Phylogenetic and Transcriptomic Analysis of Chemosensory Receptors in a Pair of Divergent Ant Species Reveals Sex-Specific Signatures of Odor Coding
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{"title"=>"Phylogenetic and Transcriptomic Analysis of Chemosensory Receptors in a Pair of Divergent Ant Species Reveals Sex-Specific Signatures of Odor Coding", "type"=>"journal", "authors"=>[{"first_name"=>"Xiaofan", "last_name"=>"Zhou", "scopus_author_id"=>"55706858800"}, {"first_name"=>"Jesse D.", "last_name"=>"Slone", "scopus_author_id"=>"15058510300"}, {"first_name"=>"Antonis", "last_name"=>"Rokas", "scopus_author_id"=>"6701584095"}, {"first_name"=>"Shelley L.", "last_name"=>"Berger", "scopus_author_id"=>"7401518995"}, {"first_name"=>"Jürgen", "last_name"=>"Liebig", "scopus_author_id"=>"6701683172"}, {"first_name"=>"Anandasankar", "last_name"=>"Ray", "scopus_author_id"=>"15833172900"}, {"first_name"=>"Danny", "last_name"=>"Reinberg", "scopus_author_id"=>"7005185878"}, {"first_name"=>"Laurence J.", "last_name"=>"Zwiebel", "scopus_author_id"=>"6701730185"}], "year"=>2012, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"365631176", "issn"=>"15537390", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "doi"=>"10.1371/journal.pgen.1002930", "scopus"=>"2-s2.0-84866174382", "pmid"=>"22952454", "sgr"=>"84866174382"}, "id"=>"cfb1f31d-5a7d-3f17-a385-bbf7535b2ebd", "abstract"=>"Ants are a highly successful family of insects that thrive in a variety of habitats across the world. Perhaps their best-known features are complex social organization and strict division of labor, separating reproduction from the day-to-day maintenance and care of the colony, as well as strict discrimination against foreign individuals. Since these social characteristics in ants are thought to be mediated by semiochemicals, a thorough analysis of these signals, and the receptors that detect them, is critical in revealing mechanisms that lead to stereotypic behaviors. To address these questions, we have defined and characterized the major chemoreceptor families in a pair of behaviorally and evolutionarily distinct ant species, Camponotus floridanus and Harpegnathos saltator. Through comprehensive re-annotation, we show that these ant species harbor some of the largest yet known repertoires of odorant receptors (Ors) among insects, as well as a more modest number of gustatory receptors (Grs) and variant ionotropic glutamate receptors (Irs). Our phylogenetic analyses further demonstrate remarkably rapid gains and losses of ant Ors, while Grs and Irs have also experienced birth-and-death evolution to different degrees. In addition, comparisons of antennal transcriptomes between sexes identify many chemoreceptors that are differentially expressed between males and females and between species. We have also revealed an agonist for a worker-enriched OR from C. floridanus, representing the first case of a heterologously characterized ant tuning Or. Collectively, our analysis reveals a large number of ant chemoreceptors exhibiting patterns of differential expression and evolution consistent with sex/species-specific functions. These differentially expressed genes are likely associated with sex-based differences, as well as the radically different social lifestyles observed between C. floridanus and H. saltator, and thus are targets for further functional characterization. Our findings represent an important advance toward understanding the molecular basis of social interactions and the differential chemical ecologies among ant species.", "link"=>"http://www.mendeley.com/research/phylogenetic-transcriptomic-analysis-chemosensory-receptors-pair-divergent-ant-species-reveals-sexsp", "reader_count"=>147, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>11, "Researcher"=>31, "Student > Doctoral Student"=>11, "Student > Ph. D. Student"=>41, "Student > Postgraduate"=>8, "Other"=>5, "Student > Master"=>18, "Student > Bachelor"=>11, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>11, "Researcher"=>31, "Student > Doctoral Student"=>11, "Student > Ph. D. 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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/583052"], "description"=>"<p>Number of <i>Or</i>, <i>Gr</i>, and <i>Ir</i> gene predictions in six hymenopteran species. For <i>Or</i> and <i>Gr</i> genes, the number to the right is the number of all gene models (coding for proteins longer than 300 aa in <i>C. floridanus</i> and <i>H. saltator</i>, or 200 aa in other species), while the number to the left is the number of seemingly intact gene models.