Female Behaviour Drives Expression and Evolution of Gustatory Receptors in Butterflies
Publication Date
July 11, 2013
Journal
PLOS Genetics
Authors
Adriana D. Briscoe, Aide Macias Muñoz, Krzysztof M. Kozak, James R. Walters, et al
Volume
9
Issue
7
Pages
e1003620
DOI
https://dx.plos.org/10.1371/journal.pgen.1003620
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1003620
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23950722
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3732137
Europe PMC
http://europepmc.org/abstract/MED/23950722
Web of Science
000322321100024
Scopus
84880831421
Mendeley
http://www.mendeley.com/research/female-behaviour-drives-expression-evolution-gustatory-receptors-butterflies
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Mendeley | Further Information

{"title"=>"Female Behaviour Drives Expression and Evolution of Gustatory Receptors in Butterflies", "type"=>"journal", "authors"=>[{"first_name"=>"Adriana D.", "last_name"=>"Briscoe", "scopus_author_id"=>"6604092245"}, {"first_name"=>"Aide", "last_name"=>"Macias-Muñoz", "scopus_author_id"=>"56008699500"}, {"first_name"=>"Krzysztof M.", "last_name"=>"Kozak", "scopus_author_id"=>"55342696900"}, {"first_name"=>"James R.", "last_name"=>"Walters", "scopus_author_id"=>"7201758486"}, {"first_name"=>"Furong", "last_name"=>"Yuan", "scopus_author_id"=>"15761619300"}, {"first_name"=>"Gabriel A.", "last_name"=>"Jamie", "scopus_author_id"=>"37067348200"}, {"first_name"=>"Simon H.", "last_name"=>"Martin", "scopus_author_id"=>"37102428400"}, {"first_name"=>"Kanchon K.", "last_name"=>"Dasmahapatra", "scopus_author_id"=>"6602134403"}, {"first_name"=>"Laura C.", "last_name"=>"Ferguson", "scopus_author_id"=>"24576541600"}, {"first_name"=>"James", "last_name"=>"Mallet", "scopus_author_id"=>"7202284097"}, {"first_name"=>"Emmanuelle", "last_name"=>"Jacquin-Joly", "scopus_author_id"=>"6601961667"}, {"first_name"=>"Chris D.", "last_name"=>"Jiggins", "scopus_author_id"=>"6603932806"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"84880831421", "doi"=>"10.1371/journal.pgen.1003620", "pui"=>"369438604", "pmid"=>"23950722", "scopus"=>"2-s2.0-84880831421", "issn"=>"15537390", "isbn"=>"1553-7404"}, "id"=>"a453edf7-fbdf-3495-882d-b2b50f91bb5a", "abstract"=>"Secondary plant compounds are strong deterrents of insect oviposition and feeding, but may also be attractants for specialist herbivores. These insect-plant interactions are mediated by insect gustatory receptors (Grs) and olfactory receptors (Ors). An analysis of the reference genome of the butterfly Heliconius melpomene, which feeds on passion-flower vines (Passiflora spp.), together with whole-genome sequencing within the species and across the Heliconius phylogeny has permitted an unprecedented opportunity to study the patterns of gene duplication and copy-number variation (CNV) among these key sensory genes. We report in silico gene predictions of 73 Gr genes in the H. melpomene reference genome, including putative CO 2 , sugar, sugar alcohol, fructose, and bitter receptors. The majority of these Grs are the result of gene duplications since Heliconius shared a common ancestor with the monarch butterfly or the silkmoth. Among Grs but not Ors, CNVs are more common within species in those gene lineages that have also duplicated over this evolutionary time-scale, suggesting ongoing rapid gene family evolution. Deep sequencing (,1 billion reads) of transcriptomes from proboscis and labial palps, antennae, and legs of adult H. melpomene males and females indicates that 67 of the predicted 73 Gr genes and 67 of the 70 predicted Or genes are expressed in these three tissues. Intriguingly, we find that one-third of all Grs show female-biased gene expression (n = 26) and nearly all of these (n = 21) are Heliconius-specific Grs. In fact, a significant excess of Grs that are expressed in female legs but not male legs are the result of recent gene duplication. This difference in Gr gene expression diversity between the sexes is accompanied by a striking sexual dimorphism in the abundance of gustatory sensilla on the forelegs of H. melpomene, suggesting that female oviposition behaviour drives the evolution of new gustatory receptors in butterfly genomes.", "link"=>"http://www.mendeley.com/research/female-behaviour-drives-expression-evolution-gustatory-receptors-butterflies", "reader_count"=>120, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>6, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>4, "Student > Master"=>20, "Other"=>2, "Student > Bachelor"=>10, "Lecturer"=>3, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>6, "Researcher"=>25, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>4, "Student > Master"=>20, "Other"=>2, "Student > Bachelor"=>10, "Lecturer"=>3, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>103, "Medicine and Dentistry"=>2, "Neuroscience"=>2, "Veterinary Science and Veterinary Medicine"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>103}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Hungary"=>1, "United States"=>5, "China"=>2, "Poland"=>1, "United Kingdom"=>1, "Australia"=>2, "Kenya"=>2, "Germany"=>2, "Russia"=>1}, "group_count"=>2}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1117559"], "description"=>"*<p>Consists of single-copy genes in <i>H. melpomene</i>; in the monarch or <i>Bombyx</i> genomes, homologues are either single-copy or duplicate genes with bootstrap support ≥80%.</p>†<p>Fisher's exact test, two-tailed, d.f. = 1.</p>‡<p>Excludes <i>Gr39</i> because of poor coverage in the reference genome read-mapping.</p>§<p>Excludes <i>Or20</i> and <i>Or24</i> because of coverage in the reference genome.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "overabundance", "legs"], "article_id"=>744461, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.t002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_An_overabundance_of_Grs_expressed_in_female_legs_are_the_result_of_Heliconius_specific_duplication_/744461", "title"=>"An overabundance of <i>Grs</i> expressed in female legs are the result of <i>Heliconius</i>-specific duplication.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117558"], "description"=>"<p>Numbers indicate intact genes and numbers in parentheses indicate pseudogenes. References are given in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Heliconius1\" target=\"_blank\">[13]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Gardiner1\" target=\"_blank\">[55]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-SnchezGracia1\" target=\"_blank\">[94]</a>. OBP = odorant binding protein; CSP = chemosensory protein; OR = olfactory receptor, GR = gustatory receptor.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "chemosensory"], "article_id"=>744460, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g010", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Insect_chemosensory_gene_family_repertoires_/744460", "title"=>"Insect chemosensory gene family repertoires.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117555"], "description"=>"<p>Scaffolds comprising each chromosome are indicated by alternating light and grey stripes. <i>Grs</i> without CNVs are indicated by open boxes and <i>Grs</i> with CNVs are indicated by closed boxes. <i>Grs</i> are classified as conserved if, in the <i>H. melpomene</i> reference genome, they have a one-to-one orthologous relationship with either a gene in <i>Danaus</i>, <i>Bombyx</i> or both (red dots, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen-1003620-g003\" target=\"_blank\">Figure 3</a>). <i>Grs</i> are classified as non-conserved if they are duplicated in the <i>H. melpomene</i> reference genome or have no orthologue in either <i>Danaus</i>, <i>Bombyx</i> or both. Genes mapped to chromosomes but without precise locations are indicated by question marks. Scaffold arrangement is based on the published linkage map <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Heliconius1\" target=\"_blank\">[13]</a>.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "variant"], "article_id"=>744457, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g007", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Copy_number_variant_CNV_analysis_of_Grs_in_the_H_melpomene_genome_/744457", "title"=>"Copy-number variant (CNV) analysis of <i>Grs</i> in the <i>H.</i><i>melpomene</i> genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117553"], "description"=>"<p>(A) Reverse-transcriptase PCR (RT-PCR) of adult <i>H. melpomene</i> tissues showing the expression of <i>HmGr22</i> and <i>elongation factor-1 alpha</i>. Two products are evident from the <i>Gr22</i> RT-PCR. The bottom RT-PCR product is <i>HmGr22</i> (arrow) and the top RT-PCR product is 18 s <i>rRNA</i>, which was verified by Sanger sequencing. (B) Neighbor-joining tree showing the phylogenetic relationship between the forty-six intact <i>Grs</i> and four pseudogenes identified in the 13 lepidopteran genomes. Bootstrap support is out of 500 bootstrap replicates. Pseudogene sequences are indicated by a ‘p’ after the gene name.