Parallel Adaptive Divergence among Geographically Diverse Human Populations
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Mendeley | Further Information

{"title"=>"Parallel adaptive divergence among geographically diverse human populations", "type"=>"journal", "authors"=>[{"first_name"=>"Jacob A.", "last_name"=>"Tennessen", "scopus_author_id"=>"8954347700"}, {"first_name"=>"Joshua M.", "last_name"=>"Akey", "scopus_author_id"=>"6601938072"}], "year"=>2011, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-79959856149", "sgr"=>"79959856149", "issn"=>"15537390", "doi"=>"10.1371/journal.pgen.1002127", "pmid"=>"21698142", "pui"=>"362058258"}, "id"=>"ee430f54-14a0-30cc-80e1-272479c56c67", "abstract"=>"Few genetic differences between human populations conform to the classic model of positive selection, in which a newly arisen mutation rapidly approaches fixation in one lineage, suggesting that adaptation more commonly occurs via moderate changes in standing variation at many loci. Detecting and characterizing this type of complex selection requires integrating individually ambiguous signatures across genomically and geographically extensive data. Here, we develop a novel approach to test the hypothesis that selection has favored modest divergence at particular loci multiple times in independent human populations. We find an excess of SNPs showing non-neutral parallel divergence, enriched for genic and nonsynonymous polymorphisms in genes encompassing diverse and often disease related functions. Repeated parallel evolution in the same direction suggests common selective pressures in disparate habitats. We test our method with extensive coalescent simulations and show that it is robust to a wide range of demographic events. Our results demonstrate phylogenetically orthogonal patterns of local adaptation caused by subtle shifts at many widespread polymorphisms that likely underlie substantial phenotypic diversity.", "link"=>"http://www.mendeley.com/research/parallel-adaptive-divergence-among-geographically-diverse-human-populations", "reader_count"=>90, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>28, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>31, "Student > Postgraduate"=>2, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>9}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>28, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>31, "Student > Postgraduate"=>2, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>4, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>9}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>7, "Mathematics"=>1, "Agricultural and Biological Sciences"=>72, "Medicine and Dentistry"=>1, "Social Sciences"=>2, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Social Sciences"=>{"Social Sciences"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>72}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"Austria"=>1, "United States"=>5, "United Kingdom"=>1, "Italy"=>1, "Switzerland"=>3, "Germany"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/764282"], "description"=>"<p>F<sub>ST</sub> between Africa (PY or WA) and Europe (EU) is compared with F<sub>ST</sub> between Oceania (OC) and East Asia (EA) or South America (SA). In each plot, F<sub>ST</sub> values for a mean of 26,864 randomly selected SNPs have been ranked for both group pairs and are plotted against each other in order of increasing F<sub>ST</sub>; darker shades represent a high proportion of SNPs falling in that particular sector. The sector in the upper right corner of each plot, representing all parallel divergent SNPs at a threshold of 5%, contains more SNPs than any other similarly-sized sector in that plot. These divergence comparisons are phylogenetically independent because the common ancestor of Oceania/Asia/America existed more recently than the common ancestor shared by these three groups and Europe or Africa. Thus, divergent natural selection acting independently both between Europe and Africa and between Oceania and Asia/America is the best explanation for this observation. Convergence due to gene flow would cause a positive correlation throughout each plot, even after excluding high-F<sub>ST</sub> SNPs, and parallel occurrences of purifying selection would cause the sectors in the lower left corner of each plot to be the darkest; these patterns are not observed.</p>", "links"=>[], "tags"=>["ranks", "divergence"], "article_id"=>434656, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002127.g003", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heat_map_showing_ranks_for_four_divergence_comparisons_/434656", "title"=>"Heat map showing ranks for four divergence comparisons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-16 01:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/764196"], "description"=>"<p>Groups are abbreviated as in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen-1002127-g001\" target=\"_blank\">Figure 1A</a>. Theoretical expectations (the threshold squared times the total) are shown in yellow (error bars = theoretical standard deviation; <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen.1002127.s008\" target=\"_blank\">Text S1</a>). Mean results from 1000 simulated samples under the neutral <i>standard</i> model are shown in blue (error bars  =  standard deviation). Observed empirical counts are shown in red (error bars  =  standard deviation among 1000 samples of independent SNPs). For all but one divergence comparison, more parallel divergent SNPs than expected were observed, indicative of parallel adaptation. For each bar, the shading indicates the orientation skew; the darker shade represents the number of SNPs showing the major orientation, and the lighter shade represents the number of SNPs showing the minor orientation. A skew deviating from 50% indicates that each group in the y-axis group pair tended to have relatively similar allele frequencies as a particular group in the x-axis group pair, as indicated by the green triangles. A single asterisk (*) indicates a significant excess of parallel divergent SNPs relative to the <i>standard</i> simulations (≥81 SNPs; p<0.05), while a double asterisk (**) indicates significance both relative to the <i>standard</i> simulations and in Bonferroni-corrected Fisher's exact tests (≥91 SNPs; p<0.05).