</p>", "links"=>[], "tags"=>["chemosensory", "receptor"], "article_id"=>253537, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Annotation_of_C_floridanus_and_H_saltator_chemosensory_receptor_genes_/253537", "title"=>"Annotation of <i>C. floridanus</i> and <i>H. saltator</i> chemosensory receptor genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 00:58:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/309192", "https://ndownloader.figshare.com/files/309242", "https://ndownloader.figshare.com/files/309260", "https://ndownloader.figshare.com/files/309274", "https://ndownloader.figshare.com/files/309282", "https://ndownloader.figshare.com/files/309318", "https://ndownloader.figshare.com/files/309346", "https://ndownloader.figshare.com/files/309379", "https://ndownloader.figshare.com/files/309405", "https://ndownloader.figshare.com/files/309418", "https://ndownloader.figshare.com/files/309431", "https://ndownloader.figshare.com/files/309462", "https://ndownloader.figshare.com/files/309479", "https://ndownloader.figshare.com/files/309495", "https://ndownloader.figshare.com/files/309516", "https://ndownloader.figshare.com/files/309534", "https://ndownloader.figshare.com/files/309544", "https://ndownloader.figshare.com/files/309555", "https://ndownloader.figshare.com/files/309567", "https://ndownloader.figshare.com/files/309589"], "description"=>"<div><p>Ants are a highly successful family of insects that thrive in a variety of habitats across the world. Perhaps their best-known features are complex social organization and strict division of labor, separating reproduction from the day-to-day maintenance and care of the colony, as well as strict discrimination against foreign individuals. Since these social characteristics in ants are thought to be mediated by semiochemicals, a thorough analysis of these signals, and the receptors that detect them, is critical in revealing mechanisms that lead to stereotypic behaviors. To address these questions, we have defined and characterized the major chemoreceptor families in a pair of behaviorally and evolutionarily distinct ant species, <em>Camponotus floridanus</em> and <em>Harpegnathos saltator</em>. Through comprehensive re-annotation, we show that these ant species harbor some of the largest yet known repertoires of odorant receptors (<em>Ors</em>) among insects, as well as a more modest number of gustatory receptors (<em>Grs</em>) and variant ionotropic glutamate receptors (<em>Irs</em>). Our phylogenetic analyses further demonstrate remarkably rapid gains and losses of ant <em>Ors</em>, while <em>Grs</em> and <em>Irs</em> have also experienced birth-and-death evolution to different degrees. In addition, comparisons of antennal transcriptomes between sexes identify many chemoreceptors that are differentially expressed between males and females and between species. We have also revealed an agonist for a worker-enriched OR from <em>C. floridanus</em>, representing the first case of a heterologously characterized ant tuning Or. Collectively, our analysis reveals a large number of ant chemoreceptors exhibiting patterns of differential expression and evolution consistent with sex/species-specific functions. These differentially expressed genes are likely associated with sex-based differences, as well as the radically different social lifestyles observed between <em>C. floridanus</em> and <em>H. saltator</em>, and thus are targets for further functional characterization. Our findings represent an important advance toward understanding the molecular basis of social interactions and the differential chemical ecologies among ant species.</p> </div>", "links"=>[], "tags"=>["phylogenetic", "transcriptomic", "chemosensory", "receptors", "divergent", "ant", "reveals", "sex-specific", "signatures", "odor", "coding"], "article_id"=>120998, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002930.s001", "https://dx.doi.org/10.1371/journal.pgen.1002930.s002", "https://dx.doi.org/10.1371/journal.pgen.1002930.s003", "https://dx.doi.org/10.1371/journal.pgen.1002930.s004", "https://dx.doi.org/10.1371/journal.pgen.1002930.s005", "https://dx.doi.org/10.1371/journal.pgen.1002930.s006", "https://dx.doi.org/10.1371/journal.pgen.1002930.s007", "https://dx.doi.org/10.1371/journal.pgen.1002930.s008", "https://dx.doi.org/10.1371/journal.pgen.1002930.s009", "https://dx.doi.org/10.1371/journal.pgen.1002930.s010", "https://dx.doi.org/10.1371/journal.pgen.1002930.s011", "https://dx.doi.org/10.1371/journal.pgen.1002930.s012", "https://dx.doi.org/10.1371/journal.pgen.1002930.s013", "https://dx.doi.org/10.1371/journal.pgen.1002930.s014", "https://dx.doi.org/10.1371/journal.pgen.1002930.s015", "https://dx.doi.org/10.1371/journal.pgen.1002930.s016", "https://dx.doi.org/10.1371/journal.pgen.1002930.s017", "https://dx.doi.org/10.1371/journal.pgen.1002930.s018", "https://dx.doi.org/10.1371/journal.pgen.1002930.s019", "https://dx.doi.org/10.1371/journal.pgen.1002930.s020"], "stats"=>{"downloads"=>33, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Phylogenetic_and_Transcriptomic_Analysis_of_Chemosensory_Receptors_in_a_Pair_of_Divergent_Ant_Species_Reveals_Sex_Specific_Signatures_of_Odor_Coding/120998", "title"=>"Phylogenetic and Transcriptomic Analysis of Chemosensory Receptors in a Pair of Divergent Ant Species Reveals Sex-Specific Signatures of Odor Coding", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-08-30 00:16:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/583950"], "description"=>"<p>Significantly differentially expressed genes were identified by using Cuffdiff (q-value≤0.05). Number in bracket indicates the number of genes with higher expression level in male (or minor worker in the major worker vs. minor worker comparison).