamily O1; 6) Superfamily O2; 7) Superfamily O1; 8) Superfamily M; 9) Superfamily A; 10) Conkunitzin; 11) Conantokin; 12) Con-ikot-ikot.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582935, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_venom_in_advanced_snakes_A_and_cone_snails_B_/1582935", "title"=>"Molecular evolution of venom in advanced snakes (A) and cone snails (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369434"], "description"=>"<p>A plot of site-specific ω against amino acid positions for various cnidarian and scorpion venom-encoding genes is presented in panel A and B, respectively. Significantly detected positively selected sites (model 8; Bayes Empirical Bayes approach) are presented as large red circles. The red horizontal line represents the line of neutrality: points above and below this line indicate positive and negative selection, respectively. A corresponding bar plot is provided, which shows the computed ω value for the respective toxin class. Bar-plot color code: <b>Panel A</b> 1) SCRiPs; 2) JFTs; 3) Hydralysins; 4) Aerolysin-related toxins in sea anemone; 5) Actinoporins; 6) KTx Type 1; 7) KTx Type 3; 8) NaTx; <b>Panel B</b> 1) Short KTx; 2) Long KTx; 3) Chloride; 4) β-NaTx; 5) α-NaTx; 6) ICK; 7) DDH; 8) Glycine-rich toxins; 9) Bradykinin Potentiating Peptides; 10) Anionic; 11) Antimicrobial peptide toxins.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582931, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_venom_in_cnidarians_A_and_scorpions_B_/1582931", "title"=>"Molecular evolution of venom in cnidarians (A) and scorpions (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-22 02:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/2369433"], "description"=>"<p>A plot of site-specific ω against amino acid positions for various Toxicofera lizard toxin types is presented. The red horizontal line represents the line of neutrality: points above and below this line indicate positive and negative selection, respectively. Bar plot color codes: 1) Phospholipase A2; 2) Nerve Growth Factors; 3) Natriuretic peptides and 4) CRiSPs; 5) Kallikreins; and 6) crotamines.</p>", "links"=>[], "tags"=>["animal venoms", "Young Animals Animal venoms", "chemical arms race scenario", "lineage", "spider toxin families", "influence", "85 toxin families", "3500 nucleotide sequences"], "article_id"=>1582930, "categories"=>["Uncategorised"], "users"=>["Kartik Sunagar", "Yehu Moran"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005596.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_evolution_of_venom_in_Toxicofera_lizards_/1582930", "title"=>"Molecular evolution of venom in Toxicofera lizards.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-22 02:57:28"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"26", "full-text"=>"14", "pdf"=>"18", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"16", "full-text"=>"14", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"19", "full-text"=>"11", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
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  • {"unique-ip"=>"14", "full-text"=>"10", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"17", "full-text"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"15", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"10", "full-text"=>"12", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"15", "full-text"=>"10", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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