</p>", "links"=>[], "tags"=>["parallel", "divergent", "snps", "divergence", "comparisons"], "article_id"=>434572, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002127.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mean_number_of_parallel_divergent_SNPs_for_all_fifteen_divergence_comparisons_at_a_5_threshold_/434572", "title"=>"Mean number of parallel divergent SNPs for all fifteen divergence comparisons at a 5% threshold.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-16 01:16:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/764091"], "description"=>"<p>(A) Unrooted phylogenetic relationship among the six demographic groups examined in this study. A phylogenetically independent divergence comparison can be made between any two sets of pairwise F<sub>ST</sub> values corresponding to two group pairs that do not appear together in the same colored region; thus, fifteen divergence comparisons are possible. (B) Hypothetical dataset comprising a single divergence comparison showing parallel divergence. Five groups (A–E) are shown, formed of two populations each; only the four groups that fall into two clear, phylogenetically independent group pairs are retained, while admixed group C is excluded. SNPs are excluded for four reasons. First, if SNPs are invariant in an entire group pair (“not globally polymorphic”), because these may represent recent mutations instead of ancestral polymorphisms. Second, if SNPs show a global minor allele frequency less than 0.4 (“not intermediate frequency”), because these may have had skewed ancestral frequencies that were less likely to become divergent via drift. Third, if SNPs cause the site frequency spectra of some groups to differ substantially from those of other groups (“not similar spectrum”), because these may reflect differences in ascertainment or demographic history. Fourth, if SNPs are in linkage disequilibrium with an included SNP (“not unlinked”), because these are not independent. Eight valid SNPs remain. Two divergent SNPs at a threshold of 25% (a higher threshold than we used in practice) in both group pairs are indicated. Both are parallel divergent SNPs showing the same orientation (A/D, B/E), so the orientation skew is 100%.</p>", "links"=>[], "tags"=>["diagram"], "article_id"=>434472, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002127.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_diagram_of_our_methodology_/434472", "title"=>"Schematic diagram of our methodology.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-16 01:14:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/764540"], "description"=>"<p>For each group pair, values of F<sub>ST</sub> at all 111,724 globally polymorphic, intermediate frequency SNPs have been ranked, shown on a log scale (y-axis); here, lower rank corresponds to higher F<sub>ST</sub>. Multiple group pairs show very low ranks due to high F<sub>ST</sub> across <i>ABCA12</i>, with several exceeding a 1% threshold. Mutations in this skin keratinization gene cause harlequin ichthyosis <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen.1002127-Thomas1\" target=\"_blank\">[27]</a>. The orientations of the most extreme divergence comparisons indicate that one allele is common in Africa and South America, while the other is common in Europe, Oceania, and East Asia. Rank lines have been staggered slightly for ease of visualization. ATP-binding cassette (ABC) transporters like this one are enriched among parallel divergent genes (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen.1002127.s006\" target=\"_blank\">Table S3</a>) and are linked to multi-drug resistance, macular degeneration, breast cancer, diabetes, and other diseases.</p>", "links"=>[], "tags"=>["chromosome", "illustrating", "parallel", "divergence"], "article_id"=>434915, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002127.g006", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ranks_of_F_ST_in_a_section_of_Chromosome_2_illustrating_parallel_divergence_at_ABCA12_/434915", "title"=>"Ranks of F<sub>ST</sub> in a section of Chromosome 2, illustrating parallel divergence at <i>ABCA12</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-16 01:21:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/764386"], "description"=>"<p>Relative proportion of parallel divergent SNPs, genic parallel divergent SNPs, and nonsynonymous parallel divergent SNPs are shown for thresholds less than or equal to 5%. All thresholds show an excess of parallel divergent SNPs that is more pronounced for genic SNPs and even more pronounced for nonsynonymous SNPs. As the threshold is lowered, the relative proportion of genic and nonsynonymous SNPs increases faster than for all SNPs combined, suggesting that positive selection is driving the pattern.</p>", "links"=>[], "tags"=>["proportions", "snp", "classes"], "article_id"=>434769, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002127.