Sex Chromosome Mosaicism and Hybrid Speciation among Tiger Swallowtail Butterflies
Publication Date
September 08, 2011
Journal
PLOS Genetics
Authors
Krushnamegh Kunte, Cristina Shea, Matthew L. Aardema, J. Mark Scriber, et al
Volume
7
Issue
9
Pages
e1002274
DOI
http://doi.org/10.1371/journal.pgen.1002274
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1002274
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21931567
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3169544
Europe PMC
http://europepmc.org/abstract/MED/21931567
Web of Science
000295419100027
Scopus
80053451826
Mendeley
http://www.mendeley.com/research/sex-chromosome-mosaicism-hybrid-speciation-among-tiger-swallowtail-butterflies
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Mendeley | Further Information

{"title"=>"Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies", "type"=>"journal", "authors"=>[{"first_name"=>"Krushnamegh", "last_name"=>"Kunte", "scopus_author_id"=>"6506697539"}, {"first_name"=>"Cristina", "last_name"=>"Shea", "scopus_author_id"=>"53980459700"}, {"first_name"=>"Matthew L.", "last_name"=>"Aardema", "scopus_author_id"=>"25521481800"}, {"first_name"=>"J. Mark", "last_name"=>"Scriber", "scopus_author_id"=>"7004491199"}, {"first_name"=>"Thomas E.", "last_name"=>"Juenger", "scopus_author_id"=>"8763161000"}, {"first_name"=>"Lawrence E.", "last_name"=>"Gilbert", "scopus_author_id"=>"7202480243"}, {"first_name"=>"Marcus R.", "last_name"=>"Kronforst", "scopus_author_id"=>"8287177800"}], "year"=>2011, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"362681124", "sgr"=>"80053451826", "pmid"=>"21931567", "doi"=>"10.1371/journal.pgen.1002274", "issn"=>"15537390", "scopus"=>"2-s2.0-80053451826", "isbn"=>"1553-7404"}, "id"=>"d077a8e1-5bc0-3c6b-af9d-d9e6afbe6372", "abstract"=>"Hybrid speciation, or the formation of a daughter species due to interbreeding between two parental species, is a potentially important means of diversification, because it generates new forms from existing variation. However, factors responsible for the origin and maintenance of hybrid species are largely unknown. Here we show that the North American butterfly Papilio appalachiensis is a hybrid species, with genomic admixture from Papilio glaucus and Papilio canadensis. Papilio appalachiensis has a mosaic phenotype, which is hypothesized to be the result of combining sex-linked traits from P. glaucus and P. canadensis. We show that P. appalachiensis' Z-linked genes associated with a cooler thermal habitat were inherited from P. canadensis, whereas its W-linked mimicry and mitochondrial DNA were inherited from P. glaucus. Furthermore, genome-wide AFLP markers showed nearly equal contributions from each parental species in the origin of P. appalachiensis, indicating that it formed from a burst of hybridization between the parental species, with little subsequent backcrossing. However, analyses of genetic differentiation, clustering, and polymorphism based on molecular data also showed that P. appalachiensis is genetically distinct from both parental species. Population genetic simulations revealed P. appalachiensis to be much younger than the parental species, with unidirectional gene flow from P. glaucus and P. canadensis into P. appalachiensis. Finally, phylogenetic analyses, combined with ancestral state reconstruction, showed that the two traits that define P. appalachiensis' mosaic phenotype, obligatory pupal diapause and mimicry, evolved uniquely in P. canadensis and P. glaucus, respectively, and were then recombined through hybridization to form P. appalachiensis. These results suggest that natural selection and sex-linked traits may have played an important role in the origin and maintenance of P. appalachiensis as a hybrid species. In particular, ecological barriers associated with a steep thermal cline appear to maintain the distinct, mosaic genome of P. appalachiensis despite contact and occasional hybridization with both parental species.", "link"=>"http://www.mendeley.com/research/sex-chromosome-mosaicism-hybrid-speciation-among-tiger-swallowtail-butterflies", "reader_count"=>133, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Researcher"=>34, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>48, "Student > Postgraduate"=>6, "Student > Master"=>16, "Other"=>6, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>7}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Researcher"=>34, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>48, "Student > Postgraduate"=>6, "Student > Master"=>16, "Other"=>6, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>7}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>117, "Medicine and Dentistry"=>1, "Social