Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in the Harvester Ant Pogonomyrmex barbatus
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{"title"=>"Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in the Harvester Ant Pogonomyrmex barbatus", "type"=>"journal", "authors"=>[{"first_name"=>"Miguel", "last_name"=>"Corona", "scopus_author_id"=>"7004211006"}, {"first_name"=>"Romain", "last_name"=>"Libbrecht", "scopus_author_id"=>"39261990700"}, {"first_name"=>"Yannick", "last_name"=>"Wurm", "scopus_author_id"=>"15766615600"}, {"first_name"=>"Oksana", "last_name"=>"Riba-Grognuz", "scopus_author_id"=>"49962206100"}, {"first_name"=>"Romain A.", "last_name"=>"Studer", "scopus_author_id"=>"24823674400"}, {"first_name"=>"Laurent", "last_name"=>"Keller", "scopus_author_id"=>"7202066299"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"369887340", "isbn"=>"1553-7404", "issn"=>"15537390", "doi"=>"10.1371/journal.pgen.1003730", "scopus"=>"2-s2.0-84884626538", "pmid"=>"23966882", "sgr"=>"84884626538"}, "id"=>"fde58362-e6aa-3004-9aca-4524d0412da5", "abstract"=>"The reproductive ground plan hypothesis (RGPH) proposes that the physiological pathways regulating reproduction were co-opted to regulate worker division of labor. Support for this hypothesis in honeybees is provided by studies demonstrating that the reproductive potential of workers, assessed by the levels of vitellogenin (Vg), is linked to task performance. Interestingly, contrary to honeybees that have a single Vg ortholog and potentially fertile nurses, the genome of the harvester ant Pogonomyrmex barbatus harbors two Vg genes (Pb_Vg1 and Pb_Vg2) and nurses produce infertile trophic eggs. P. barbatus, thus, provides a unique model to investigate whether Vg duplication in ants was followed by subfunctionalization to acquire reproductive and non-reproductive functions and whether Vg reproductive function was co-opted to regulate behavior in sterile workers. To investigate these questions, we compared the expression patterns of P. barbatus Vg genes and analyzed the phylogenetic relationships and molecular evolution of Vg genes in ants. qRT-PCRs revealed that Pb_Vg1 is more highly expressed in queens compared to workers and in nurses compared to foragers. By contrast, the level of expression of Pb_Vg2 was higher in foragers than in nurses and queens. Phylogenetic analyses show that a first duplication of the ancestral Vg gene occurred after the divergence between the poneroid and formicoid clades and subsequent duplications occurred in the lineages leading to Solenopsis invicta, Linepithema humile and Acromyrmex echinatior. The initial duplication resulted in two Vg gene subfamilies preferentially expressed in queens and nurses (subfamily A) or in foraging workers (subfamily B). Finally, molecular evolution analyses show that the subfamily A experienced positive selection, while the subfamily B showed overall relaxation of purifying selection. Our results suggest that in P. barbatus the Vg gene underwent subfunctionalization after duplication to acquire caste- and behavior- specific expression associated with reproductive and non-reproductive functions, supporting the validity of the RGPH in ants.", "link"=>"http://www.mendeley.com/research/vitellogenin-underwent-subfunctionalization-acquire-caste-behavioral-specific-expression-harvester-a", "reader_count"=>87, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>20, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>2, "Student > Master"=>19, "Other"=>1, "Student > Bachelor"=>5, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>20, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>2, "Student > Master"=>19, "Other"=>1, "Student > Bachelor"=>5, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>11, "Agricultural and Biological Sciences"=>62, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>62}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Unspecified"=>{"Unspecified"=>7}, "Environmental Science"=>{"Environmental Science"=>3}}, "reader_count_by_country"=>{"Canada"=>1, "Austria"=>1, "United States"=>2, "Brazil"=>1, "France"=>2, "Germany"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1171497"], "description"=>"<p>A. Exon-intron organization of <i>Pb_Vg1</i> and <i>Pb_Vg2</i> genes. Blue boxes represent exons and joining lines introns. Green and red lines indicate start and stop codons respectively. Exon number (I–VII) and size (31–1596 bp) are indicated at the bottom and top of the figure. Exon VII in <i>Pb_Vg2</i> (282 bp) is truncated with respect to <i>Pb_Vg1</i> (591 bp). B. Localization of predicted protein structural domains: LPD-N (vitellogenin), DUF1943 and VDW.