Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies
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{"title"=>"Genetic evidence for hybrid trait speciation in Heliconius butterflies", "type"=>"journal", "authors"=>[{"first_name"=>"Camilo", "last_name"=>"Salazar", "scopus_author_id"=>"8283928400"}, {"first_name"=>"Simon W.", "last_name"=>"Baxter", "scopus_author_id"=>"8600199700"}, {"first_name"=>"Carolina", "last_name"=>"Pardo-Diaz", "scopus_author_id"=>"36178306900"}, {"first_name"=>"Grace", "last_name"=>"Wu", "scopus_author_id"=>"56520658700"}, {"first_name"=>"Alison", "last_name"=>"Surridge", "scopus_author_id"=>"7004132948"}, {"first_name"=>"Mauricio", "last_name"=>"Linares", "scopus_author_id"=>"7005524905"}, {"first_name"=>"Eldredge", "last_name"=>"Bermingham", "scopus_author_id"=>"36938170900"}, {"first_name"=>"Chris D.", "last_name"=>"Jiggins", "scopus_author_id"=>"6603932806"}], "year"=>2010, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"358837575", "issn"=>"15537390", "isbn"=>"1553-7390", "doi"=>"10.1371/journal.pgen.1000930", "scopus"=>"2-s2.0-77952376744", "pmid"=>"20442862", "sgr"=>"77952376744"}, "id"=>"67e7c1fa-528b-38cd-a8d7-68f4cce7915a", "abstract"=>"Homoploid hybrid speciation is the formation of a new hybrid species without change in chromosome number. So far, there has been a lack of direct molecular evidence for hybridization generating novel traits directly involved in animal speciation. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has been proposed as a hybrid species, and its color pattern can be recreated by introgression of the H. m. melpomene red band into the genetic background of the yellow banded H. cydno cordula. This hybrid color pattern is also involved in mate choice and leads to reproductive isolation between H. heurippa and its close relatives. Here, we provide molecular evidence for adaptive introgression by sequencing genes across the Heliconius red band locus and comparing them to unlinked wing patterning genes in H. melpomene, H. cydno, and H. heurippa. 670 SNPs distributed among 29 unlinked coding genes (25,847bp) showed H. heurippa was related to H. c. cordula or the three species were intermixed. In contrast, among 344 SNPs distributed among 13 genes in the red band region (18,629bp), most showed H. heurippa related with H. c. cordula, but a block of around 6,5kb located in the 3' of a putative kinesin gene grouped H. heurippa with H. m. melpomene, supporting the hybrid introgression hypothesis. Genealogical reconstruction showed that this introgression occurred after divergence of the parental species, perhaps around 0.43Mya. Expression of the kinesin gene is spatially restricted to the distal region of the forewing, suggesting a mechanism for pattern regulation. This gene therefore constitutes the first molecular evidence for adaptive introgression during hybrid speciation and is the first clear candidate for a Heliconius wing patterning locus.", "link"=>"http://www.mendeley.com/research/genetic-evidence-hybrid-trait-speciation-heliconius-butterflies", "reader_count"=>141, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>10, "Researcher"=>37, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>36, "Student > Postgraduate"=>10, "Student > Master"=>20, "Other"=>2, "Student > Bachelor"=>13, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>10, "Researcher"=>37, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>36, "Student > Postgraduate"=>10, "Student > Master"=>20, "Other"=>2, "Student > Bachelor"=>13, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>126, "Chemical Engineering"=>1, "Physics and Astronomy"=>2}, "reader_count_by_subdiscipline"=>{"Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>126}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>2}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"Austria"=>1, "Netherlands"=>1, "United States"=>6, "Brazil"=>2, "Poland"=>1, "United Kingdom"=>3, "Mexico"=>1, "Portugal"=>1, "India"=>1, "Russia"=>1}, "group_count"=>5}