Sciences"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>117}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>3}}, "reader_count_by_country"=>{"United States"=>11, "Japan"=>2, "United Kingdom"=>7, "Portugal"=>2, "Russia"=>1, "India"=>3, "Greece"=>1, "Canada"=>1, "Netherlands"=>1, "Austria"=>1, "Finland"=>1, "Italy"=>1, "Germany"=>2}, "group_count"=>5}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/737814"], "description"=>"<p>(A) Population clustering of AFLP data in STRUCTURE under the assumption of two, three and four populations, comparing <i>appalachiensis</i> with laboratory-generated <i>glaucus</i> x <i>canadensis</i> hybrids. (B) <i>appalachiensis</i> AFLP allele frequencies with respect to <i>glaucus</i> and <i>canadensis</i>, based on species pair-wise locus-by-locus AMOVAs. Allele frequencies of “<i>glaucus</i>-like” AFLPs were significantly different from <i>canadensis</i>, “<i>canadensis</i>-like” AFLPs were significantly different from <i>glaucus</i>, “intermediate” were intermediate between <i>glaucus</i> and <i>canadensis</i> but significantly different from neither, and “different” were significantly different from both <i>glaucus</i> and <i>canadensis</i>. (C) Population clustering in STRUCTURE under the assumption of four populations, showing genomic similarity between the laboratory-generated hybrids and late flight <i>canadensis</i>, and distinctiveness of <i>appalachiensis</i> (also see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#pgen.1002274.s002\" target=\"_blank\">Figure S2</a>). For (A) and (C), admixture proportions of the sampled individuals, rather than their assignment probabilities, are shown.</p>", "links"=>[], "tags"=>["admixture", "hybrid", "laboratory-generated", "hybrids"], "article_id"=>408171, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.g003", "stats"=>{"downloads"=>4, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_admixture_in_appalachiensis_showing_its_hybrid_origin_and_its_contrast_with_laboratory_generated_hybrids_and_late_flight_canadensis_/408171", "title"=>"Genomic admixture in <i>appalachiensis</i> showing its hybrid origin and its contrast with laboratory-generated hybrids and late flight <i>canadensis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:16:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/737686"], "description"=>"<p>(A) <i>appalachiensis</i> genotypes at loci that were significantly different (p<0.001) between <i>glaucus</i> and <i>canadensis</i>, as judged by <i>F<sub>ST</sub></i> values from a locus-by-locus AMOVA comparing <i>glaucus</i> and <i>canadensis</i>. Genotypes are nucleotide bases at specific SNP or indel polymorphisms, which can be diploid (Z-linked polymorphisms scored in males) or haploid (mtDNA, and Z-linked polymorphisms scored in females). Color code: purple: genotypes characteristic of <i>glaucus</i>; light blue: genotypes characteristic of <i>canadensis</i>; black: heterozygotes; grey: missing data; orange: late flight <i>canadensis</i>. (B) Species pair-wise <i>F<sub>ST</sub></i> values for the mitochondrial and Z-linked genes (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#pgen.1002274.s009\" target=\"_blank\">Table S4</a> for individual values for each gene and species pair-wise comparisons).</p>", "links"=>[], "tags"=>["differentiation", "mismatch", "mitochondrial", "z-linked", "genes"], "article_id"=>408036, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genotypic_differentiation_between_glaucus_and_canadensis_and_the_mismatch_in_mitochondrial_and_Z_linked_genes_in_appalachiensis_/408036", "title"=>"Genotypic differentiation between <i>glaucus</i> and <i>canadensis</i>, and the mismatch in mitochondrial and Z-linked genes in <i>appalachiensis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:13:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/738278"], "description"=>"<p>For some Z-linked genes, the number of sequences differed from the number of samples sequenced because of heterozygosity in males.</p>", "links"=>[], "tags"=>["nucleotide", "polymorphisms", "haplotype"], "article_id"=>408646, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.t002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_single_nucleotide_polymorphisms_and_haplotype_diversity_among_glaucus_canadensis_and_appalachiensis_/408646", "title"=>"Distribution of single nucleotide polymorphisms and haplotype diversity among <i>glaucus</i>, <i>canadensis</i>, and <i>appalachiensis</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:24:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/737958"], "description"=>"<p>(A) AFLP-based neighbor-joining tree, with percentage bootstrap support shown for branches. The ten <i>appalachiensis</i> and two <i>canadensis</i> samples that cluster outside their species are marked with asterisks. (B) Character evolution based on the AFLP phylogeny.