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{"title"=>"Phylogenetic codivergence supports coevolution of mimetic Heliconius butterflies", "type"=>"journal", "authors"=>[{"first_name"=>"Jennifer", "last_name"=>"Hoyal Cuthill", "scopus_author_id"=>"55208132700"}, {"first_name"=>"Michael", "last_name"=>"Charleston", "scopus_author_id"=>"55911425300"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"22586474", "doi"=>"10.1371/journal.pone.0036464", "sgr"=>"84860628141", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-84860628141", "issn"=>"19326203", "pui"=>"364751076"}, "id"=>"6d4b246c-75ca-32a9-88f7-4b61aed3a979", "abstract"=>"The unpalatable and warning-patterned butterflies Heliconius erato and Heliconius melpomene provide the best studied example of mutualistic Mullerian mimicry, thought-but rarely demonstrated-to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of H. erato and H. melpomene, and this was initially hailed as one of the most striking known cases of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of H. erato and H. melpomene, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of H. erato and H. melpomene. Cophylogenetic historical reconstructions support repeated codivergence of mimetic populations, from the base of the sampled radiations. Pairwise distance correlation tests, based on our coalescent analyses plus recently published AFLP and wing colour pattern gene data, also suggest that the phylogenies of H. erato and H. melpomene show significant topological congruence. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of H. erato and H. melpomene occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. Our results suggest that differences in within-species genetic divergence are the result of a greater overall effective population size for H. erato relative to H. melpomene and do not imply incongruence in the timing of their phylogenetic radiations. Repeated codivergence between Mullerian co-mimics, predicted to exert mutual selection pressures, strongly suggests coevolution. Our results therefore support a history of reciprocal coevolution between Mullerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change.", "link"=>"http://www.mendeley.com/research/phylogenetic-codivergence-supports-coevolution-mimetic-heliconius-butterflies", "reader_count"=>84, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>3, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>4, "Student > Master"=>13, "Other"=>2, "Student > Bachelor"=>13, "Lecturer"=>3, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>3, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>4, "Student > Master"=>13, "Other"=>2, "Student > Bachelor"=>13, "Lecturer"=>3, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Mathematics"=>2, "Agricultural and Biological Sciences"=>65, "Computer Science"=>2, "Earth and Planetary Sciences"=>3}, "reader_count_by_subdiscipline"=>{"Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>65}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>2}}, "reader_count_by_country"=>{"Canada"=>1, "Argentina"=>1, "United States"=>5, "China"=>1, "Brazil"=>3, "Italy"=>1, "France"=>1, "Australia"=>1, "India"=>1}, "group_count"=>2}

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• http://doi.org/10.1111/mec.12844
• http://doi.org/10.1093/gbe/evz202
• http://doi.org/10.1073/pnas.1907068116
• http://doi.org/10.1093/cz/zow018
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• http://doi.org/10.1093/sysbio/syaa033
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• http://doi.org/10.1111/evo.12374
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• http://doi.org/10.1016/j.compbiolchem.2015.02.003
• http://doi.org/10.1093/molbev/msy209
• http://doi.org/10.1016/j.cois.2016.09.006
• http://doi.org/10.1186/1471-2105-15-S16-S14
• http://doi.org/10.1093/sysbio/syv007
• http://doi.org/10.1371/journal.pbio.3000597
• http://doi.org/10.1186/s13015-016-0077-5
• http://doi.org/10.1371/journal.pone.0057033
• http://doi.org/10.1080/23256214.2014.906070
• http://doi.org/10.1111/evo.12812
• http://doi.org/10.1111/nph.16176
• http://doi.org/10.1111/jeb.12672
• http://doi.org/10.1080/00222933.2019.1669730
• http://doi.org/10.1098/rspb.2012.2302

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• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/958f6b16-d656-496b-b16e-0e8b3dbdde49", "title"=>"Reference correction", "body"=>"Reference 3 should read: Sheppard PM, Turner JRG, Brown KS, Benson WW, Singer MC (1985) Genetics and the evolution of Muellerian mimicry in \"Heliconius\" butterflies. Phil Trans Roy Soc Lond 308: 433-613.", "highlightedText"=>"''[3]''\nhttp://plosone.org/article/info:doi/10.1371/journal.pone.0036464#article1.body1.sec1.p1", "isRemoved"=>false, "created"=>"2012-08-10T06:26:46Z", "lastModified"=>"2012-08-10T06:26:46Z", "creator"=>{"userId"=>"139265"}, "competingInterestStatement"=>{"creatorWasPrompted"=>true, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0036464", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2012-08-10T06:26:46Z", "replies"=>[]}