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  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/423875/Figure_S1.pdf", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/423912/Figure_S2.pdf", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/423941/Figure_S3.pdf", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/423965/Table_S1.doc", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/423987/Table_S2.doc"], "description"=>"<div><p>Homoploid hybrid speciation is the formation of a new hybrid species without change in chromosome number. So far, there has been a lack of direct molecular evidence for hybridization generating novel traits directly involved in animal speciation. <em>Heliconius</em> butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. <em>Heliconius heurippa</em> has been proposed as a hybrid species, and its color pattern can be recreated by introgression of the <em>H. m. melpomene</em> red band into the genetic background of the yellow banded <em>H. cydno cordula</em>. This hybrid color pattern is also involved in mate choice and leads to reproductive isolation between <em>H. heurippa</em> and its close relatives. Here, we provide molecular evidence for adaptive introgression by sequencing genes across the <em>Heliconius</em> red band locus and comparing them to unlinked wing patterning genes in <em>H. melpomene</em>, <em>H. cydno</em>, and <em>H. heurippa</em>. 670 SNPs distributed among 29 unlinked coding genes (25,847bp) showed <em>H. heurippa</em> was related to <em>H. c. cordula</em> or the three species were intermixed. In contrast, among 344 SNPs distributed among 13 genes in the red band region (18,629bp), most showed <em>H. heurippa</em> related with <em>H. c. cordula</em>, but a block of around 6,5kb located in the 3′ of a putative <em>kinesin</em> gene grouped <em>H. heurippa</em> with <em>H. m. melpomene</em>, supporting the hybrid introgression hypothesis. Genealogical reconstruction showed that this introgression occurred after divergence of the parental species, perhaps around 0.43Mya. Expression of the <em>kinesin</em> gene is spatially restricted to the distal region of the forewing, suggesting a mechanism for pattern regulation. This gene therefore constitutes the first molecular evidence for adaptive introgression during hybrid speciation and is the first clear candidate for a <em>Heliconius</em> wing patterning locus.</p></div>", "links"=>[], "tags"=>["hybrid", "speciation", "butterflies"], "article_id"=>143684, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/Genetic_Evidence_for_Hybrid_Trait_Speciation_in_Heliconius_Butterflies/143684", "title"=>"Genetic Evidence for Hybrid Trait Speciation in <em>Heliconius</em> Butterflies", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-04-29 01:01:24"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/851783/Figure_1.tif"], "description"=>"<p>Likelihood values are plotted for each variable position, where positive likelihood values indicate a SNP position at which <i>H. heurippa</i> and <i>H. m. melpomene</i> are more similar, and negative values a position at which <i>H. heurippa</i> shows a stronger association with <i>H. c. cordula</i>. Fixed sites are indicated by dotted lines showing a likelihood value of 244 for a complete association of <i>H. heurippa</i> with <i>H. m. melpomene</i> and −244 for that with <i>H. c. cordula</i>. Colors represent different coding regions. The majority of unlinked SNPs (634) show shared polymorphism among the three species (240> ΔLnL >−240). At unlinked loci, <i>H. heurippa</i> and <i>H. c. cordula</i> shared fixed polymorphism at only 8 SNPs whereas <i>H. heurippa</i> and <i>H. m. melpomene</i> did not share any fixed polymorphism. For the <i>HmB</i> locus, sequenced BAC clones are indicated above the gene annotation <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000930#pgen.1000930-Baxter2\" target=\"_blank\">[41]</a>.</p>", "links"=>[], "tags"=>["genes", "unlinked"], "article_id"=>522235, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Relative_likelihood_of_association_between_H_heurippa_and_H_m_melpomene_versus_H_c_cordula_for_A_genes_unlinked_to_color_pattern_and_B_across_the_HmB_red_color_pattern_locus_/522235", "title"=>"Relative likelihood of association between <i>H. heurippa</i> and <i>H. m. melpomene</i> versus <i>H. c. cordula</i> for (A) genes unlinked to color pattern and (B) across the <i>HmB</i> red color pattern locus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-29 00:37:15"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/851888/Figure_2.tif"], "description"=>"<p>The average of likelihood values for each unlinked marker and for 1,000 bp windows in the <i>HmB</i> region was calculated. This histogram shows the distribution of these values. Dotted lines represent the 95% two-tailed interval for unlinked genes. The asterisk over the bars indicates those 1,000 bp windows showing average values that lie outside the unlinked genes distribution (p<0,005). Positive values outside that distribution correspond to <i>3′ kinesin</i> whereas negative values are those in <i>kin_2</i>.