Repeated Adaptive Introgression at a Gene under Multiallelic Balancing Selection
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{"title"=>"Repeated adaptive introgression at a gene under multiallelic balancing selection", "type"=>"journal", "authors"=>[{"first_name"=>"Vincent", "last_name"=>"Castric", "scopus_author_id"=>"8061725400"}, {"first_name"=>"Jesper", "last_name"=>"Bechsgaard", "scopus_author_id"=>"12766173900"}, {"first_name"=>"Mikkel H.", "last_name"=>"Schierup", "scopus_author_id"=>"6603704923"}, {"first_name"=>"Xavier", "last_name"=>"Vekemans", "scopus_author_id"=>"7003349131"}], "year"=>2008, "source"=>"PLoS Genetics", "identifiers"=>{"isbn"=>"1553-7404", "pmid"=>"18769722", "pui"=>"352264347", "issn"=>"15537390", "doi"=>"10.1371/journal.pgen.1000168", "scopus"=>"2-s2.0-50849109480", "sgr"=>"50849109480"}, "id"=>"20817e0d-12f3-3454-bc88-be8c866199af", "abstract"=>"Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, Arabidopsis halleri and A. lyrata, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (K = 0.0193) is about four times lower than the genomic background (K = 0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.", "link"=>"http://www.mendeley.com/research/repeated-adaptive-introgression-gene-under-multiallelic-balancing-selection", "reader_count"=>121, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>15, "Researcher"=>43, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>2, "Student > Master"=>6, "Other"=>2, "Student > Bachelor"=>5, "Professor"=>10}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>15, "Researcher"=>43, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>2, "Student > Master"=>6, "Other"=>2, "Student > Bachelor"=>5, "Professor"=>10}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Mathematics"=>1, "Agricultural and Biological Sciences"=>106, "Physics and Astronomy"=>2, "Chemical Engineering"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>106}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"United States"=>6, "United Kingdom"=>3, "Portugal"=>1, "Switzerland"=>1, "Spain"=>2, "Canada"=>1, "Austria"=>2, "Netherlands"=>2, "Belgium"=>1, "Brazil"=>1, "South Africa"=>1, "France"=>4, "Germany"=>3, "Croatia"=>1}, "group_count"=>5}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/921841"], "description"=>"<p>The phylogeny was obtained by the neighbour-joining method on pairwise proportion of nucleotide divergence after Jukes-Cantor's correction. Brackets indicate interspecific pairs of sequences assumed to represent “trans-specifically shared S-alleles”, <i>i.e.</i> alleles assumed to have evolved from a single S-allele in the direct ancestor of <i>A. lyrata</i> and <i>A. halleri</i>.</p>", "links"=>[], "tags"=>["68", "sequences"], "article_id"=>592288, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000168.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogeny_of_the_68_SRK_sequences_of_A_lyrata_and_A_halleri_/592288", "title"=>"Phylogeny of the 68 <i>SRK</i> sequences of <i>A. lyrata</i> and <i>A. halleri.</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-29 00:38:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/922295"], "description"=>"<p>All estimates were Jukes & Cantor corrected.</p>*<p>Note that Aly 9 is a member of the S-domain gene family, but polymorphism data for this gene was used here to increase the genomic background dataset.</p>", "links"=>[], "tags"=>["genes", "members", "s-gene", "fourfold", "degenerate", "sites"], "article_id"=>592740, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000168.t002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Divergence_between_Arabidopsis_halleri_and_A_lyrata_at_reference_genes_and_members_of_the_S_gene_family_at_fourfold_degenerate_sites_K_4fold_/592740", "title"=>"Divergence between <i>Arabidopsis halleri</i> and <i>A. lyrata</i> at reference genes and members of the S-gene family at fourfold degenerate sites (<i>K</i><sub>4fold</sub>).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-08-29 00:45:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/922267"], "description"=>"<p>All estimates were Jukes & Cantor corrected. HV refers to hypervariable regions as defined by Nishio and Kusaba <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000168#pgen.1000168-Nishio1\" target=\"_blank\">[60]</a>.</p>", "links"=>[], "tags"=>["trans-specifically", "alleles", "synonymous", "non", "fourfold", "degenerate", "sites"], "article_id"=>592712, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000168.t001", "stats"=>{"downloads"=>5, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Divergence_between_Arabidopsis_halleri_and_A_lyrata_at_trans_specifically_shared_SRK_alleles_at_synonymous_K_S_non_synonymous_K_A_and_fourfold_degenerate_sites_K_4fold_/592712", "title"=>"Divergence between <i>Arabidopsis halleri</i> and <i>A. lyrata</i> at trans-specifically shared <i>SRK</i> alleles at synonymous (<i>K</i><sub>S</sub>), non synonymous (<i>K</i><sub>A</sub>) and fourfold degenerate sites (<i>K</i><sub>4fold</sub>).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-08-29 00:45:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/455017", "https://ndownloader.figshare.com/files/455121", "https://ndownloader.figshare.com/files/455223", "https://ndownloader.figshare.com/files/455315", "https://ndownloader.figshare.com/files/455403", "https://ndownloader.figshare.com/files/455476", "https://ndownloader.figshare.com/files/455523"], "description"=>"<div><p>Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, <em>Arabidopsis halleri</em> and <em>A. lyrata</em>, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (<em>K = </em>0.0193) is about four times lower than the genomic background (<em>K = </em>0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.