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary biology", "genetics", "genomics", "Molecular cell biology", "Population biology", "vitellogenin", "genes"], "article_id"=>773872, "categories"=>["Biological Sciences"], "users"=>["Miguel Corona", "Romain Libbrecht", "Yannick Wurm", "Oksana Riba-Grognuz", "Romain A. Studer", "Laurent Keller"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003730.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_map_of_vitellogenin_genes_in_Pogonomyrmex_barbatus_/773872", "title"=>"Genomic map of vitellogenin genes in <i>Pogonomyrmex barbatus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-15 03:28:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1171498"], "description"=>"<p>Vg sequences from species belonging to representative Hymenopteran groups are also included. Values at the nodes represent bootstrap support from 10,000 replicates. A and B represent different subfamilies of the formicoid clade.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary biology", "genetics", "genomics", "Molecular cell biology", "Population biology", "ant"], "article_id"=>773873, "categories"=>["Biological Sciences"], "users"=>["Miguel Corona", "Romain Libbrecht", "Yannick Wurm", "Oksana Riba-Grognuz", "Romain A. Studer", "Laurent Keller"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003730.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maximum_likelihood_tree_of_ant_vitellogenins_/773873", "title"=>"Maximum likelihood tree of ant vitellogenins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-15 03:28:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1171500"], "description"=>"<p>Values were pooled from five independent colonies (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003730#pgen.1003730.s001\" target=\"_blank\">Figure S1</a>). The y axes indicate the relative gene expression, corresponding to the <i>Pb_Vg1</i> and <i>Pb_Vg2</i> mRNA levels relative to the ribosomal protein RP49 (control) gene mRNA level (mean ± se). The upper panel (A) compares the expression levels of each Vg gene among queens, nurses and foragers. The lower panel (B) compares the expression of both Vg genes separately in queens, nurses and foragers.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary biology", "genetics", "genomics", "Molecular cell biology", "Population biology", "mrna", "nurses"], "article_id"=>773876, "categories"=>["Biological Sciences"], "users"=>["Miguel Corona", "Romain Libbrecht", "Yannick Wurm", "Oksana Riba-Grognuz", "Romain A. Studer", "Laurent Keller"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003730.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_mRNA_levels_of_Pb_Vg1_and_Pb_Vg2_in_queens_nurses_and_foragers_/773876", "title"=>"Relative mRNA levels of <i>Pb_Vg1</i> and <i>Pb_Vg2</i> in queens, nurses and foragers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-15 03:28:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1171502"], "description"=>"<p>Vg paralogs are divided in two subfamilies with different phylogenetic origin and protein length. Subfamilies A and B, range from 1641 to 1673 and from 1738 to 1845 amino acids, respectively. Known expression bias and gene identification numbers of the automatic gene predictions from which our gene models were derived are specified. <i>Ac_Vg2</i> genomic sequence is uncompleted.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary biology", "genetics", "genomics", "Molecular cell biology", "Population biology", "vg", "genes"], "article_id"=>773877, "categories"=>["Biological Sciences"], "users"=>["Miguel Corona", "Romain Libbrecht", "Yannick Wurm", "Oksana Riba-Grognuz", "Romain A. Studer", "Laurent Keller"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003730.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predicted_protein_length_of_Vg_genes_in_ants_/773877", "title"=>"Predicted protein length of Vg genes in ants.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-08-15 03:28:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1171503"], "description"=>"<p>Selective pressures are divided into three classes: ω0 (dN/dS<1, negative selection), ω1 (dN/dS = 1, neutral evolution) and ω2 (dN/dS ≥1, positive selection). p0, p1 and p2a+p2b are their respective proportion. lnL0 and lnL1 are the likelihood values of the null (ω2 = 1) and alternative (ω2≥1) models, respectively. The likelihood ratio test [2*(lnL1-lnL0)] allows discriminating between neutral evolution and positive selection. A p-value<0.01 presents a significant test (marked as **). Sites under positive selection with BEB score >95% are shown.