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• {"title"=>"Heliconius melpomene", "url"=>"http://en.wikipedia.org/wiki/Heliconius_melpomene", "timestamp"=>"2019-03-13T23:21:19Z"}

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• {"files"=>["https://ndownloader.figshare.com/files/641657"], "description"=>"<p>Example phylogenies independently estimated for <i>H. erato</i> (black, left) and <i>H. melpomene</i> (orange, right) using the Minimise Deep Coalescence (MDC) method <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Maddison1\" target=\"_blank\">[32]</a>. These correspond to cophylogenetic analysis “separate MDC countries 1” in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone-0036464-t001\" target=\"_blank\">Table 1</a>. <i>H. erato</i>/<i>H. melpomene</i> co-mimics (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone-0036464-g001\" target=\"_blank\">Figure 1</a>) are indicated by grey lines. This is one of several possible phylogeny pairs with similarly high congruence (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone-0036464-t001\" target=\"_blank\">Table 1</a>). Taxon labels indicate the sampled biogeographic region (East or West of the Andes), and country (abbreviations are: CR Costa Rica, Pa Panama, E Ecuador, C Colombia, FG French Guiana, T Trinidad and Pe Peru).</p>", "links"=>[], "tags"=>["illustrating", "branching", "orders", "co-mimetic", "populations"], "article_id"=>312147, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jennifer Hoyal Cuthill", "Michael Charleston"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036464.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenies_of_H_erato_and_H_melpomene_illustrating_branching_orders_of_co_mimetic_country_level_populations_within_each_species_/312147", "title"=>"Phylogenies of <i>H. erato</i> and <i>H. melpomene</i> illustrating branching orders of co-mimetic country level populations within each species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:35:47"}
• {"files"=>["https://ndownloader.figshare.com/files/331503", "https://ndownloader.figshare.com/files/331552", "https://ndownloader.figshare.com/files/331606", "https://ndownloader.figshare.com/files/331659", "https://ndownloader.figshare.com/files/331702", "https://ndownloader.figshare.com/files/331773", "https://ndownloader.figshare.com/files/331833", "https://ndownloader.figshare.com/files/331895", "https://ndownloader.figshare.com/files/331945", "https://ndownloader.figshare.com/files/331962", "https://ndownloader.figshare.com/files/332008"], "description"=>"<div><p>The unpalatable and warning-patterned butterflies <em>Heliconius erato</em> and <em>Heliconius melpomene</em> provide the best studied example of mutualistic Müllerian mimicry, thought–but rarely demonstrated–to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of <em>H. erato</em> and <em>H. melpomene</em>, and this was initially hailed as one of the most striking known cases of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of <em>H. erato</em> and <em>H. melpomene</em>, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of <em>H. erato</em> and <em>H. melpomene</em>. Cophylogenetic historical reconstructions support repeated codivergence of mimetic populations, from the base of the sampled radiations. Pairwise distance correlation tests, based on our coalescent analyses plus recently published AFLP and wing colour pattern gene data, also suggest that the phylogenies of <em>H. erato</em> and <em>H. melpomene</em> show significant topological congruence. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of <em>H. erato</em> and <em>H. melpomene</em> occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. Our results suggest that differences in within-species genetic divergence are the result of a greater overall effective population size for <em>H. erato</em> relative to <em>H. melpomene</em> and do not imply incongruence in the timing of their phylogenetic radiations. Repeated codivergence between Müllerian co-mimics, predicted to exert mutual selection pressures, strongly suggests coevolution. Our results therefore support a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change.</p> </div>", "links"=>[], "tags"=>["phylogenetic", "codivergence", "supports", "coevolution", "mimetic", "butterflies"], "article_id"=>125462, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jennifer Hoyal Cuthill", "Michael Charleston"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0036464.s001", "https://dx.doi.org/10.1371/journal.pone.0036464.s002", "https://dx.doi.org/10.1371/journal.pone.0036464.s003", "https://dx.doi.org/10.1371/journal.pone.0036464.s004", "https://dx.doi.org/10.1371/journal.pone.0036464.s005", "https://dx.doi.org/10.1371/journal.pone.0036464.s006", "https://dx.doi.org/10.1371/journal.pone.0036464.s007", "https://dx.doi.org/10.1371/journal.pone.0036464.s008", "https://dx.doi.org/10.1371/journal.pone.0036464.s009", "https://dx.doi.org/10.1371/journal.pone.0036464.s010", "https://dx.doi.org/10.1371/journal.pone.0036464.s011"], "stats"=>{"downloads"=>12, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Phylogenetic_Codivergence_Supports_Coevolution_of_Mimetic_Heliconius_Butterflies/125462", "title"=>"Phylogenetic Codivergence Supports Coevolution of Mimetic <em>Heliconius</em> Butterflies", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-05-07 01:31:02"}
