MHC Adaptive Divergence between Closely Related and Sympatric African Cichlids
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{"title"=>"MHC adaptive divergence between closely related and sympatric African cichlids", "type"=>"journal", "authors"=>[{"first_name"=>"Jonatan", "last_name"=>"Blais", "scopus_author_id"=>"14828756000"}, {"first_name"=>"Ciro", "last_name"=>"Rico", "scopus_author_id"=>"56269496600"}, {"first_name"=>"Cock", "last_name"=>"van Oosterhout", "scopus_author_id"=>"6603278930"}, {"first_name"=>"Joanne", "last_name"=>"Cable", "scopus_author_id"=>"7005219307"}, {"first_name"=>"George F.", "last_name"=>"Turner", "scopus_author_id"=>"7401708788"}, {"first_name"=>"Louis", "last_name"=>"Bernatchez", "scopus_author_id"=>"7005123164"}], "year"=>2007, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-40349108566", "pui"=>"351338878", "doi"=>"10.1371/journal.pone.0000734", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"40349108566", "pmid"=>"17710134"}, "id"=>"2952a1c7-7572-3411-b6b5-c6041d753e33", "abstract"=>"BACKGROUND: The haplochromine cichlid species assemblages of Lake Malawi and Victoria represent some of the most important study systems in evolutionary biology. Identifying adaptive divergence between closely-related species can provide important insights into the processes that may have contributed to these spectacular radiations. Here, we studied a pair of sympatric Lake Malawi species, Pseudotropheus fainzilberi and P. emmiltos, whose reproductive isolation depends on olfactory communication. We tested the hypothesis that these species have undergone divergent selection at MHC class II genes, which are known to contribute to olfactory-based mate choice in other taxa.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Divergent selection on functional alleles was inferred from the higher genetic divergence at putative antigen binding sites (ABS) amino acid sequences than at putatively neutrally evolving sites at intron 1, exon 2 synonymous sequences and exon 2 amino acid residues outside the putative ABS. In addition, sympatric populations of these fish species differed significantly in communities of eukaryotic parasites.\\n\\nCONCLUSIONS/SIGNIFICANCE: We propose that local host-parasite coevolutionary dynamics may have driven adaptive divergence in MHC alleles, influencing odor-mediated mate choice and leading to reproductive isolation. These results provide the first evidence for a novel mechanism of adaptive speciation and the first evidence of adaptive divergence at the MHC in closely related African cichlid fishes.", "link"=>"http://www.mendeley.com/research/mhc-adaptive-divergence-between-closely-related-sympatric-african-cichlids", "reader_count"=>134, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>8, "Researcher"=>41, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>42, "Student > Postgraduate"=>3, "Student > Master"=>17, "Other"=>5, "Student > Bachelor"=>6, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>8, "Researcher"=>41, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>42, "Student > Postgraduate"=>3, "Student > Master"=>17, "Other"=>5, "Student > Bachelor"=>6, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>9, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>107, "Medicine and Dentistry"=>1, "Philosophy"=>1, "Chemical Engineering"=>1, "Computer Science"=>2, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>107}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>9}, "Chemical Engineering"=>{"Chemical Engineering"=>1}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Czech Republic"=>1, "Japan"=>1, "Finland"=>1, "Egypt"=>1, "Brazil"=>1, "United Kingdom"=>4, "Australia"=>1, "Switzerland"=>1, "Germany"=>3}, "group_count"=>8}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/465886", "https://ndownloader.figshare.com/files/465903", "https://ndownloader.figshare.com/files/465922", "https://ndownloader.figshare.com/files/465939", "https://ndownloader.figshare.com/files/466145", "https://ndownloader.figshare.com/files/466407", "https://ndownloader.figshare.com/files/466455", "https://ndownloader.figshare.com/files/466512"], "description"=>"<div><h3>Background</h3><p>The haplochromine cichlid species assemblages of Lake Malawi and Victoria represent some of the most important study systems in evolutionary biology. Identifying adaptive divergence between closely-related species can provide important insights into the processes that may have contributed to these spectacular radiations. Here, we studied a pair of sympatric Lake Malawi species, <em>Pseudotropheus fainzilberi</em> and <em>P. emmiltos</em>, whose reproductive isolation depends on olfactory communication. We tested the hypothesis that these species have undergone divergent selection at MHC class II genes, which are known to contribute to olfactory-based mate choice in other taxa.