</p>", "links"=>[], "tags"=>["relationships", "tiger"], "article_id"=>408328, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.g004", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_relationships_and_character_evolution_among_tiger_swallowtails_/408328", "title"=>"Phylogenetic relationships and character evolution among tiger swallowtails.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:18:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/372323", "https://ndownloader.figshare.com/files/372360", "https://ndownloader.figshare.com/files/372412", "https://ndownloader.figshare.com/files/372466", "https://ndownloader.figshare.com/files/372507", "https://ndownloader.figshare.com/files/372553", "https://ndownloader.figshare.com/files/372659", "https://ndownloader.figshare.com/files/372703", "https://ndownloader.figshare.com/files/372779", "https://ndownloader.figshare.com/files/372822", "https://ndownloader.figshare.com/files/372863"], "description"=>"<div><p>Hybrid speciation, or the formation of a daughter species due to interbreeding between two parental species, is a potentially important means of diversification, because it generates new forms from existing variation. However, factors responsible for the origin and maintenance of hybrid species are largely unknown. Here we show that the North American butterfly <em>Papilio appalachiensis</em> is a hybrid species, with genomic admixture from <em>Papilio glaucus</em> and <em>Papilio canadensis</em>. <em>Papilio appalachiensis</em> has a mosaic phenotype, which is hypothesized to be the result of combining sex-linked traits from <em>P. glaucus</em> and <em>P. canadensis</em>. We show that <em>P. appalachiensis</em>' Z-linked genes associated with a cooler thermal habitat were inherited from <em>P. canadensis</em>, whereas its W-linked mimicry and mitochondrial DNA were inherited from <em>P. glaucus</em>. Furthermore, genome-wide AFLP markers showed nearly equal contributions from each parental species in the origin of <em>P. appalachiensis</em>, indicating that it formed from a burst of hybridization between the parental species, with little subsequent backcrossing. However, analyses of genetic differentiation, clustering, and polymorphism based on molecular data also showed that <em>P. appalachiensis</em> is genetically distinct from both parental species. Population genetic simulations revealed <em>P. appalachiensis</em> to be much younger than the parental species, with unidirectional gene flow from <em>P. glaucus</em> and <em>P. canadensis</em> into <em>P. appalachiensis</em>. Finally, phylogenetic analyses, combined with ancestral state reconstruction, showed that the two traits that define <em>P. appalachiensis</em>' mosaic phenotype, obligatory pupal diapause and mimicry, evolved uniquely in <em>P. canadensis</em> and <em>P. glaucus</em>, respectively, and were then recombined through hybridization to form <em>P. appalachiensis</em>. These results suggest that natural selection and sex-linked traits may have played an important role in the origin and maintenance of <em>P. appalachiensis</em> as a hybrid species. In particular, ecological barriers associated with a steep thermal cline appear to maintain the distinct, mosaic genome of <em>P. appalachiensis</em> despite contact and occasional hybridization with both parental species.</p> </div>", "links"=>[], "tags"=>["chromosome", "mosaicism", "hybrid", "speciation", "tiger", "swallowtail", "butterflies"], "article_id"=>133547, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002274.s001", "https://dx.doi.org/10.1371/journal.pgen.1002274.s002", "https://dx.doi.org/10.1371/journal.pgen.1002274.s003", "https://dx.doi.org/10.1371/journal.pgen.1002274.s004", "https://dx.doi.org/10.1371/journal.pgen.1002274.s005", "https://dx.doi.org/10.1371/journal.pgen.1002274.s006", "https://dx.doi.org/10.1371/journal.pgen.1002274.s007", "https://dx.doi.org/10.1371/journal.pgen.1002274.s008", "https://dx.doi.org/10.1371/journal.pgen.1002274.s009", "https://dx.doi.org/10.1371/journal.pgen.1002274.s010", "https://dx.doi.org/10.1371/journal.pgen.1002274.s011"], "stats"=>{"downloads"=>19, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Sex_Chromosome_Mosaicism_and_Hybrid_Speciation_among_Tiger_Swallowtail_Butterflies/133547", "title"=>"Sex Chromosome Mosaicism and Hybrid Speciation among Tiger Swallowtail Butterflies", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-08 00:59:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/738316"], "description"=>"<p>Linkage disequilibrium was calculated as pair-wise associations among all polymorphisms, and summarized below as the average percentage of polymorphisms that were significantly (p≤0.01) associated with each other. For AFLPs, differences in levels of linkage disequilibrium among all the groups were highly significant (p<0.0001), except among <i>appalachiensis</i> and <i>glaucus</i> (p = 0.053). For Z-linked genes, <i>canadensis</i> and <i>appalachiensis</i> were not significantly different from each other (p = 0.214) but they are both different from <i>glaucus</i> (p<0.0001).