• {"files"=>["https://ndownloader.figshare.com/files/641510"], "description"=>"<p>Mimetic morphs <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Sheppard1\" target=\"_blank\">[3]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Brower1\" target=\"_blank\">[15]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Quek1\" target=\"_blank\">[30]</a> (aligned rows), from <i>H. erato</i> (left) and <i>H. melpomene</i> (right), included in this study (photographs show the type specimens). Coloured boundaries on a satellite image of Central and South America indicate the geographic range of each morph <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Sheppard1\" target=\"_blank\">[3]</a>. Numbers indicate countries where morphs were sampled (by <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Flanagan1\" target=\"_blank\">[29]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Quek1\" target=\"_blank\">[30]</a>), West of the Andes: 1 Costa Rica, 2 Panama, 3 West Ecuador; East of the Andes: 4 Colombia, 5 French Guiana, 6 Trinidad, 7 Peru and 8 East Ecuador.</p>", "links"=>[], "tags"=>["patterns", "morphs", "geographic", "distributions", "co-mimics"], "article_id"=>312003, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jennifer Hoyal Cuthill", "Michael Charleston"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036464.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Wing_patterns_morphs_and_geographic_distributions_of_the_M_llerian_co_mimics_H_erato_and_H_melpomene_/312003", "title"=>"Wing patterns morphs and geographic distributions of the Müllerian co-mimics <i>H. erato</i> and <i>H. melpomene</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:33:23"}
• {"files"=>["https://ndownloader.figshare.com/files/641714"], "description"=>"<p>Example cophylogenetic history of the mimicry relationship between <i>H. erato</i> and <i>H. melpomene</i> based on MDC phylogenetic estimates (shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone-0036464-g002\" target=\"_blank\">Figure 2</a>), and reconstructed using TreeMap 3. Bars indicate 95% Bayesian confidence intervals for divergence times, corresponding to <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464.s001\" target=\"_blank\">Figure S1</a>. Grey-filled dots correspond to reconstructed codivergence events; white-filled dots represent duplication events which, in this case, are both followed by model switch events – one for the colonisation of <i>H. erato etylus</i> in East Ecuador by <i>H. melpomene ecuadoriensis</i>, here the sister to <i>H. melpomene malleti</i> (also from East Ecuador), the other for the colonisation of the <i>H. erato hydara</i> population from Trinidad by a population of <i>H. melpomene melpomene</i>, here the sister of a lineage from French Guiana (one of the sampled mainland countries closest to Trinidad); the only mimicry loss event is indicated at the most recent common ancestor of <i>H. erato hydara</i> populations from Trinidad and Panama. Taxon labels correspond to those in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone-0036464-g002\" target=\"_blank\">Figure 2</a>.</p>", "links"=>[], "tags"=>["reconstruction", "mimicry", "populations"], "article_id"=>312206, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jennifer Hoyal Cuthill", "Michael Charleston"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036464.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cophylogenetic_reconstruction_of_the_history_of_mimicry_between_country_level_populations_of_H_erato_and_H_melpomene_/312206", "title"=>"Cophylogenetic reconstruction of the history of mimicry between country level populations of <i>H. erato</i> and <i>H. melpomene</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:36:46"}
• {"files"=>["https://ndownloader.figshare.com/files/641780"], "description"=>"<p>Phylogenies were estimated separately for the clades of <i>H. erato</i> and <i>H. melpomene</i> and in a combined analysis of the <i>Heliconius</i>. The significance of the cophylogeny mapping analyses was estimated based on minimising total reconstruction costs with Jane 3, either by randomising the leaf associations (column 2) or by randomizing the <i>H. melpomene</i> phylogeny (column 3). The significance of the pairwise distance correlation was calculated, at the root of the <i>H. melpomene</i> phylogeny (column 4) and at the root of the <i>H. erato</i> phylogeny (column 5), using TreeMap 3. Each <i>p</i>-value was estimated with 1000 Monte-Carlo replicates, and the 95% confidence upper bound was calculated for each using Wilson's score interval for binomial proportions <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036464#pone.0036464-Wilson1\" target=\"_blank\">[68]</a>.</p>", "links"=>[], "tags"=>["topological", "congruence"], "article_id"=>312279, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jennifer Hoyal Cuthill", "Michael Charleston"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036464.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Significance_of_topological_congruence_between_H_erato_and_H_melpomene_phylogenies_/312279", "title"=>"Significance of topological congruence between <i>H. erato</i> and <i>H. melpomene</i> phylogenies.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-05-07 00:37:59"}

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Relative Metric

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F1000Prime