Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in Heliconius erato
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{"title"=>"Genomic hotspots for adaptation: The population genetics of Müllerian mimicry in Heliconius erato", "type"=>"journal", "authors"=>[{"first_name"=>"Brian A.", "last_name"=>"Counterman", "scopus_author_id"=>"6506288862"}, {"first_name"=>"Felix", "last_name"=>"Araujo-Perez", "scopus_author_id"=>"35726533300"}, {"first_name"=>"Heather M.", "last_name"=>"Hines", "scopus_author_id"=>"10438960900"}, {"first_name"=>"Simon W.", "last_name"=>"Baxter", "scopus_author_id"=>"8600199700"}, {"first_name"=>"Clay M.", "last_name"=>"Morrison", "scopus_author_id"=>"14822302700"}, {"first_name"=>"Daniel P.", "last_name"=>"Lindstrom", "scopus_author_id"=>"35788851400"}, {"first_name"=>"Riccardo", "last_name"=>"Papa", "scopus_author_id"=>"7004930189"}, {"first_name"=>"Laura", "last_name"=>"Ferguson", "scopus_author_id"=>"24576541600"}, {"first_name"=>"Mathieu", "last_name"=>"Joron", "scopus_author_id"=>"6602305237"}, {"first_name"=>"Richard H.", "last_name"=>"Ffrench-Constant", "scopus_author_id"=>"34975054200"}, {"first_name"=>"Christopher P.", "last_name"=>"Smith", "scopus_author_id"=>"16550560400"}, {"first_name"=>"Dahlia M.", "last_name"=>"Nielsen", "scopus_author_id"=>"7202174007"}, {"first_name"=>"Rui", "last_name"=>"Chen", "scopus_author_id"=>"55650841700"}, {"first_name"=>"Chris D.", "last_name"=>"Jiggins", "scopus_author_id"=>"6603932806"}, {"first_name"=>"Robert D.", "last_name"=>"Reed", "scopus_author_id"=>"7401921567"}, {"first_name"=>"Georg", "last_name"=>"Halder", "scopus_author_id"=>"6701435991"}, {"first_name"=>"Jim", "last_name"=>"Mallet", "scopus_author_id"=>"7202284097"}, {"first_name"=>"W. Owen", "last_name"=>"McMillan", "scopus_author_id"=>"7004840804"}], "year"=>2010, "source"=>"PLoS Genetics", "identifiers"=>{"pmid"=>"20140188", "issn"=>"15537390", "doi"=>"10.1371/journal.pgen.1000796", "pui"=>"358392143", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "scopus"=>"2-s2.0-77649259742", "sgr"=>"77649259742"}, "id"=>"880d29ef-056d-3f60-953f-2aeb485e90d6", "abstract"=>"Wing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are \"hotspots\" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by approximately 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.", "link"=>"http://www.mendeley.com/research/genomic-hotspots-adaptation-population-genetics-m%C3%BCllerian-mimicry-heliconius-erato", "reader_count"=>246, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>26, "Researcher"=>59, "Student > Doctoral Student"=>11, "Student > Ph. D. 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  • {"files"=>["https://ndownloader.figshare.com/files/864103"], "description"=>"<p>Individual BAC clones tiling across the color pattern intervals are represented by horizontal shaded bars, with clone name provided directly below. Black horizontal bar above BAC tile path represents consensus sequence assembled from overlapping BACs. Slashes indicate gaps in the consensus sequence across the interval. There were two small gaps (≈10kb between <i>H. erato</i> clone 33L14 and 18A1 and ≈5kb between 38G06 and 47M12) and one large gap (≈250 kb) in our assembly based on comparisons to <i>Bombyx mori</i> and <i>H. melpomene</i>. For the <i>Cr</i> interval, the grey horizontal bar extending to the right of the black horizontal bar represents a region with no available information on recombination. Vertical white markers denote approximate positions of genetic markers used for brood mapping, with marker names stated directly above. Below each marker is the number of individuals showing a recombination event between the genetic marker and color pattern phenotype over the total number of individuals genotyped. For the <i>D</i> locus, four phenotypically distinct races of <i>H. erato</i> were used for fine mapping in crosses with <i>H. himera </i><a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000796#pgen.1000796-Kapan2\" target=\"_blank\">[39]</a>,<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000796#pgen.1000796-Tobler2\" target=\"_blank\">[100]</a>,and the results for each race are provided separately. Genetic markers designated NA were either not polymorphic or could not be reliably scored in the corresponding crosses. Shaded areas denote approximate locations of ‘zero recombinant intervals’.</p>", "links"=>[], "tags"=>["paths"], "article_id"=>534537, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000796.g002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BAC_tile_paths_and_fine_mapping_across_the_D_and_Cr_color_pattern_intervals_/534537", "title"=>"BAC tile paths and fine mapping across the <i>D</i> and <i>Cr</i> color pattern intervals.