</p>", "links"=>[], "tags"=>["linkage", "arranged", "highest", "lowest"], "article_id"=>408684, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.t001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimates_of_linkage_disequilibrium_arranged_from_highest_to_lowest_values_with_mean_177_SD_/408684", "title"=>"Estimates of linkage disequilibrium, arranged from highest to lowest values, with mean ± SD.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:24:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/738064"], "description"=>"<p>Dates of divergence estimated by IMa2 are: (a) <i>appalachiensis</i> and <i>glaucus</i>: ca 100,000 years ago, (b) <i>appalachiensis</i> and <i>canadensis</i>: ca 90,000 years ago, (c) <i>glaucus</i> and <i>canadensis</i>: ca 580,000 years ago.</p>", "links"=>[], "tags"=>["divergence", "times", "hybrid"], "article_id"=>408434, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimated_divergence_times_between_the_parental_glaucus_and_canadensis_and_the_hybrid_appalachiensis_/408434", "title"=>"Estimated divergence times between the parental <i>glaucus</i> and <i>canadensis</i> and the hybrid <i>appalachiensis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:20:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/738170"], "description"=>"<p>Gene flow was estimated as the population migration rate or 2Nm, which is equivalent to the historical average number of immigrants between species per generation: <i>glaucus</i> to <i>appalachiensis</i>: 2.3; <i>canadensis</i> to <i>appalachiensis</i>: 1.8; <i>appalachiensis</i> to either <i>glaucus</i> or <i>canadensis</i>: 0; <i>glaucus</i> to <i>canadensis</i>: 0.1; <i>canadensis</i> to <i>glaucus</i>: 0.</p>", "links"=>[], "tags"=>["genetics and genomics", "ecology", "Evolutionary biology"], "article_id"=>408539, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimated_gene_flow_among_appalachiensis_glaucus_and_canadensis_/408539", "title"=>"Estimated gene flow among <i>appalachiensis</i>, <i>glaucus</i>, and <i>canadensis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:22:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/737526"], "description"=>"<p>(A) <i>Papilio appalachiensis</i> is endemic to mid- and high elevations in the Appalachian Mountains and sympatric with <i>glaucus</i> throughout its range, but presumably parapatric with <i>canadensis</i> in its northernmost range <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#pgen.1002274-Pavulaan1\" target=\"_blank\">[35]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#pgen.1002274-Pavulaan2\" target=\"_blank\">[36]</a> (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#s3\" target=\"_blank\">Materials and Methods</a>). Also shown is the range of <i>Battus philenor</i>, Batesian model for the mimetic <i>glaucus</i>, <i>appalachiensis</i> and <i>garcia</i> melanic female forms. (B) Ecological and morphological differentiation between <i>glaucus</i> and <i>canadensis</i>, and their admixture in <i>appalachiensis </i><a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#pgen.1002274-Pavulaan1\" target=\"_blank\">[35]</a>–<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#pgen.1002274-Scriber7\" target=\"_blank\">[38]</a> (also see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002274#pgen.1002274.s001\" target=\"_blank\">Figure S1</a>).</p>", "links"=>[], "tags"=>["distributional", "ranges", "hybrid", "zones", "tiger", "phenotype"], "article_id"=>407871, "categories"=>["Ecology", "Genetics", "Evolutionary Biology"], "users"=>["Krushnamegh Kunte", "Cristina Shea", "Matthew L. Aardema", "J. Mark Scriber", "Thomas E. Juenger", "Lawrence E. Gilbert", "Marcus R. Kronforst"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002274.g001", "stats"=>{"downloads"=>6, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_distributional_ranges_and_hybrid_zones_of_tiger_swallowtails_and_the_hybrid_phenotype_of_Papilio_appalachiensis_/407871", "title"=>"The distributional ranges and hybrid zones of tiger swallowtails, and the hybrid phenotype of <i>Papilio appalachiensis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:11:11"}

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Relative Metric

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