</p><h3>Methodology/Principal Findings</h3><p>Divergent selection on functional alleles was inferred from the higher genetic divergence at putative antigen binding sites (ABS) amino acid sequences than at putatively neutrally evolving sites at intron 1, exon 2 synonymous sequences and exon 2 amino acid residues outside the putative ABS. In addition, sympatric populations of these fish species differed significantly in communities of eukaryotic parasites.</p><h3>Conclusions/Significance</h3><p>We propose that local host-parasite coevolutionary dynamics may have driven adaptive divergence in MHC alleles, influencing odor-mediated mate choice and leading to reproductive isolation. These results provide the first evidence for a novel mechanism of adaptive speciation and the first evidence of adaptive divergence at the MHC in closely related African cichlid fishes.</p></div>", "links"=>[], "tags"=>["mhc", "adaptive", "divergence", "sympatric", "african", "cichlids"], "article_id"=>151840, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Cancer"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.s001", "https://dx.doi.org/10.1371/journal.pone.0000734.s002", "https://dx.doi.org/10.1371/journal.pone.0000734.s003", "https://dx.doi.org/10.1371/journal.pone.0000734.s004", "https://dx.doi.org/10.1371/journal.pone.0000734.s005", "https://dx.doi.org/10.1371/journal.pone.0000734.s006", "https://dx.doi.org/10.1371/journal.pone.0000734.s007", "https://dx.doi.org/10.1371/journal.pone.0000734.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/MHC_Adaptive_Divergence_between_Closely_Related_and_Sympatric_African_Cichlids/151840", "title"=>"MHC Adaptive Divergence between Closely Related and Sympatric African Cichlids", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2007-08-15 00:30:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/947239"], "description"=>"<p>Individuals of a) <i>Pseudotropheus fainzilberi</i> and b) <i>P. emmiltos</i> were collected at Mpanga Rocks, Luwino Reef, and Chirwa Island off the North Western shore of Lake Malawi. The two species are sympatric at Mpanga Rocks and Luwino Reef. Photograhs show males in full nuptial dress and are courtesy of Ad Konings.</p>", "links"=>[], "tags"=>["Evolutionary biology", "computational biology/comparative sequence analysis", "computational biology/population genetics", "computational biology/protein structure prediction", "ecology/community ecology and biodiversity", "evolutionary biology/bioinformatics", "evolutionary biology/evolutionary ecology", "evolutionary biology/sexual behavior", "immunology/antigen processing and recognition", "immunology/genetics of the immune system"], "article_id"=>617568, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sampling_Locations_/617568", "title"=>"Sampling Locations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-15 02:06:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/947312"], "description"=>"<p>The tertiary structure prediction was based on Psemmil_m58_c exon 2 sequence (Accession number: EF540049) of 41% homology with mouse MHC sequence gi|13399459 in the Protein Data Bank (<a href=\"http://www.pdb.org/pdb/home/home.do\" target=\"_blank\">http://www.pdb.org/pdb/home/home.do</a>) using the 3D-jigsaw server v.2.0 (<a href=\"http://www.bmm.icnet.uk/~3djigsaw/\" target=\"_blank\">http://www.bmm.icnet.uk/~3djigsaw/</a>). The graphical representation was created using the program Pymol v.0.99. Amino acid residues under significant positive selection in <i>Pseudotropheus fainzilberi</i> and <i>P. emmiltos</i> and corresponding to peptide binding sites in humans are highlighted in orange. Residues shown in red were under significant positive selection in <i>P. fainzilberi</i> and <i>P. emmiltos</i> but do not correspond with peptide binding sites in humans. Residues in yellow are human peptide binding sites that were not found to evolve under positive selection in cichlids. The 84 amplified exon 2 codons are numbered 1-84 on the graph. Those correspond to codons 6-89 of the mature protein.</p>", "links"=>[], "tags"=>["cichlid", "mhc"], "article_id"=>617661, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Three_Dimensional_Model_of_the_1_Domain_of_Cichlid_MHC_Class_II_/617661", "title"=>"Three-Dimensional Model of the β<sub>1</sub> Domain of Cichlid MHC Class II.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-15 02:07:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/947382"], "description"=>"<p>Structure predictions were obtained from the PSIPRED server (<a href=\"http://bioinf.cs.ucl.ac.uk/psipred/psiform.html\" target=\"_blank\">http://bioinf.cs.ucl.ac.uk/psipred/psiform.html</a>) for a) mouse sequence gi:13399459 and b) cichlid sequence Psemmil_m58_c (Accession number: EF540049). Mammalian and fish secondary structures are similar except for an additional short alpha-helix at position 46–49 predicted for the mouse sequence, and an additional short strand at position 74 predicted for the cichlid sequence.