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "adults", "intronless", "whole-genome"], "article_id"=>744455, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g005", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HmGr22_expression_in_adults_and_intronless_Grs_from_whole_genome_sequence_data_across_the_Heliconius_phylogeny_/744455", "title"=>"<i>HmGr22</i> expression in adults and intronless <i>Grs</i> from whole-genome sequence data across the <i>Heliconius</i> phylogeny.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117554"], "description"=>"<p>Estimates of the number of <i>Gr</i> loci (number of pseudogenes is indicated in parentheses) on internal nodes of the lepidopteran phylogeny and gene gain (purple dots), gene loss (orange slashes) and pseudogenisation events (red slashes) on each branch. <i>Heliconius</i> phylogeny is based on Beltran et al. (2007) <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Beltran1\" target=\"_blank\">[90]</a>. Reconciliation of gene trees onto the species tree was performed in Notung using maximum likelihood gene family trees. Primary <i>Passiflora</i> host plant subgenera (green dots) affiliated with each <i>Heliconius</i> species <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Brown1\" target=\"_blank\">[53]</a>. No clear relationship exists between the number of known <i>Passiflora</i> subgenera used and the number of intronless <i>Grs</i> in a species, which are presumed to be putative bitter receptors, but whose ligands are not yet identified. The woody vine specialist, <i>H. doris</i>, with the smallest effective population size, has the fewest intact intronless <i>Grs</i>.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "patterns", "intronless", "genus"], "article_id"=>744456, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g006", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inferred_patterns_of_intronless_Gr_gene_gain_and_loss_across_the_genus_Heliconius_/744456", "title"=>"Inferred patterns of intronless <i>Gr</i> gene gain and loss across the genus <i>Heliconius</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117552"], "description"=>"<p>A maximum likelihood analysis of amino acid sequences was performed. Bootstrap support is out of 500 replicates. Fewer lineage-specific duplications are evident among the <i>Ors</i> compared to the <i>Grs</i>, with the exception of one large butterfly-specific expansion (orange arc). Small red dots indicate single-copy <i>Heliconius Ors</i> classified as conserved genes in the analyses shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen-1003620-t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen-1003620-t002\" target=\"_blank\">Table 2</a>. <i>Ors</i> that are enriched in male or female adult <i>B. mori</i> antennae (blue and black arcs) are described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Wanner2\" target=\"_blank\">[91]</a>; <i>cis</i>-jasmonate and monoterpene citral receptors are described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Tanaka1\" target=\"_blank\">[92]</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Jordan1\" target=\"_blank\">[93]</a>. Phylogenetic tree reconstruction details are given in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Heliconius1\" target=\"_blank\">[13]</a>. Bar indicates branch lengths in proportion to amino acid substitutions/site. Small arrows indicate female-specific <i>Ors</i> expressed in adult <i>H. melpomene</i> legs. Bm = <i>Bombyx mori</i>, Hm = <i>Heliconius melpomene</i>, Dp = <i>Danaus plexippus</i>.