Episodic Positive Selection in the Evolution of Avian Toll-Like Receptor Innate Immunity Genes
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{"title"=>"Episodic positive selection in the evolution of avian toll-like receptor innate immunity genes", "type"=>"journal", "authors"=>[{"first_name"=>"Catherine E.", "last_name"=>"Grueber", "scopus_author_id"=>"24080444100"}, {"first_name"=>"Graham P.", "last_name"=>"Wallis", "scopus_author_id"=>"7102196704"}, {"first_name"=>"Ian G.", "last_name"=>"Jamieson", "scopus_author_id"=>"7004916616"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84897049000", "sgr"=>"84897049000", "pui"=>"372716770", "isbn"=>"1932-6203", "pmid"=>"24595315", "doi"=>"10.1371/journal.pone.0089632"}, "id"=>"4ccc5683-e57f-33ea-b0a5-9d651ec37ad0", "abstract"=>"Toll-like receptors (TLRs) are a family of conserved pattern-recognition molecules responsible for initiating innate and acquired immune responses. Because they play a key role in host defence, these genes have received increasing interest in the evolutionary and population genetics literature, as their variation represents a potential target of adaptive evolution. However, the role of pathogen-mediated selection (i.e. episodic positive selection) in the evolution of these genes remains poorly known and has not been examined outside of mammals. A recent increase in the number of bird species for which TLR sequences are available has enabled us to examine the selective processes that have influenced evolution of the 10 known avian TLR genes. Specifically, we tested for episodic positive selection to identify codons that experience purifying selection for the majority of their evolution, interspersed with bursts of positive selection that may occur only in restricted lineages. We included up to 23 species per gene (mean = 16.0) and observed that, although purifying selection was evident, an average of 4.5% of codons experienced episodic positive selection across all loci. For four genes in which sequence coverage traversed both the extracellular leucine-rich repeat region (LRR) and transmembrane/intracellular domains of the proteins, increased positive selection was observed at the extracellular domain, consistent with theoretical predictions. Our results provide evidence that episodic positive selection has played an important role in the evolution of most avian TLRs, consistent with the role of these loci in pathogen recognition and a mechanism of host-pathogen coevolution.", "link"=>"http://www.mendeley.com/research/episodic-positive-selection-evolution-avian-tolllike-receptor-innate-immunity-genes", "reader_count"=>46, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>5, "Researcher"=>10, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>4, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>5, "Researcher"=>10, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>8, "Other"=>2, "Student > Bachelor"=>4, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>2, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>37}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>37}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Czech Republic"=>1, "United Kingdom"=>1, "India"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1404928", "https://ndownloader.figshare.com/files/1404929", "https://ndownloader.figshare.com/files/1404930", "https://ndownloader.figshare.com/files/1404931", "https://ndownloader.figshare.com/files/1404932", "https://ndownloader.figshare.com/files/1404933", "https://ndownloader.figshare.com/files/1404934", "https://ndownloader.figshare.com/files/1404935", "https://ndownloader.figshare.com/files/1404936", "https://ndownloader.figshare.com/files/1404938", "https://ndownloader.figshare.com/files/1404939", "https://ndownloader.figshare.com/files/1404940", "https://ndownloader.figshare.com/files/1404941", "https://ndownloader.figshare.com/files/1404942"], "description"=>"<div><p>Toll-like receptors (TLRs) are a family of conserved pattern-recognition molecules responsible for initiating innate and acquired immune responses. Because they play a key role in host defence, these genes have received increasing interest in the evolutionary and population genetics literature, as their variation represents a potential target of adaptive evolution. However, the role of pathogen-mediated selection (i.e. episodic positive selection) in the evolution of these genes remains poorly known and has not been examined outside of mammals. A recent increase in the number of bird species for which TLR sequences are available has enabled us to examine the selective processes that have influenced evolution of the 10 known avian TLR genes. Specifically, we tested for episodic positive selection to identify codons that experience purifying selection for the majority of their evolution, interspersed with bursts of positive selection that may occur only in restricted lineages. We included up to 23 species per gene (mean = 16.0) and observed that, although purifying selection was evident, an average of 4.5% of codons experienced episodic positive selection across all loci. For four genes in which sequence coverage traversed both the extracellular leucine-rich repeat region (LRR) and transmembrane/intracellular domains of the proteins, increased positive selection was observed at the extracellular domain, consistent with theoretical predictions. Our results provide evidence that episodic positive selection has played an important role in the evolution of most avian TLRs, consistent with the role of these loci in pathogen recognition and a mechanism of host-pathogen coevolution.