</p>", "links"=>[], "tags"=>["differentially", "chemosensory", "receptor", "genes", "revealed", "antennal"], "article_id"=>254433, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.t001", "stats"=>{"downloads"=>4, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significantly_differentially_expressed_C_floridanus_and_H_saltator_chemosensory_receptor_genes_revealed_by_analysis_of_antennal_transcriptomes_/254433", "title"=>"Significantly differentially expressed <i>C. floridanus</i> and <i>H. saltator</i> chemosensory receptor genes revealed by analysis of antennal transcriptomes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-08-30 01:13:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/583409"], "description"=>"<p>A maximum-likelihood tree of hymenopteran <i>Ir</i> genes estimated by using RAxML with Le-Gascuel (LG) model. Reliability of internal nodes was evaluated by 100 bootstrap replicates. Grey round dots indicate well-supported clades of “antennal” or “divergent” <i>IRs</i> (bootstrap value ≥80). Bootstrap values ≥70 are shown for relationships among the well supported clades. Subfamilies are named after the orthologs in <i>L. humile</i> and <i>P. barbatus</i>. <i>Irs</i> in different species are color-coded as following: <i>N. vitripennis</i>, black; <i>A. mellifera</i>, purple; <i>H. saltator</i>, blue; <i>L. humile</i>, yellow; <i>P. barbatus</i>, green; and <i>C. floridanus</i>, red. Clades for “antennal <i>IRs</i>” are highlighted in red. The clades for ionotropic glutamate receptors were collapsed.</p>", "links"=>[], "tags"=>["relationships", "hymenoptera"], "article_id"=>253900, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_relationships_of_Hymenoptera_Ir_genes_/253900", "title"=>"Phylogenetic relationships of Hymenoptera <i>Ir</i> genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 01:05:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/583255"], "description"=>"<p>A maximum-likelihood tree of hymenopteran <i>Gr</i> genes estimated by using RAxML with Le-Gascuel (LG) model. Reliability of internal nodes was evaluated by 100 bootstrap replicates. Grey round dots indicate well-supported subfamilies (bootstrap value ≥80). Bootstrap values ≥70 are shown for relationships among subfamilies. Subfamilies showing interesting evolutionary patterns are named after the orthologs in <i>N. vitripennis</i> and <i>A. mellifera</i>. The other subfamilies are named as <i>A</i>–<i>H</i>. <i>Grs</i> in different species are color-coded as following: <i>N. vitripennis</i>, black; <i>A. mellifera</i>, purple; <i>H. saltator</i>, blue; <i>L. humile</i>, yellow; <i>P. barbatus</i>, green; and <i>C. floridanus</i>, red.</p>", "links"=>[], "tags"=>["relationships", "hymenoptera"], "article_id"=>253742, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_relationships_of_Hymenoptera_Gr_genes_/253742", "title"=>"Phylogenetic relationships of Hymenoptera <i>Gr</i> genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 01:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/583794"], "description"=>"<p>(A) The <i>GR</i> family. (B) The <i>IR</i> family. Short lines indicate median expression levels for each gene set. In both panels, genes expressed below the medians of their respective transcriptomes were labeled by grey.</p>", "links"=>[], "tags"=>["levels"], "article_id"=>254287, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g007", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_levels_of_Gr_and_Ir_genes_/254287", "title"=>"Expression levels of <i>Gr</i> and <i>Ir</i> genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 01:11:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/583552"], "description"=>"<p>(A) <i>OR</i> family. (B) <i>GR</i> family. (C) <i>IR</i> family. The results of CAFÉ and Notung are highlighted in blue and red, respectively. Numbers above branches indicate net copy number changes estimated by CAFÉ. Numbers below branches with plus and negative signs indicate the number of gene gain and loss events estimated by Notung, respectively. Single asterisk indicates significant branch-specific expansions/contractions. Double asterisk indicates gene families that significantly violate the random gene birth and death assumption of CAFÉ. The phylogeny of Hymenoptera and the time scale are from <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002930#pgen.1002930-Moreau1\" target=\"_blank\">[1]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002930#pgen.1002930-Brady1\" target=\"_blank\">[102]</a>.</p>", "links"=>[], "tags"=>["numbers", "birth-and-death", "events", "ancestral", "copies", "chemosensory"], "article_id"=>254034, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g005", "stats"=>{"downloads"=>4, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimated_numbers_of_gene_birth_and_death_events_and_ancestral_gene_copies_for_chemosensory_gene_families_/254034", "title"=>"Estimated numbers of gene birth-and-death events and ancestral gene copies for chemosensory gene families.