</p>", "links"=>[], "tags"=>["cichlid", "mhc", "ii", "exon"], "article_id"=>617714, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_Secondary_Structure_of_Mouse_and_Cichlid_MHC_Class_II_Exon_2_/617714", "title"=>"Comparison of Secondary Structure of Mouse and Cichlid MHC Class II Exon 2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-15 02:08:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/947484"], "description"=>"<p>Fst values (HudSon et al. 1992) from pairwise comparisons of conspecific allopatric populations (Mpanga Rocks (Mpg), Luwino Reef (Lwo), and Chirwa Island (Chw)) and between heterospecific sympatric populations of <i>P. fainzilberi</i> (fainz.), and <i>P. emmiltos</i> (emm.). Neutral Fst estimates were obtained from intron 1 p-distances, modified Nei and Gojobori synonymous distances at exon 2, and from amino acid EX distance at exon 2 sites outside the putative ABS region (dN/dS≤1) and functional Fst were obtained from EX distance at putative exon 2 ABS (dN/dS>1). Negative Fst estimates were forced to zero. Evidence of significant genetic divergence between pairs of allopatric populations was found only for neutral Fst estimates between <i>P. emmiltos</i> populations from Luwino Reef and Mpanga Rocks. Evidence of significant genetic divergence between pairs of <i>P. fainzilberi</i> and <i>P. emmiltos</i> sympatric populations was found only at putative ABS at Mpanga Rocks. <sup>*</sup>Significantly different from zero (p<0.05; 200 permutations)</p>", "links"=>[], "tags"=>["divergence", "heterospecific", "sympatric", "populations", "conspecific", "allopatric"], "article_id"=>617810, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_Genetic_Divergence_Between_Heterospecific_Sympatric_Populations_and_Conspecific_Allopatric_Populations_/617810", "title"=>"Comparison of Genetic Divergence Between Heterospecific Sympatric Populations and Conspecific Allopatric Populations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-08-15 02:10:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/947563"], "description"=>"<p>95% confidence intervals for the coefficients of the model (Coeff. 95% CI) are the 5% and 95% bias corrected and accelerated (BCa) percentiles of 1000 bootstrap replicates of the original data. Significant effects correspond to CI excluding zero and are marked in bold.</p>", "links"=>[], "tags"=>["squares", "degrees", "multivariate", "linear", "variance", "incidence", "prevalence", "16", "types"], "article_id"=>617857, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.t004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sum_of_squares_SS_and_degrees_of_freedom_df_of_a_multivariate_general_linear_model_testing_the_effect_of_host_species_collection_site_host_sex_and_host_standard_length_on_four_principal_component_analysis_factors_PC1_PC4_representing_84_of_the_original_v/617857", "title"=>"Sum of squares (SS) and degrees of freedom (df) of a multivariate general linear model testing the effect of host species, collection site, host sex, and host standard length on four principal component analysis factors (PC1-PC4) representing 84% of the original variance of the incidence and prevalence of 16 different types of parasites.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2007-08-15 02:10:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/947613"], "description"=>"<p>Distinctiveness scores <i>Dc</i> between intron 1 alleles and the whole sequence of exon 2 amino acid alleles (Exon 2), between intron 1 alleles and positively selected putative ABS amino acid sequences (dN/dS>1), and between intron 1 alleles and exon 2 amino acid alleles outside the putative ABS region (dN/dS≤1), were compared using Mann-Whitney <i>U</i> tests. Significant p-values (α = 0.05) are in bold.</p>", "links"=>[], "tags"=>["alleles", "mhc", "ii", "intron", "exon", "amino"], "article_id"=>617944, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proportions_of_private_and_shared_alleles_between_Pseudotropheus_fainzilberi_and_P_emmiltos_at_MHC_class_II_B_intron_1_alleles_and_exon_2_amino_acid_alleles_/617944", "title"=>"Proportions of private and shared alleles between <i>Pseudotropheus fainzilberi</i> and <i>P. emmiltos</i> at MHC class II B intron 1 alleles and exon 2 amino acid alleles.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2007-08-15 02:12:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/947659"], "description"=>"<p>Parasite infections of <i>Pseudotropheus emmiltos</i> and <i>P. fainzilberi</i>: eigenvectors of the first four factors explaining 84% of the original variance returned from a principal component analysis on incidence and abundance of 16 types of parasites transformed according to equation 12 in Legendre and Gallagher <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000734#pone.0000734-Legendre1\" target=\"_blank\">[38]</a>.