</p></div>", "links"=>[], "tags"=>["Evolutionary biology", "Evolutionary processes", "Evolutionary selection", "Evolutionary genetics", "Evolutionary immunology", "genetics", "Animal genetics", "immunology", "immunity", "Innate immunity", "Genetics of the immune system", "Zoology", "Ornithology", "avian", "toll-like", "receptor", "innate"], "article_id"=>949787, "categories"=>["Biological Sciences"], "users"=>["Catherine E. Grueber", "Graham P. Wallis", "Ian G. Jamieson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0089632.s001", "https://dx.doi.org/10.1371/journal.pone.0089632.s002", "https://dx.doi.org/10.1371/journal.pone.0089632.s003", "https://dx.doi.org/10.1371/journal.pone.0089632.s004", "https://dx.doi.org/10.1371/journal.pone.0089632.s005", "https://dx.doi.org/10.1371/journal.pone.0089632.s006", "https://dx.doi.org/10.1371/journal.pone.0089632.s007", "https://dx.doi.org/10.1371/journal.pone.0089632.s008", "https://dx.doi.org/10.1371/journal.pone.0089632.s009", "https://dx.doi.org/10.1371/journal.pone.0089632.s010", "https://dx.doi.org/10.1371/journal.pone.0089632.s011", "https://dx.doi.org/10.1371/journal.pone.0089632.s012", "https://dx.doi.org/10.1371/journal.pone.0089632.s013", "https://dx.doi.org/10.1371/journal.pone.0089632.s014"], "stats"=>{"downloads"=>14, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Episodic_Positive_Selection_in_the_Evolution_of_Avian_Toll_Like_Receptor_Innate_Immunity_Genes_/949787", "title"=>"Episodic Positive Selection in the Evolution of Avian Toll-Like Receptor Innate Immunity Genes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-03-03 02:45:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1404902"], "description"=>"<p>In A, filled circles indicate the mean <i>d<sub>N</sub></i>-<i>d<sub>S</sub></i> values (estimated using the SLAC method) of codons located in LRR domains, while open circles indicate the mean values of all other codons; error bars indicate the standard error; numbers of codons assayed in each region are shown along <i>x</i>-axis. Panel B shows the proportion of statistically significant results for codons under positive selection (as determined by the SLAC or REL methods, circles on left, hits at the same site from multiple methods were counted separately) or episodic diversifying selection (as determined by the MEME method, diamonds on right), that fell within LRR domains of each toll-like receptor gene. Crosses indicate the proportion of results expected to fall within LRR domains under the null hypothesis, given the number of genotyped codons in those regions. Total numbers of significant findings by each method are shown along the <i>x</i>-axis; error bars are 95% confidence intervals for binomial proportions (see Methods).</p>", "links"=>[], "tags"=>["Evolutionary biology", "Evolutionary processes", "Evolutionary selection", "Evolutionary genetics", "Evolutionary immunology", "genetics", "Animal genetics", "immunology", "immunity", "Innate immunity", "Genetics of the immune system", "Zoology", "Ornithology", "lrr", "domains", "tlr", "genes"], "article_id"=>949767, "categories"=>["Biological Sciences"], "users"=>["Catherine E. Grueber", "Graham P. Wallis", "Ian G. Jamieson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089632.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differences_in_selection_across_LRR_and_other_domains_of_four_TLR_genes_in_birds_/949767", "title"=>"Differences in selection across LRR and other domains of four TLR genes in birds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-03 02:45:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1404903"], "description"=>"<p>NOTE. <b>bp</b> base-pairs, <b>aa</b> amino acids, <b><i>d<sub>N</sub></i></b> (number of non-synonymous substitutions per non-synonymous site) and <b><i>d<sub>S</sub></i></b> (number of synonymous substitutions per synonymous site) were estimated using the modified Nei-Gojobori/Jukes-Cantor method <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632-Nei1\" target=\"_blank\">[61]</a>, <b>SE</b> of <i>d<sub>N</sub></i> and <i>d<sub>S</sub></i> were estimated using 500 bootstrap iterations in MEGA, <b><i>d<sub>N</sub></i></b><b>/</b><b><i>d<sub>S</sub></i></b> was estimated using the SLAC method implemented in datamonkey,</p><p>* “Either” indicates the number (and percentage) of codons at which selection was detected with either the SLAC or REL methods.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Evolutionary processes", "Evolutionary selection", "Evolutionary genetics", "Evolutionary immunology", "genetics", "Animal genetics", "immunology", "immunity", "Innate immunity", "Genetics of the immune system", "Zoology", "Ornithology", "avian", "tlr"], "article_id"=>949768, "categories"=>["Biological Sciences"], "users"=>["Catherine E. Grueber", "Graham P. Wallis", "Ian G. Jamieson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089632.t001", "stats"=>{"downloads"=>4, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Selection_and_diversity_statistics_for_ten_avian_TLR_alignments_/949768", "title"=>"Selection and diversity statistics for ten avian TLR alignments.