</p></div>", "links"=>[], "tags"=>["repeated", "adaptive", "introgression", "multiallelic", "balancing"], "article_id"=>149642, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000168.s001", "https://dx.doi.org/10.1371/journal.pgen.1000168.s002", "https://dx.doi.org/10.1371/journal.pgen.1000168.s003", "https://dx.doi.org/10.1371/journal.pgen.1000168.s004", "https://dx.doi.org/10.1371/journal.pgen.1000168.s005", "https://dx.doi.org/10.1371/journal.pgen.1000168.s006", "https://dx.doi.org/10.1371/journal.pgen.1000168.s007"], "stats"=>{"downloads"=>36, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Repeated_Adaptive_Introgression_at_a_Gene_under_Multiallelic_Balancing_Selection/149642", "title"=>"Repeated Adaptive Introgression at a Gene under Multiallelic Balancing Selection", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-08-29 02:40:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/922330"], "description"=>"<p><i>N<sub>A = </sub></i>Effective population size in the common ancestor of <i>A. lyrata</i> and <i>A. halleri.</i></p><p><i>N<sub>lyrata = </sub></i>Effective population size in <i>A. lyrata</i>.</p><p><i>N<sub>halleri = </sub></i>Effective population size in <i>A. halleri</i>.</p><p><i>m<sub>hal→lyr</sub> = </i>Rate at which genes come into <i>A. lyrata</i> from <i>A. halleri</i> as time moves forward.</p><p><i>m<sub>lyr→hal</sub></i> = Rate at which genes come into <i>A. halleri</i> from <i>A. lyrata</i> as time moves forward.</p>", "links"=>[], "tags"=>["splitting", "rates", "introgression"], "article_id"=>592779, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000168.t003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimates_of_952_8202_8202_4_N_956_effective_population_sizes_splitting_time_and_rates_of_introgression_using_the_isolation_with_migration_model_38_/592779", "title"=>"Estimates of <i>θ = </i>4<i>Nμ</i>, effective population sizes, splitting time and rates of introgression using the isolation with migration model [38].", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-08-29 00:46:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/922157"], "description"=>"<p>10,000 coalescent simulations were performed for each case using maximum likelihood parameter estimates obtained under the “isolation with migration” model, except for the dotted line, where the 2.5% low ancestral population size estimate was used in order to be conservative. Observed nucleotide divergence for the genomic background and S-alleles are represented by grey and black stars on the x-axis, respectively.</p>", "links"=>[], "tags"=>["nucleotide", "divergence", "genomic", "s-alleles", "introgression", "5-fold"], "article_id"=>592598, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000168.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predicted_nucleotide_divergence_between_A_halleri_and_A_lyrata_for_the_genomic_background_grey_line_S_alleles_with_the_same_rate_of_introgression_as_the_genomic_background_dotted_line_and_S_alleles_with_5_fold_increased_rate_of_introgression_relative_to_/592598", "title"=>"Predicted nucleotide divergence between <i>A. halleri</i> and <i>A. lyrata</i> for the genomic background (grey line), S-alleles with the same rate of introgression as the genomic background (dotted line) and S-alleles with 5-fold increased rate of introgression relative to the genomic background (black line).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-29 00:43:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/922026"], "description"=>"<p>Divergence times were taken from Koch et al. <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000168#pgen.1000168-Koch1\" target=\"_blank\">[18]</a>,<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000168#pgen.1000168-Koch2\" target=\"_blank\">[58]</a>. <i>θ<sub>lyrata</sub></i>, <i>θ<sub>halleri</sub></i> and <i>θ<sub>A</sub></i>, refer to polymorphism (<i>θ = </i>4<i>Nμ·</i> in <i>A. lyrata</i>, <i>A. halleri</i> and their common ancestor. As compared to unlinked genes, divergence between trans-specifically shared S-alleles is affected by two confounding factors: (1) lower effective population size than the genomic background reducing coalescence time in the ancestral species, and (2) expected higher introgression as represented by thicker dark grey arrows.</p>", "links"=>[], "tags"=>["unlinked", "genes", "trans-specifically", "pairs"], "article_id"=>592471, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000168.g003", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Divergence_process_between_Arabidopsis_lyrata_A_halleri_and_A_thaliana_at_unlinked_genes_genomic_background_and_trans_specifically_shared_pairs_of_S_alleles_/592471", "title"=>"Divergence process between <i>Arabidopsis lyrata</i>, <i>A. halleri</i> and <i>A. thaliana</i> at unlinked genes (genomic background) and trans-specifically shared pairs of S-alleles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-29 00:41:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/921939"], "description"=>"<p>Note the distinct peak of highly similar sequences observed. The vertical arrow represents the chosen threshold to define “trans-specifically shared” pairs of sequences (≤12 nucleotide differences). Note also that the two pairs of sequences with intermediate nucleotide differences (45 between <i>AlSRK03</i> and <i>AhSRK28</i>, and 50 between <i>AlSRK28</i> and <i>AhSRK03</i>) cannot represent trans-specifically shared S-alleles because they are not monophyletic (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000168#pgen-1000168-g001\" target=\"_blank\">Figure 1</a>).</p>", "links"=>[], "tags"=>["pairwise", "nucleotide", "differences", "sequences", "interspecific", "comparisons"], "article_id"=>592382, "categories"=>["Evolutionary Biology"], "users"=>["Vincent Castric", "Jesper Bechsgaard", "Mikkel H. Schierup", "Xavier Vekemans"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000168.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_the_number_of_pairwise_nucleotide_differences_for_SRK_sequences_in_interspecific_comparisons_between_A_halleri_and_A_lyrata_/592382", "title"=>"Distribution of the number of pairwise nucleotide differences for <i>SRK</i> sequences in interspecific comparisons between <i>A. halleri</i> and <i>A. lyrata</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-08-29 00:39:42"}

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