</p>", "links"=>[], "tags"=>["snps", "unlinked", "linked"], "article_id"=>522343, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Distribution_of_average_likelihood_values_at_SNPs_in_unlinked_and_HmB_linked_loci_/522343", "title"=>"Distribution of average likelihood values at SNPs in unlinked and <i>HmB</i> linked loci.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-29 00:39:03"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/852026/Figure_3.tif"], "description"=>"<p>Pairwise estimates of linkage disequilibrium (r<sup>2</sup>) among 199 SNPs in the <i>HmB</i> locus (those with a rare allele frequency less than 10% were excluded) for combined <i>H. c. cordula</i> and <i>H. heurippa</i> population samples. Physical distance between sites is shown in the adjacent map.</p>", "links"=>[], "tags"=>["linkage", "disequilibrium"], "article_id"=>522477, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_HmB_linkage_disequilibrium_analysis_/522477", "title"=>"<i>HmB</i> linkage disequilibrium analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-29 00:41:17"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/852167/Figure_4.tif"], "description"=>"<p>(A) sorting nexin (sdp); (B) 3′ <i>kinesin</i>; and (C) 5′ <i>kinesin</i> partial sequence (<i>kin</i>_2). Filled color circles represent alleles of each species. The 3′ <i>kinesin</i> tree is rooted with <i>H. numata</i> as outgroup (black). Numbers above and below the branches are bootstrap support values for likelihood and parsimony analyses respectively. (B) shows <i>H. heurippa</i> most closely related <i>to H. m. melpomene</i>, while (A,C), the genomic regions surrounding 3′ <i>kinesin</i>, show <i>H. heurippa</i> alleles more closely related to <i>H. c. cordula</i>. A similar tree topology was obtained from an amino acid alignment (data not shown).</p>", "links"=>[], "tags"=>["genealogies", "flanking"], "article_id"=>522620, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Gene_genealogies_for_3_kinesin_and_its_flanking_regions_/522620", "title"=>"Gene genealogies for 3′ <i>kinesin</i> and its flanking regions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-29 00:43:40"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/852275/Figure_5.tif"], "description"=>"<p>Of (A) <i>H. m. cythera</i> and (B) <i>H. cydno</i>. A similar expression pattern to that present in (A) is also observed in <i>H. m. rosina</i> forewings (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000930#pgen.1000930.s003\" target=\"_blank\">Figure S3</a>), consistent with the red band phenotype of these two races. The lack of any localized <i>kinesin</i> expression in <i>H. cydno</i> forewings is consistent with the absence of a red band in this species. (C) Model of how <i>kinesin</i> expression (K, solid line), might interact with an unknown gene (X, dotted line) to regulate forewing red band expression.</p>", "links"=>[], "tags"=>["Evolutionary biology", "evolutionary biology/animal genetics"], "article_id"=>522731, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Expression_pattern_of_kinesin_in_forewings_/522731", "title"=>"Expression pattern of <i>kinesin</i> in forewings.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-29 00:45:31"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/852365/Table_1.xls"], "description"=>"*<p>s indicate significance: * p<0.05; n.a.: not applicable due to lack of polymorphism.</p>‡<p><i>Kin 3′</i> includes amplicons <i>Kin 8</i> to <i>Kin 14</i>. Haplotype numbers were determined over 20 sequences per species.</p>", "links"=>[], "tags"=>["nucleotide"], "article_id"=>522819, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Species_nucleotide_diversity_for_each_locus_/522819", "title"=>"Species nucleotide diversity for each locus.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-04-29 00:46:59"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/852408/Table_2.xls"], "description"=>"<p><b>c:</b><i>H. c cordula</i>; <b>m:</b><i>H. m. melpomene</i>; <b>h:</b><i>H. heurippa</i>.</p>‡<p><i>Kin 3′</i> includes amplions <i>Kin 8</i> to <i>Kin 14</i>.</p>", "links"=>[], "tags"=>["divergence"], "article_id"=>522861, "categories"=>["Evolutionary Biology"], "users"=>["Camilo Salazar", "Simon W. Baxter", "Carolina Pardo-Diaz", "Grace Wu", "Alison Surridge", "Mauricio Linares", "Eldredge Bermingham", "Chris D. Jiggins"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1000930.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Net_divergence_among_populations_/522861", "title"=>"Net divergence among populations.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-04-29 00:47:41"}

PMC Usage Stats | Further Information

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