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary biology", "genetics", "genomics", "Molecular cell biology", "Population biology"], "article_id"=>773878, "categories"=>["Biological Sciences"], "users"=>["Miguel Corona", "Romain Libbrecht", "Yannick Wurm", "Oksana Riba-Grognuz", "Romain A. Studer", "Laurent Keller"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003730.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_test_of_positive_selection_/773878", "title"=>"Results of test of positive selection.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-08-15 03:28:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1171504", "https://ndownloader.figshare.com/files/1171505"], "description"=>"<div><p>The reproductive ground plan hypothesis (RGPH) proposes that the physiological pathways regulating reproduction were co-opted to regulate worker division of labor. Support for this hypothesis in honeybees is provided by studies demonstrating that the reproductive potential of workers, assessed by the levels of vitellogenin (Vg), is linked to task performance. Interestingly, contrary to honeybees that have a single Vg ortholog and potentially fertile nurses, the genome of the harvester ant <i>Pogonomyrmex barbatus</i> harbors two Vg genes (<i>Pb_Vg1</i> and <i>Pb_Vg2</i>) and nurses produce infertile trophic eggs. <i>P. barbatus</i>, thus, provides a unique model to investigate whether Vg duplication in ants was followed by subfunctionalization to acquire reproductive and non-reproductive functions and whether Vg reproductive function was co-opted to regulate behavior in sterile workers. To investigate these questions, we compared the expression patterns of <i>P. barbatus</i> Vg genes and analyzed the phylogenetic relationships and molecular evolution of Vg genes in ants. qRT-PCRs revealed that <i>Pb_Vg1</i> is more highly expressed in queens compared to workers and in nurses compared to foragers. By contrast, the level of expression of <i>Pb_Vg2</i> was higher in foragers than in nurses and queens. Phylogenetic analyses show that a first duplication of the ancestral Vg gene occurred after the divergence between the poneroid and formicoid clades and subsequent duplications occurred in the lineages leading to <i>Solenopsis invicta</i>, <i>Linepithema humile</i> and <i>Acromyrmex echinatior</i>. The initial duplication resulted in two Vg gene subfamilies preferentially expressed in queens and nurses (subfamily A) or in foraging workers (subfamily B). Finally, molecular evolution analyses show that the subfamily A experienced positive selection, while the subfamily B showed overall relaxation of purifying selection. Our results suggest that in <i>P. barbatus</i> the Vg gene underwent subfunctionalization after duplication to acquire caste- and behavior- specific expression associated with reproductive and non-reproductive functions, supporting the validity of the RGPH in ants.</p></div>", "links"=>[], "tags"=>["developmental biology", "Evolutionary biology", "genetics", "genomics", "Molecular cell biology", "Population biology", "vitellogenin", "underwent", "subfunctionalization", "caste", "harvester", "ant"], "article_id"=>773879, "categories"=>["Biological Sciences"], "users"=>["Miguel Corona", "Romain Libbrecht", "Yannick Wurm", "Oksana Riba-Grognuz", "Romain A. Studer", "Laurent Keller"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003730.s001", "https://dx.doi.org/10.1371/journal.pgen.1003730.s002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Vitellogenin_Underwent_Subfunctionalization_to_Acquire_Caste_and_Behavioral_Specific_Expression_in_the_Harvester_Ant_Pogonomyrmex_barbatus_/773879", "title"=>"Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in the Harvester Ant <i>Pogonomyrmex barbatus</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-08-15 03:28:41"}

PMC Usage Stats | Further Information

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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", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Computational biology", "average_usage"=>[295, 511, 651, 775, 882, 992, 1100, 1201, 1304, 1400, 1486, 1570, 1650]}, {"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/Zoology", "average_usage"=>[294, 473, 591, 693, 788, 883, 972, 1054, 1140, 1222, 1299, 1381, 1446]}, {"subject_area"=>"/Medicine and health sciences/Anatomy and physiology", "average_usage"=>[253, 430]}]}
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