</p>", "links"=>[], "tags"=>["infections", "eigenvectors", "explaining", "variance", "returned", "incidence", "abundance", "16", "types", "parasites", "transformed", "12", "legendre", "gallagher"], "article_id"=>617971, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Parasite_infections_of_Pseudotropheus_emmiltos_and_P_fainzilberi_eigenvectors_of_the_first_four_factors_explaining_84_of_the_original_variance_returned_from_a_principal_component_analysis_on_incidence_and_abundance_of_16_types_of_parasites_transformed_ac/617971", "title"=>"Parasite infections of <i>Pseudotropheus emmiltos</i> and <i>P. fainzilberi</i>: eigenvectors of the first four factors explaining 84% of the original variance returned from a principal component analysis on incidence and abundance of 16 types of parasites transformed according to equation 12 in Legendre and Gallagher [38].", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2007-08-15 02:12:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/947700"], "description"=>"<p>Neutral Fst values were calculated from intron 1, exon 2 synonymous alleles (exon 2 dS) and the 65 exon 2 amino acid sites evolving under a mixture of purifying and nearly neutral evolution (dN/dS≤1 sites). Functional Fst estimate was obtained from the 19 amino acid exon 2 putative ABS (dN/dS>1 sites). Association indices (AI) were obtained for intron 1 and for exon 2 phylogenies from neighbor-joining trees using Kimura 2-parameters distances and a <i>Salmo salar</i> outgroup sequence (gi:57335063) in the HYPHY package. AI values reflect the level of phylogenetic compartmentalization and correspond to the mean ratio of the sum over all nodes of the association values <i>d = (1-f)/2<sup>n−1</sup></i> from 100 bootstrapped tree of the test sequences on species-reassigned control. Lower values reflect higher divergence of samples.</p>1<p>(Hudson et al. 1992); <sup>2</sup> (Wang et al. 2001); †significantly different from zero (p<0.01) from 200 permutations; <sup>††</sup>significantly different from zero (p = 0.015) from 200 permutations; ‡significantly different from zero (P<0.01) from 100 bootstrap tree replicates; * <i>dS</i> calculated using the modified Nei and Gojobori method with transition/transversion = 1.26 estimated from the data; ** Experimental exchangeability distance (EX) for amino acid <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000734#pone.0000734-Yampolsky1\" target=\"_blank\">[81]</a> estimated by maximum likelihood.</p>", "links"=>[], "tags"=>["differentiation", "estimates"], "article_id"=>618029, "categories"=>["Evolutionary Biology", "Medicine", "Ecology", "Immunology", "Infectious Diseases"], "users"=>["Jonatan Blais", "Ciro Rico", "Cock van Oosterhout", "Joanne Cable", "George F. Turner", "Louis Bernatchez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0000734.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neutral_and_functional_genetic_differentiation_estimates_between_Pseudotropheus_fainzilberi_and_P_emmiltos_samples_/618029", "title"=>"Neutral and functional genetic differentiation estimates between <i>Pseudotropheus fainzilberi</i> and <i>P. emmiltos</i> samples.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2007-08-15 02:13:49"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"11", "full-text"=>"21", "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"=>"5", "full-text"=>"6", "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"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"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"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"5", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"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"=>"2"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"7", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
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  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"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"=>"12"}
  • {"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"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
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  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "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"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"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"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"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"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"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"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"23", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"22", "full-text"=>"15", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"16", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
  • {"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"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
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Relative Metric

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