The Eyes Have It: Regulatory and Structural Changes Both Underlie Cichlid Visual Pigment Diversity
Publication Date
December 22, 2009
Journal
PLOS Biology
Authors
Christopher M. Hofmann, Kelly E. O'quin, N. Justin Marshall, Thomas W. Cronin, et al
Volume
7
Issue
12
Pages
e1000266
DOI
https://dx.plos.org/10.1371/journal.pbio.1000266
Publisher URL
http://journals.plos.org/plosbiology/article?id=10.1371%2Fjournal.pbio.1000266
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/20027211
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2790343
Europe PMC
http://europepmc.org/abstract/MED/20027211
Web of Science
000273060500012
Scopus
73949118416
Mendeley
http://www.mendeley.com/research/eyes-it-regulatory-structural-changes-both-underlie-cichlid-visual-pigment-diversity
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Mendeley | Further Information

{"title"=>"The eyes have it: Regulatory and structural changes both underlie cichlid visual pigment diversity", "type"=>"journal", "authors"=>[{"first_name"=>"Christopher M.", "last_name"=>"Hofmann", "scopus_author_id"=>"15052182000"}, {"first_name"=>"Kelly E.", "last_name"=>"O'Quin", "scopus_author_id"=>"36977456400"}, {"first_name"=>"N.", "last_name"=>"Justin Marshall", "scopus_author_id"=>"16156946800"}, {"first_name"=>"Thomas W.", "last_name"=>"Cronin", "scopus_author_id"=>"7102710025"}, {"first_name"=>"Ole", "last_name"=>"Seehausen", "scopus_author_id"=>"7003799773"}, {"first_name"=>"Karen L.", "last_name"=>"Carleton", "scopus_author_id"=>"6603395298"}], "year"=>2009, "source"=>"PLoS Biology", "identifiers"=>{"pui"=>"358096219", "sgr"=>"73949118416", "issn"=>"15449173", "pmid"=>"20027211", "scopus"=>"2-s2.0-73949118416", "doi"=>"10.1371/journal.pbio.1000266", "isbn"=>"1545-7885 (Electronic)\\n1544-9173 (Linking)"}, "id"=>"cb67fe7b-056f-32e0-ae1d-63a25b4ccdbf", "abstract"=>"A major goal of evolutionary biology is to unravel the molecular genetic mechanisms that underlie functional diversification and adaptation. We investigated how changes in gene regulation and coding sequence contribute to sensory diversification in two replicate radiations of cichlid fishes. In the clear waters of Lake Malawi, differential opsin expression generates diverse visual systems, with sensitivities extending from the ultraviolet to the red regions of the spectrum. These sensitivities fall into three distinct clusters and are correlated with foraging habits. In the turbid waters of Lake Victoria, visual sensitivity is constrained to longer wavelengths, and opsin expression is correlated with ambient light. In addition to regulatory changes, we found that the opsins coding for the shortest- and longest-wavelength visual pigments have elevated numbers of potentially functional substitutions. Thus, we present a model of sensory evolution in which both molecular genetic mechanisms work in concert. Changes in gene expression generate large shifts in visual pigment sensitivity across the collective opsin spectral range, but changes in coding sequence appear to fine-tune visual pigment sensitivity at the short- and long-wavelength ends of this range, where differential opsin expression can no longer extend visual pigment sensitivity.", "link"=>"http://www.mendeley.com/research/eyes-it-regulatory-structural-changes-both-underlie-cichlid-visual-pigment-diversity", "reader_count"=>155, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>14, "Librarian"=>1, "Researcher"=>36, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>39, "Student > Postgraduate"=>2, "Other"=>6, "Student > Master"=>17, "Student > Bachelor"=>20, "Professor"=>10}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>14, "Librarian"=>1, "Researcher"=>36, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>39, "Student > Postgraduate"=>2, "Other"=>6, "Student > Master"=>17, "Student > Bachelor"=>20, "Professor"=>10}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>1, "Environmental Science"=>5, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>135, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>1, "Social Sciences"=>1, "Earth and Planetary Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>135}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>5}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>5, "Norway"=>1, "Japan"=>1, "Philippines"=>1, "Brazil"=>2, "United Kingdom"=>1, "France"=>1, "Switzerland"=>1, "Spain"=>2}, "group_count"=>9}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/870957"], "description"=>"<p>(A) Normalized absorbance values of all seven cichlid cone visual pigments. Curves were generated using the λ<sub>max</sub> values from <i>O. niloticus </i><a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000266#pbio.1000266-Spady1\" target=\"_blank\">[29]</a> and the equations of Govardovskii, et al. <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000266#pbio.1000266-Govardovskii1\" target=\"_blank\">[68]</a>. Dotted lines represent opsins that were not expressed in our Lake Victoria cichlid populations. (B) Number of amino acid substitutions in the transmembrane regions (barred) and retinal binding pocket (solid) regions of each opsin class from all species surveyed. (C) Number of substitutions in Lake Malawi. (D) Number of substitutions in Lake Victoria. Only substitutions between residues with different chemical properties are shown.