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:15:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/864380"], "description"=>"<p>Plot of genotype-phenotype associations (black circles) and population differentiation (red squares) across the <i>D</i>, <i>Cr</i> and unlinked intervals. The left axis is the strength of associations (log<sub>10</sub> of the probability of a genotype-by-phenotype association) between genotypes and color patterns. The right axis measures degree of population differentiation, measured as <i>F<sub>ST</sub></i>, between <i>H. e. favorinus</i> and <i>H. e. emma</i>. Distance across the genomic intervals is in kilobases. Points above the horizontal show a significant genotype-by-phenotype association using a bonferroni correction to adjust for multiple tests (<i>α</i> = 0.05, <i>n</i> = 432).</p>", "links"=>[], "tags"=>["sites", "coding", "regions"], "article_id"=>534790, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000796.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Several_sites_in_multiple_coding_regions_are_associated_with_the_transition_in_D_and_Cr_color_patterns_/534790", "title"=>"Several sites in multiple coding regions are associated with the transition in <i>D</i> and <i>Cr</i> color patterns.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:19:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/864662"], "description"=>"<p>Estimates of genetic diversity across the <i>H. erato</i> hybrid zone.</p>", "links"=>[], "tags"=>["hybrid"], "article_id"=>535092, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000796.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimates_of_genetic_diversity_across_the_H_erato_hybrid_zone_/535092", "title"=>"Estimates of genetic diversity across the <i>H. erato</i> hybrid zone.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-02-05 01:24:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/864598"], "description"=>"<p>High genetic differentiation near color pattern loci.</p>", "links"=>[], "tags"=>["differentiation"], "article_id"=>535025, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000796.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_High_genetic_differentiation_near_color_pattern_loci_/535025", "title"=>"High genetic differentiation near color pattern loci.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-02-05 01:23:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/429009", "https://ndownloader.figshare.com/files/429044", "https://ndownloader.figshare.com/files/429114", "https://ndownloader.figshare.com/files/429165", "https://ndownloader.figshare.com/files/429196", "https://ndownloader.figshare.com/files/429235"], "description"=>"<div><p>Wing pattern evolution in <em>Heliconius</em> butterflies provides some of the most striking examples of adaptation by natural selection. The genes controlling pattern variation are classic examples of Mendelian loci of large effect, where allelic variation causes large and discrete phenotypic changes and is responsible for both <em>convergent</em> and <em>highly divergent</em> wing pattern evolution across the genus. We characterize nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium (LD), and candidate gene expression patterns across two unlinked genomic intervals that control yellow and red wing pattern variation among mimetic forms of <em>Heliconius erato</em>. Despite very strong natural selection on color pattern, we see neither a strong reduction in genetic diversity nor evidence for extended LD across either patterning interval. This observation highlights the extent that recombination can erase the signature of selection in natural populations and is consistent with the hypothesis that either the adaptive radiation or the alleles controlling it are quite old. However, across both patterning intervals we identified SNPs clustered in several coding regions that were strongly associated with color pattern phenotype. Interestingly, coding regions with associated SNPs were widely separated, suggesting that color pattern alleles may be composed of multiple functional sites, conforming to previous descriptions of these loci as “supergenes.” Examination of gene expression levels of genes flanking these regions in both <em>H. erato</em> and its co-mimic, <em>H. melpomene</em>, implicate a gene with high sequence similarity to a kinesin as playing a key role in modulating pattern and provides convincing evidence for parallel changes in gene regulation across co-mimetic lineages. The complex genetic architecture at these color pattern loci stands in marked contrast to the single casual mutations often identified in genetic studies of adaptation, but may be more indicative of the type of genetic changes responsible for much of the adaptive variation found in natural populations.