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "ors", "lepidopteran"], "article_id"=>744454, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogeny_of_the_Ors_identified_in_three_lepidopteran_genomes_/744454", "title"=>"Phylogeny of the Ors identified in three lepidopteran genomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117563", "https://ndownloader.figshare.com/files/1117564", "https://ndownloader.figshare.com/files/1117565", "https://ndownloader.figshare.com/files/1117566", "https://ndownloader.figshare.com/files/1117567", "https://ndownloader.figshare.com/files/1117569", "https://ndownloader.figshare.com/files/1117570", "https://ndownloader.figshare.com/files/1117571", "https://ndownloader.figshare.com/files/1117572", "https://ndownloader.figshare.com/files/1117574", "https://ndownloader.figshare.com/files/1117575", "https://ndownloader.figshare.com/files/1117576", "https://ndownloader.figshare.com/files/1117578", "https://ndownloader.figshare.com/files/1117579", "https://ndownloader.figshare.com/files/1117580", "https://ndownloader.figshare.com/files/1117582"], "description"=>"<div><p>Secondary plant compounds are strong deterrents of insect oviposition and feeding, but may also be attractants for specialist herbivores. These insect-plant interactions are mediated by insect gustatory receptors (<i>Grs</i>) and olfactory receptors (<i>Ors</i>). An analysis of the reference genome of the butterfly <i>Heliconius melpomene</i>, which feeds on passion-flower vines (<i>Passiflora</i> spp.), together with whole-genome sequencing within the species and across the <i>Heliconius</i> phylogeny has permitted an unprecedented opportunity to study the patterns of gene duplication and copy-number variation (CNV) among these key sensory genes. We report <i>in silico</i> gene predictions of 73 <i>Gr</i> genes in the <i>H. melpomene</i> reference genome, including putative CO<sub>2</sub>, sugar, sugar alcohol, fructose, and bitter receptors. The majority of these <i>Grs</i> are the result of gene duplications since <i>Heliconius</i> shared a common ancestor with the monarch butterfly or the silkmoth. Among <i>Grs</i> but not <i>Ors</i>, CNVs are more common within species in those gene lineages that have also duplicated over this evolutionary time-scale, suggesting ongoing rapid gene family evolution. Deep sequencing (∼1 billion reads) of transcriptomes from proboscis and labial palps, antennae, and legs of adult <i>H. melpomene</i> males and females indicates that 67 of the predicted 73 <i>Gr</i> genes and 67 of the 70 predicted <i>Or</i> genes are expressed in these three tissues. Intriguingly, we find that one-third of all <i>Grs</i> show female-biased gene expression (n = 26) and nearly all of these (n = 21) are <i>Heliconius</i>-specific <i>Grs</i>. In fact, a significant excess of <i>Grs</i> that are expressed in female legs but not male legs are the result of recent gene duplication. This difference in <i>Gr</i> gene expression diversity between the sexes is accompanied by a striking sexual dimorphism in the abundance of gustatory sensilla on the forelegs of <i>H. melpomene</i>, suggesting that female oviposition behaviour drives the evolution of new gustatory receptors in butterfly genomes.</p></div>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "behaviour", "drives", "gustatory", "receptors"], "article_id"=>744465, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003620.s001", "https://dx.doi.org/10.1371/journal.pgen.1003620.s002", "https://dx.doi.org/10.1371/journal.pgen.1003620.s003", "https://dx.doi.org/10.1371/journal.pgen.1003620.s004", "https://dx.doi.org/10.1371/journal.pgen.1003620.s005", "https://dx.doi.org/10.1371/journal.pgen.1003620.s006", "https://dx.doi.org/10.1371/journal.pgen.1003620.s007", "https://dx.doi.org/10.1371/journal.pgen.1003620.s008", "https://dx.doi.org/10.1371/journal.pgen.1003620.s009", "https://dx.doi.org/10.1371/journal.pgen.1003620.s010", "https://dx.doi.org/10.1371/journal.pgen.1003620.s011", "https://dx.doi.org/10.1371/journal.pgen.1003620.s012", "https://dx.doi.org/10.1371/journal.pgen.1003620.s013", "https://dx.doi.org/10.1371/journal.pgen.1003620.s014", "https://dx.doi.org/10.1371/journal.pgen.1003620.s015", "https://dx.doi.org/10.1371/journal.pgen.1003620.s016"], "stats"=>{"downloads"=>3, "page_views"=>47, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Female_Behaviour_Drives_Expression_and_Evolution_of_Gustatory_Receptors_in_Butterflies_/744465", "title"=>"Female Behaviour Drives Expression and Evolution of Gustatory Receptors in Butterflies", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117548"], "description"=>"<p>(A) The labial palps (lp) and proboscis (p) of the <i>H. erato</i> head contain gustatory sensilla. (B) The proximal portion of the <i>H. melpomene</i> proboscis has hair-like <i>sensilla chaetica</i> (sc). (C) The tip portion of the proboscis has specialized ridges for pollen collection along with <i>sensilla styloconica</i> (ss). Reproduced with permission <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Krenn1\" target=\"_blank\">[9]</a>. (D) <i>H. melpomene</i> with a pollen-load. c, clypeus, ce, compound eye; pr, proximal region; mr, mid region; tr, tip region; dgl, dorsal galeal linking structures; sb, blunt-tipped sensilla.