</p>", "links"=>[], "tags"=>["shortest-", "longest-wavelength", "opsins"], "article_id"=>541404, "categories"=>["Evolutionary Biology", "Ecology", "Molecular Biology"], "users"=>["Christopher M. Hofmann", "Kelly E. O'Quin", "N. Justin Marshall", "Thomas W. Cronin", "Ole Seehausen", "Karen L. Carleton"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000266.g006", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_shortest_and_longest_wavelength_opsins_have_the_greatest_sequence_diversity_/541404", "title"=>"The shortest- and longest-wavelength opsins have the greatest sequence diversity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:23:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/870581"], "description"=>"<p>(A) Relative <i>SWS1</i> (ultraviolet) opsin expression is higher among Lake Malawi cichlids foraging on phytoplankton, zooplankton, and epilithic algae (phylogenetic ANOVA). (B) Relative <i>SWS2B</i> opsin expression is positively correlated with the predicted quantum catch that an SWS2B-based visual pigment would have at clear and murky locations in Lake Victoria (phylogenetically independent contrasts [PIC]). See <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000266#pbio.1000266.s002\" target=\"_blank\">Figure S2</a> for the phylogenies used in these comparative analyses.</p>", "links"=>[], "tags"=>["pressures", "opsin"], "article_id"=>541033, "categories"=>["Evolutionary Biology", "Ecology", "Molecular Biology"], "users"=>["Christopher M. Hofmann", "Kelly E. O'Quin", "N. Justin Marshall", "Thomas W. Cronin", "Ole Seehausen", "Karen L. Carleton"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000266.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Selective_pressures_drive_opsin_expression_within_each_lake_/541033", "title"=>"Selective pressures drive opsin expression within each lake.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:17:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/870323"], "description"=>"<p>Triangle plots illustrate the relationships between opsins within the single and double cones of Lake Malawi and Victoria cichlids. Malawian single and double cones vary along two axes, whereas Victorian single and double cones only vary along one. Bar graphs below each plot show expression of the corresponding opsins and emphasize the qualitative differences in expression profiles between lakes. No Lake Victoria taxa express more than trace amounts of <i>SWS1</i> or <i>Rh2B</i> (open bar), and all express high levels of <i>LWS</i> (filled bar). Opsin expression was measured using real-time PCR. Each point or column represents a different taxon (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000266#pbio.1000266.s004\" target=\"_blank\">Table S1</a>). Triangle plots were generated using a freely available Excel worksheet <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000266#pbio.1000266-Graham1\" target=\"_blank\">[74]</a>.</p>", "links"=>[], "tags"=>["ecology/physiological ecology", "Evolutionary biology", "evolutionary biology/evolutionary and comparative genetics", "evolutionary biology/evolutionary ecology", "molecular biology/molecular evolution"], "article_id"=>540771, "categories"=>["Evolutionary Biology", "Ecology", "Molecular Biology"], "users"=>["Christopher M. Hofmann", "Kelly E. O'Quin", "N. Justin Marshall", "Thomas W. Cronin", "Ole Seehausen", "Karen L. Carleton"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000266.g001", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Opsin_gene_expression_from_all_species_surveyed_/540771", "title"=>"Opsin gene expression from all species surveyed.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:12:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/432155", "https://ndownloader.figshare.com/files/432241", "https://ndownloader.figshare.com/files/432300", "https://ndownloader.figshare.com/files/432342", "https://ndownloader.figshare.com/files/432386", "https://ndownloader.figshare.com/files/432432", "https://ndownloader.figshare.com/files/432478", "https://ndownloader.figshare.com/files/432516", "https://ndownloader.figshare.com/files/432564", "https://ndownloader.figshare.com/files/432607", "https://ndownloader.figshare.com/files/432634", "https://ndownloader.figshare.com/files/432670", "https://ndownloader.figshare.com/files/432709"], "description"=>"<div><p>A major goal of evolutionary biology is to unravel the molecular genetic mechanisms that underlie functional diversification and adaptation. We investigated how changes in gene regulation and coding sequence contribute to sensory diversification in two replicate radiations of cichlid fishes. In the clear waters of Lake Malawi, differential opsin expression generates diverse visual systems, with sensitivities extending from the ultraviolet to the red regions of the spectrum. These sensitivities fall into three distinct clusters and are correlated with foraging habits. In the turbid waters of Lake Victoria, visual sensitivity is constrained to longer wavelengths, and opsin expression is correlated with ambient light. In addition to regulatory changes, we found that the opsins coding for the shortest- and longest-wavelength visual pigments have elevated numbers of potentially functional substitutions. Thus, we present a model of sensory evolution in which both molecular genetic mechanisms work in concert. Changes in gene expression generate large shifts in visual pigment sensitivity across the collective opsin spectral range, but changes in coding sequence appear to fine-tune visual pigment sensitivity at the short- and long-wavelength ends of this range, where differential opsin expression can no longer extend visual pigment sensitivity.