</p></div>", "links"=>[], "tags"=>["genomic", "hotspots", "genetics", "mimicry"], "article_id"=>144706, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000796.s001", "https://dx.doi.org/10.1371/journal.pgen.1000796.s002", "https://dx.doi.org/10.1371/journal.pgen.1000796.s003", "https://dx.doi.org/10.1371/journal.pgen.1000796.s004", "https://dx.doi.org/10.1371/journal.pgen.1000796.s005", "https://dx.doi.org/10.1371/journal.pgen.1000796.s006"], "stats"=>{"downloads"=>25, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Genomic_Hotspots_for_Adaptation_The_Population_Genetics_of_M_llerian_Mimicry_in_Heliconius_erato_/144706", "title"=>"Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in <em>Heliconius erato</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-02-05 01:18:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/863950"], "description"=>"<p>Geographic representation of the five locations where <i>H. erato</i> was sampled across the Eastern Peruvian hybrid zone. Dotted line is approximate location of the Tarapoto-Yurimaguas road that transects the hybrid zone and was used for sampling. The <i>D</i> locus affects the presence of the proximal red patch (“dennis”), red hindwing rays and the forewing band color. The <i>Cr</i> locus is responsible for the presence of the hindwing yellow bar and interacts with the <i>Sd</i> locus to affect the shape of the forewing band and hindwing bar.</p>", "links"=>[], "tags"=>["sites"], "article_id"=>534382, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000796.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sampling_sites_across_the_transition_between_H_e_favorinus_and_H_e_emma_/534382", "title"=>"Sampling sites across the transition between <i>H. e. favorinus</i> and <i>H. e. emma</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:13:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/864493"], "description"=>"<p>Quantitative PCR data for five candidate genes in the <i>D</i>-interval. Y-axis values are Log<sub>2</sub> transformed values of the initial concentration of the gene divided by the EF-1α initial concentration; developmental stage is displayed on the X axis, including 5<sup>th</sup> instar larvae and pupal developmental days 1, 3, and 5. Bars represent standard error among the biological replicates.</p>", "links"=>[], "tags"=>["pcr", "genes", "implicates"], "article_id"=>534905, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000796.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantitative_PCR_of_D_interval_candidate_genes_implicates_kinesin_/534905", "title"=>"Quantitative PCR of <i>D</i>-interval candidate genes implicates <i>kinesin</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:21:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/864228"], "description"=>"<p>Correlation matrix of composite LD estimates among SNPs from the 22 coding regions sampled across the <i>D</i> and <i>Cr</i> intervals using all 76 individuals. SNPs are concatenated by their position along the <i>D</i> and <i>Cr</i> intervals. The upper left matrix shows LD between the 401 SNPs sampled across the <i>D</i> and <i>Cr</i> intervals. The lower right matrix only shows SNPs from the <i>D</i> and <i>Cr</i> intervals that are strongly associated with wing color pattern.</p>", "links"=>[], "tags"=>["ld", "snps", "intervals", "peruvian", "hybrid"], "article_id"=>534646, "categories"=>["Evolutionary Biology", "Genetics"], "users"=>["Brian A. Counterman", "Félix Araújo-Pérez", "Heather M. Hines", "Simon W. Baxter", "Clay M. Morrison", "Daniel P. Lindstrom", "Riccardo Papa", "Laura Ferguson", "Mathieu Joron", "Richard H. ffrench-Constant", "Christopher P. Smith", "Dahlia M. Nielsen", "Rui Chen", "Chris D. Jiggins", "Robert D. Reed", "Georg Halder", "Jim Mallet", "W. Owen McMillan"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000796.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lack_of_LD_between_SNPs_across_the_D_and_Cr_intervals_in_the_Peruvian_hybrid_zone_/534646", "title"=>"Lack of LD between SNPs across the <i>D</i> and <i>Cr</i> intervals in the Peruvian hybrid zone.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-02-05 01:17:26"}

PMC Usage Stats | Further Information

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Relative Metric

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