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "electron", "micrographs", "proboscis"], "article_id"=>744450, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scanning_electron_micrographs_of_the_proboscis_of_Heliconius_butterflies_/744450", "title"=>"Scanning electron micrographs of the proboscis of <i>Heliconius</i> butterflies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117560"], "description"=>"*<p>Consists of single-copy genes in <i>H. melpomene</i>; in the monarch or <i>Bombyx</i> genomes, homologues are either single-copy or duplicate genes with bootstrap support ≥80%.</p>§<p>Fisher's exact test, two-tailed.</p>†<p>Excludes 3 Grs where read-mapping of the reference genome reads back to the reference assembly indicated areas of poor assembly: <i>Gr37</i>, <i>Gr39</i> and <i>Gr49</i>.</p>‡<p>Excludes 3 Ors where read-mapping of the reference genome reads back to the reference assembly indicated areas of poor assembly: <i>Or20</i>, <i>Or24</i>, <i>Or43</i>, <i>Or50</i> and <i>Or74</i>.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "evolutionarily-conserved", "genes", "copy-number"], "article_id"=>744462, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_between_evolutionarily_conserved_genes_and_copy_number_variation_CNV_/744462", "title"=>"Relationship between evolutionarily-conserved genes and copy-number variation (CNV).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117557"], "description"=>"<p>(A) The common set of <i>Grs</i> expressed in each tissue in both males and females. Red box indicates the presence of reads uniquely mapping to the coding region of each <i>Gr</i> gene model. To facilitate the visualization of tissue-specific expression found in both males and females, only <i>Grs</i> where both sexes show expression are indicated. Where only one sex or neither sex shows expression, the box is empty. (B) <i>Grs</i> showing sex-specific expression. To facilitate the visualization of sex-specific <i>Grs</i>, only <i>Grs</i> where one sex shows expression are indicated by a filled box. <i>Grs</i> which are expressed in both sexes or no sex are indicated by an empty box. (C) Venn diagram showing the number of uniquely expressed gustatory receptors in each transcriptome. (D) The common set of <i>Ors</i> expressed in each tissue in both males and females. Blue box indicates the presence of reads uniquely mapping to the coding region of each <i>Or</i> gene model. As above, only <i>Ors</i> where both sexes show expression are indicated. Where only one sex or neither sex show expression, the box is empty. (E) <i>Ors</i> showing sex-specific expression are indicated by a filled box. <i>Ors</i> which are expressed in both sexes or no sex are indicated by an empty box. (F) Venn diagram showing the number of uniquely expressed gustatory receptors in each transcriptome. The proboscis libraries also included both labial palps, the antennal libraries included both antennae, and the leg libraries included all six legs.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "chemosensory"], "article_id"=>744459, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g009", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_Gr_and_Or_expression_in_male_and_female_adult_H_melpomene_chemosensory_tissues_/744459", "title"=>"Comparison of <i>Gr</i> and <i>Or</i> expression in male and female adult <i>H.</i><i>melpomene</i> chemosensory tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117556"], "description"=>"<p>Scaffolds comprising each chromosome are indicated by alternating light and grey stripes. <i>Ors</i> without CNVs are indicated by open boxes and <i>Ors</i> with CNVs are indicated by closed boxes. The classification of <i>Ors</i> as being either conserved or non-conserved follows the same criteria as for the <i>Grs</i>. The eight genes for which the chromosome locality is not known are shown at the bottom.