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-03-03 02:45:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1404901"], "description"=>"<p>The analysed region of each gene is positioned on an <i>x</i>-axis aligned with chicken TLRs. Within each panel of the figure, vertical black lines indicate the degree of positive (<i>d<sub>N</sub></i>-<i>d<sub>S</sub></i>>0) or negative (<i>d<sub>N</sub></i>-<i>d<sub>S</sub></i><0) selection at each codon site. Note that the <i>y</i>-axes vary in scale. Panel backgrounds are shaded to illustrate locations of conserved domains within the alignment region (based on LRRfinder <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632-Offord1\" target=\"_blank\">[43]</a>) (pink = signal domain; light green = extracellular LRR regions; dark green = C-terminal LRR regions; cyan = transmembrane domain; orange = TIR). Within each panel, three rows of symbols indicate codons for which statistically significant evidence of selection was detected: the top row of symbols (circles) indicates codons under positive selection in the current study, using either the SLAC or REL methods, larger symbols are used where the two methods correspond. The second row of symbols (triangles) indicates codons detected in the current study as being under episodic diversifying selection, using the MEME analysis. The third row of symbols (asterisks) indicates sites previously observed to be under positive selection in a smaller avian alignment of the same regions <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632-Alcaide1\" target=\"_blank\">[17]</a> using either the SLAC or REL methods, larger symbols indicate codons in which the two methods correspond.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Evolutionary processes", "Evolutionary selection", "Evolutionary genetics", "Evolutionary immunology", "genetics", "Animal genetics", "immunology", "immunity", "Innate immunity", "Genetics of the immune system", "Zoology", "Ornithology", "nucleotide", "substitution", "patterns", "toll-like", "receptor", "loci"], "article_id"=>949766, "categories"=>["Biological Sciences"], "users"=>["Catherine E. Grueber", "Graham P. Wallis", "Ian G. Jamieson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089632.g003", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Map_of_nucleotide_substitution_patterns_at_Toll_like_receptor_loci_in_birds_/949766", "title"=>"Map of nucleotide substitution patterns at Toll-like receptor loci in birds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-03 02:45:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1404898"], "description"=>"<p>Frequency with which each amino-acid substitution type (<i>N</i> = 190 possible substitutions) was observed, relative to their predicted physicochemical distances <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632-Grantham1\" target=\"_blank\">[42]</a> (A). The number of amino acid substitution types (<i>N</i> = 190) that were observed at least once in each of 10 avian TLR loci, as a function of the number of alignments in which each type was observed (B).</p>", "links"=>[], "tags"=>["Evolutionary biology", "Evolutionary processes", "Evolutionary selection", "Evolutionary genetics", "Evolutionary immunology", "genetics", "Animal genetics", "immunology", "immunity", "Innate immunity", "Genetics of the immune system", "Zoology", "Ornithology", "substitutions", "occurring", "toll-like", "receptor", "loci"], "article_id"=>949763, "categories"=>["Biological Sciences"], "users"=>["Catherine E. Grueber", "Graham P. Wallis", "Ian G. Jamieson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089632.g001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characteristics_of_substitutions_occurring_in_ten_Toll_like_receptor_loci_in_birds_/949763", "title"=>"Characteristics of substitutions occurring in ten Toll-like receptor loci in birds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-03 02:45:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1404900"], "description"=>"<p>Positively selected sites were determined by MEME analysis; trees are available in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632.s005\" target=\"_blank\">Figure S1</a>. Points indicate observed proportions; error bars are Agresti-Coull binomial 95% confidence intervals <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632-Agresti1\" target=\"_blank\">[44]</a> calculated using the R package “binom” <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632-Sundar1\" target=\"_blank\">[45]</a>. Crosses indicate the proportion expected under a null hypothesis of random distribution, based on the sum of internal/terminal branch lengths. Values along the <i>x</i>-axis are sample sizes of mapped MEME results; note that these values can be larger than those presented in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone-0089632-t001\" target=\"_blank\">Table 1</a>, as some sites are selected on multiple branches, while not all sites under selection were mapped to specific branches (i.e. they showed pervasive selection) (see also <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089632#pone.0089632.s009\" target=\"_blank\">Figure S5</a>).</p>", "links"=>[], "tags"=>["Evolutionary biology", "Evolutionary processes", "Evolutionary selection", "Evolutionary genetics", "Evolutionary immunology", "genetics", "Animal genetics", "immunology", "immunity", "Innate immunity", "Genetics of the immune system", "Zoology", "Ornithology", "positively", "sites", "terminal", "branches"], "article_id"=>949765, "categories"=>["Biological Sciences"], "users"=>["Catherine E. Grueber", "Graham P. Wallis", "Ian G. Jamieson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089632.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proportion_of_positively_selected_sites_detected_on_internal_or_terminal_branches_of_each_gene_tree_/949765", "title"=>"Proportion of positively selected sites detected on internal or terminal branches of each gene tree.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-03 02:45:48"}

PMC Usage Stats | Further Information

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Relative Metric

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