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 01:07:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/583862"], "description"=>"<p>When paired with a previously characterized mosquito Or (AgOR10) <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002930#pgen.1002930-Bohbot1\" target=\"_blank\">[103]</a>, both CfOrco (<i>C. floridanus</i> Orco) (A) and HsOrco (<i>H.saltator</i> Orco) (B) produced responses to VUAA1 (an agonist for Orco) <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002930#pgen.1002930-Jones1\" target=\"_blank\">[35]</a> and benzaldehyde (BA, an agonist for AgOR10) in <i>Xenopus</i> oocytes. These responses were not observed in water-injected control oocytes (C). The novel <i>C. floridanus</i> tuning Or CfOr263 also shows a specific and dose-dependent response to 2,4,5-trimethylthiazole (TMT) (D), while the novel <i>H. saltator</i> tuning Or HsOr55 shows a similar dose-dependent response to 4-methoxyphenylacetone (4 MPA) (F). Neither response is observed in water-injected oocytes (E,G).</p>", "links"=>[], "tags"=>["ligands"], "article_id"=>254351, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g008", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_ligands_for_C_floridanus_and_H_saltator_Ors_/254351", "title"=>"Identification of ligands for <i>C. floridanus</i> and <i>H. saltator</i> Ors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 01:12:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/583135"], "description"=>"<p>(A) A maximum-likelihood tree of hymenopteran <i>Or</i> genes estimated by using RAxML with Le-Gascuel (LG) model. Reliability of internal nodes was evaluated by 100 bootstrap replicates. Grey round dots indicate well-supported subfamilies (bootstrap value ≥80). Bootstrap values ≥70 are shown for relationships among subfamilies. <i>Ors</i> in different species are color-coded as following: <i>N. vitripennis</i>, black; <i>A. mellifera</i>, purple; <i>H. saltator</i>, blue; <i>L. humile</i>, yellow; <i>P. barbatus</i>, green; and <i>C. floridanus</i>, red. Subfamilies with rapid changes in gene copy numbers are highlighted in red. (B) Numbers of hymenopteran <i>Or</i> genes in well supported subfamilies.</p>", "links"=>[], "tags"=>["relationships", "hymenoptera"], "article_id"=>253622, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_relationships_of_Hymenoptera_Or_genes_/253622", "title"=>"Phylogenetic relationships of Hymenoptera <i>Or</i> genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 01:00:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/583682"], "description"=>"<p>(A) Expression profiles of <i>C. floridanus</i> and <i>H. saltator Ors</i> shown along with the phylogeny of <i>Or</i> genes. In the phylogenetic tree, <i>C. floridanus Ors</i> are labeled by red and <i>H. saltator Ors</i> by blue. In the heat-map, red color indicates higher expression level in worker and green indicates higher expression level in male. The inner circle shows the relative expressions of <i>C. floridanus Ors</i> between major worker and male (comparison between minor worker and male not shown because of the highly similar expression profiles of <i>C. floridanus</i> major and minor workers); the outer circle shows the relative expressions of <i>H. saltator Ors</i> between worker and male. FPKM stands for Fragments Per Kilobase of exon per Million fragments mapped. (B) Expression levels of <i>Ors</i> belonging to the three basal clades in the 9-exon subfamilies. <i>C. floridanus Ors</i> had significantly higher expression in male (<i>p</i>-value<0.05; Wilcoxon ranked-sum test), while <i>H. saltator Ors</i> had significantly higher expressions in worker (<i>p</i>-value<1e-4; Wilcoxon ranked-sum test). (C) Expression levels of the remaining <i>Ors</i> in the 9-exon subfamilies. For both <i>C. floridanus</i> and <i>H. saltator</i>, <i>Ors</i> had significantly higher expressions in worker (<i>p</i>-value<1e-15; Wilcoxon ranked-sum test). Short lines indicate median expression levels for each gene set. For both panels (B) and (C), genes expressed below the medians of their respective transcriptomes were labeled by grey.</p>", "links"=>[], "tags"=>["expressions", "evolutionarily"], "article_id"=>254171, "categories"=>["Neuroscience", "Genetics", "Evolutionary Biology"], "users"=>["Xiaofan Zhou", "Jesse D. Slone", "Antonis Rokas", "Shelley L. Berger", "Jürgen Liebig", "Anandasankar Ray", "Danny Reinberg", "Laurence J. Zwiebel"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002930.g006", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Diversified_expressions_of_evolutionarily_related_Or_genes_/254171", "title"=>"Diversified expressions of evolutionarily related <i>Or</i> genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-30 01:09:31"}

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Relative Metric

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