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "variant"], "article_id"=>744458, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g008", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Copy_number_variant_CNV_analysis_of_Ors_in_the_H_melpomene_genome_/744458", "title"=>"Copy-number variant (CNV) analysis of <i>Ors</i> in the <i>H.</i><i>melpomene</i> genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117551"], "description"=>"<p>A maximum likelihood analysis of amino acid sequences was performed. Bootstrap support is out of 500 replicates. Putative CO<sub>2</sub> and fructose receptors show a conserved 1-to-1 orthologous relationship in each of the three lepidopteran genomes, while putative sugar receptors of the monarch butterfly have duplicated twice. By contrast, numerous butterfly- or moth-specific gene duplications are evident among the remaining <i>Grs</i>, which are hypothesized to be bitter receptors. Small red dots indicate single-copy <i>Heliconius Grs</i> classified as conserved genes in the analyses shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen-1003620-t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen-1003620-t002\" target=\"_blank\">Table 2</a>. Small black arrows indicate female-specific <i>Grs</i> expressed in adult <i>H. melpomene</i> legs. Small red arrows indicate <i>Grs</i> expressed in adult <i>H. melpomene</i> proboscis only. Bar indicates branch lengths in proportion to amino acid substitutions/site. Synephrine and fructose receptors are described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Ozaki1\" target=\"_blank\">[52]</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003620#pgen.1003620-Sato1\" target=\"_blank\">[32]</a>. Bm = <i>Bombyx mori</i>, Hm = <i>Heliconius melpomene</i>, Dp = <i>Danaus plexippus</i>, Px = <i>Papilio xuthus</i>.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "grs", "lepidopteran"], "article_id"=>744453, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogeny_of_the_Grs_identified_in_three_lepidopteran_genomes_/744453", "title"=>"Phylogeny of the Grs identified in three lepidopteran genomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1117550"], "description"=>"<p>Scanning electron micrographs of adult legs showing a sexual dimorphism in gustatory (trichoid) sensilla. Foreleg foretarsi of a male (A) and a female (B). Four pairs of clumped taste sensilla are each found associated with a pair of cuticular spines on each female foot (only three are shown). Arrow indicates a clump of taste sensilla. Antennae of an adult male (C) and a female (D) showing individual gustatory sensilla (arrow).</p>", "links"=>[], "tags"=>["Evolutionary biology", "Comparative genomics", "Genomic evolution", "genetics", "Molecular genetics", "Gene duplication", "gene expression", "genomics", "Genome sequencing", "neuroscience", "Sensory systems", "Gustatory system", "Olfactory system", "dimorphism", "chemosensory"], "article_id"=>744452, "categories"=>["Biological Sciences"], "users"=>["Adriana D. Briscoe", "Aide Macias-Muñoz", "Krzysztof M. Kozak", "James R. Walters", "Furong Yuan", "Gabriel A. Jamie", "Simon H. Martin", "Kanchon K. Dasmahapatra", "Laura C. Ferguson", "James Mallet", "Emmanuelle Jacquin-Joly", "Chris D. Jiggins"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003620.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sexual_dimorphism_in_H_melpomene_chemosensory_tissues_/744452", "title"=>"Sexual dimorphism in <i>H.</i><i>melpomene</i> chemosensory tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-11 03:32:49"}

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Anatomy", "average_usage"=>[248, 440, 562, 666, 765, 856, 944, 1028, 1112, 1198, 1282, 1362, 1430]}, {"subject_area"=>"/Biology and life sciences/Biotechnology", "average_usage"=>[259, 472, 622, 759, 885, 1009, 1123, 1232, 1335, 1437, 1533, 1627, 1698]}, {"subject_area"=>"/Biology and life sciences/Evolutionary biology", "average_usage"=>[302, 488, 607, 717, 832, 931, 1024, 1117, 1212, 1302, 1389, 1469, 1535]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[284, 491, 620, 738, 843, 945, 1043, 1137, 1225, 1315, 1400, 1479, 1555]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}, {"subject_area"=>"/Biology and life sciences/Zoology", "average_usage"=>[294, 473, 591, 693, 788, 883, 972, 1054, 1140, 1222, 1299, 1381, 1446]}, {"subject_area"=>"/Medicine and health sciences/Anatomy", "average_usage"=>[248, 441, 564, 668, 769, 859, 948, 1034, 1117, 1202, 1290, 1368, 1437]}]}
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