</p></div>", "links"=>[], "tags"=>["eyes", "changes", "underlie", "cichlid", "pigment"], "article_id"=>145291, "categories"=>["Evolutionary Biology", "Ecology", "Molecular Biology"], "users"=>["Christopher M. Hofmann", "Kelly E. O'Quin", "N. Justin Marshall", "Thomas W. Cronin", "Ole Seehausen", "Karen L. Carleton"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000266.s001", "https://dx.doi.org/10.1371/journal.pbio.1000266.s002", "https://dx.doi.org/10.1371/journal.pbio.1000266.s003", "https://dx.doi.org/10.1371/journal.pbio.1000266.s004", "https://dx.doi.org/10.1371/journal.pbio.1000266.s005", "https://dx.doi.org/10.1371/journal.pbio.1000266.s006", "https://dx.doi.org/10.1371/journal.pbio.1000266.s007", "https://dx.doi.org/10.1371/journal.pbio.1000266.s008", "https://dx.doi.org/10.1371/journal.pbio.1000266.s009", "https://dx.doi.org/10.1371/journal.pbio.1000266.s010", "https://dx.doi.org/10.1371/journal.pbio.1000266.s011", "https://dx.doi.org/10.1371/journal.pbio.1000266.s012", "https://dx.doi.org/10.1371/journal.pbio.1000266.s013"], "stats"=>{"downloads"=>79, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Eyes_Have_It_Regulatory_and_Structural_Changes_Both_Underlie_Cichlid_Visual_Pigment_Diversity/145291", "title"=>"The Eyes Have It: Regulatory and Structural Changes Both Underlie Cichlid Visual Pigment Diversity", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-12-22 01:28:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/870694"], "description"=>"<p>(A) Relative irradiance at 2 m depth at three locations in Lake Victoria (Makobe Island, Python Island, and Luanso Island). (B) In Lake Victoria, estimated quantum catches are predicted to vary over several orders of magnitude, both across visual pigments and geographic locations.</p>", "links"=>[], "tags"=>["pigment"], "article_id"=>541148, "categories"=>["Evolutionary Biology", "Ecology", "Molecular Biology"], "users"=>["Christopher M. Hofmann", "Kelly E. O'Quin", "N. Justin Marshall", "Thomas W. Cronin", "Ole Seehausen", "Karen L. Carleton"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000266.g004", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Visual_pigment_performance_in_Lake_Victoria_/541148", "title"=>"Visual pigment performance in Lake Victoria.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:19:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/870801"], "description"=>"<p>(A) Relative irradiance at 2 m depth at two locations in Lake Malawi (Thumbi West Island and Zimbawe Rock). (B) In Lake Malawi, all visual pigments would have relatively similar, high quantum catches at both locations.</p>", "links"=>[], "tags"=>["pigment"], "article_id"=>541253, "categories"=>["Evolutionary Biology", "Ecology", "Molecular Biology"], "users"=>["Christopher M. Hofmann", "Kelly E. O'Quin", "N. Justin Marshall", "Thomas W. Cronin", "Ole Seehausen", "Karen L. Carleton"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000266.g005", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Visual_pigment_performance_in_Lake_Malawi_/541253", "title"=>"Visual pigment performance in Lake Malawi.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:20:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/870452"], "description"=>"<p>(A) Hierarchical clustering of species' opsin expression profiles revealed three clusters. S, short wavelength; M, medium wavelength; L, long wavelength. (B) Estimates of Lake Malawi single- and double-cone sensitivities suggest that these three clusters correspond to visual palettes sensitive to short-, medium-, and long-wavelength portions of the cichlid visible light spectrum. Species from the mbuna clade are shown in blue, non-mbuna are shown in green. Lake Victoria cichlids (red) all fall within the longest-wavelength Malawian cluster. Single- and double-cone λ<sub>max</sub> values were estimated by weighting the peak absorbance of each opsin by its relative expression level.</p>", "links"=>[], "tags"=>["profiles", "single-", "double-cone", "sensitivities"], "article_id"=>540897, "categories"=>["Evolutionary Biology", "Ecology", "Molecular Biology"], "users"=>["Christopher M. Hofmann", "Kelly E. O'Quin", "N. Justin Marshall", "Thomas W. Cronin", "Ole Seehausen", "Karen L. Carleton"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000266.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_expression_profiles_and_single_and_double_cone_sensitivities_form_three_clusters_/540897", "title"=>"Gene expression profiles and single- and double-cone sensitivities form three clusters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:14:57"}

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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
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  • {"unique-ip"=>"2", "full-text"=>"0", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"5"}
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  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"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"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"23", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"1", "full-text"=>"0", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
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  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"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"=>"5"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"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"=>"2017", "month"=>"7"}
  • {"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"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"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"=>"11"}
  • {"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"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"13", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
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  • {"unique-ip"=>"7", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"4", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
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Relative Metric

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