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_proportions_of_SNP_classes_across_various_thresholds_/434769", "title"=>"Relative proportions of SNP classes across various thresholds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-16 01:19:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/764622"], "description"=>"<p>Confidence intervals are calculated from 100 independent datasets generated under each model. The empirical mean values are significantly higher than the simulated mean values across all models. A moderate excess of parallel divergent SNPs, although not as high as the empirically observed parallel divergence, was generated by three models: <i>constantlow</i>, <i>3tightestbottle</i>, and <i>OC-EAmig100</i>. These models represent extreme demographic scenarios that are unlikely to accurately approximate the histories of the populations analyzed. Descriptions of the simulated models and their results can be found in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen.1002127.s007\" target=\"_blank\">Table S4</a>. (A) Mean number of parallel divergent SNPs (B) Mean orientation skew (frequency of major orientation).</p>", "links"=>[], "tags"=>["parallel", "divergent", "snps", "skew", "simulation"], "article_id"=>434993, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002127.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mean_number_of_parallel_divergent_SNPs_and_orientation_skew_for_nine_simulation_models_/434993", "title"=>"Mean number of parallel divergent SNPs and orientation skew for nine simulation models.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-16 01:23:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/385179", "https://ndownloader.figshare.com/files/385208", "https://ndownloader.figshare.com/files/385233", "https://ndownloader.figshare.com/files/385270", "https://ndownloader.figshare.com/files/385313", "https://ndownloader.figshare.com/files/385361", "https://ndownloader.figshare.com/files/385402", "https://ndownloader.figshare.com/files/385444"], "description"=>"<div><p>Few genetic differences between human populations conform to the classic model of positive selection, in which a newly arisen mutation rapidly approaches fixation in one lineage, suggesting that adaptation more commonly occurs via moderate changes in standing variation at many loci. Detecting and characterizing this type of complex selection requires integrating individually ambiguous signatures across genomically and geographically extensive data. Here, we develop a novel approach to test the hypothesis that selection has favored modest divergence at particular loci multiple times in independent human populations. We find an excess of SNPs showing non-neutral parallel divergence, enriched for genic and nonsynonymous polymorphisms in genes encompassing diverse and often disease related functions. Repeated parallel evolution in the same direction suggests common selective pressures in disparate habitats. We test our method with extensive coalescent simulations and show that it is robust to a wide range of demographic events. Our results demonstrate phylogenetically orthogonal patterns of local adaptation caused by subtle shifts at many widespread polymorphisms that likely underlie substantial phenotypic diversity.</p> </div>", "links"=>[], "tags"=>["parallel", "adaptive", "divergence", "geographically", "populations"], "article_id"=>136042, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002127.s001", "https://dx.doi.org/10.1371/journal.pgen.1002127.s002", "https://dx.doi.org/10.1371/journal.pgen.1002127.s003", "https://dx.doi.org/10.1371/journal.pgen.1002127.s004", "https://dx.doi.org/10.1371/journal.pgen.1002127.s005", "https://dx.doi.org/10.1371/journal.pgen.1002127.s006", "https://dx.doi.org/10.1371/journal.pgen.1002127.s007", "https://dx.doi.org/10.1371/journal.pgen.1002127.s008"], "stats"=>{"downloads"=>5, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Parallel_Adaptive_Divergence_among_Geographically_Diverse_Human_Populations/136042", "title"=>"Parallel Adaptive Divergence among Geographically Diverse Human Populations", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-06-16 01:40:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/764443"], "description"=>"<p>Most divergence comparisons showed parallel divergent genes in this pathway (enrichment = 1.27), and the PY-EU vs. OC-SA divergence comparison was particularly enriched (enrichment = 2.67) with eleven parallel divergent genes. In this pathway, receptors in the axon growth cone sense guidance cues and signal downstream processes that regulate the cytoskeleton and determine which direction the axon will grow, ultimately influencing the development of neuronal networks. “Positive regulation of axonogenesis” is also an enriched GO term (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen.1002127.s006\" target=\"_blank\">Table S3</a>). Ephrin receptor <i>EPHA6</i> in particular overlaps parallel divergent SNPs in most divergence comparisons and is still observed for “PY-EU vs. EA-SA” and “WA-EU vs. EA-SA” at thresholds as low as 0.5%. Although there are more enriched genes in this pathway than in the pathways in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen.1002127.s006\" target=\"_blank\">Table S3</a>, the overall per-SNP enrichment is slightly lower for this pathway than for the <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002127#pgen.1002127.s006\" target=\"_blank\">Table S3</a> pathways, in part due to differences in mean gene length.</p>", "links"=>[], "tags"=>["pathway", "highlighting", "genes", "containing", "parallel", "divergent"], "article_id"=>434815, "categories"=>["Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Jacob A. Tennessen", "Joshua M. Akey"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002127.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Axon_guidance_pathway_highlighting_genes_containing_parallel_divergent_SNPs_/434815", "title"=>"Axon guidance pathway highlighting genes containing parallel divergent SNPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-16 01:20:15"}

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Relative Metric

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