Male-Mediated Gene Flow in Patrilocal Primates
Publication Date
July 01, 2011
Journal
PLOS ONE
Authors
Grit Schubert, Colin J. Stoneking, Mimi Arandjelovic, Christophe Boesch, et al
Volume
6
Issue
7
Pages
e21514
DOI
https://dx.plos.org/10.1371/journal.pone.0021514
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0021514
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21747938
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3128582
Europe PMC
http://europepmc.org/abstract/MED/21747938
Web of Science
000292293400014
Scopus
79959799617
Mendeley
http://www.mendeley.com/research/malemediated-gene-flow-patrilocal-primates
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Mendeley | Further Information

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/381905", "https://ndownloader.figshare.com/files/381941", "https://ndownloader.figshare.com/files/381988", "https://ndownloader.figshare.com/files/382032", "https://ndownloader.figshare.com/files/382064", "https://ndownloader.figshare.com/files/382094", "https://ndownloader.figshare.com/files/382133"], "description"=>"<div><h3>Background</h3><p>Many group–living species display strong sex biases in dispersal tendencies. However, gene flow mediated by apparently philopatric sex may still occur and potentially alters population structure. In our closest living evolutionary relatives, dispersal of adult males seems to be precluded by high levels of territoriality between males of different groups in chimpanzees, and has only been observed once in bonobos. Still, male–mediated gene flow might occur through rare events such as extra–group matings leading to extra–group paternity (EGP) and female secondary dispersal with offspring, but the extent of this gene flow has not yet been assessed.</p> <h3>Methodology/Principal Findings</h3><p>Using autosomal microsatellite genotyping of samples from multiple groups of wild western chimpanzees (<em>Pan troglodytes verus</em>) and bonobos (<em>Pan paniscus</em>), we found low genetic differentiation among groups for both males and females. Characterization of Y–chromosome microsatellites revealed levels of genetic differentiation between groups in bonobos almost as high as those reported previously in eastern chimpanzees, but lower levels of differentiation in western chimpanzees. By using simulations to evaluate the patterns of Y–chromosomal variation expected under realistic assumptions of group size, mutation rate and reproductive skew, we demonstrate that the observed presence of multiple and highly divergent Y–haplotypes within western chimpanzee and bonobo groups is best explained by successful male–mediated gene flow.</p> <h3>Conclusions/Significance</h3><p>The similarity of inferred rates of male–mediated gene flow and published rates of EGP in western chimpanzees suggests this is the most likely mechanism of male–mediated gene flow in this subspecies. In bonobos more data are needed to refine the estimated rate of gene flow. Our findings suggest that dispersal patterns in these closely related species, and particularly for the chimpanzee subspecies, are more variable than previously appreciated. This is consistent with growing recognition of extensive behavioral variation in chimpanzees and bonobos.</p> </div>", "links"=>[], "tags"=>["male-mediated", "patrilocal", "primates"], "article_id"=>135435, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Grit Schubert", "Colin J. Stoneking", "Mimi Arandjelovic", "Christophe Boesch", "Nadin Eckhardt", "Gottfried Hohmann", "Kevin Langergraber", "Dieter Lukas", "Linda Vigilant"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0021514.s001", "https://dx.doi.org/10.1371/journal.pone.0021514.s002", "https://dx.doi.org/10.1371/journal.pone.0021514.s003", "https://dx.doi.org/10.1371/journal.pone.0021514.s004", "https://dx.doi.org/10.1371/journal.pone.0021514.s005", "https://dx.doi.org/10.1371/journal.pone.0021514.s006", "https://dx.doi.org/10.1371/journal.pone.0021514.s007"], "stats"=>{"downloads"=>37, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Male_Mediated_Gene_Flow_in_Patrilocal_Primates/135435", "title"=>"Male-Mediated Gene Flow in Patrilocal Primates", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-07-01 01:30:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/759498"], "description"=>"<p>Using empirically–based levels of reproductive skew, mutation rates and group sizes, we examined levels of haplotype diversity in terms of (A), number of haplotypes and (B), maximum number of mutational steps between Y–haplotypes that might arise within groups in the absence male–mediated gene flow. (A), the proportion of groups with more than one Y–haplotype and (B), the simulated maximum number of mutations possible between Y–haplotypes within groups increases with the number of males in the group. White bars indicate bonobos, grey bars indicate chimpanzees. Maximum numbers of mutations are only shown if observed in >1% of simulated groups. Average number of reproducing males in the habituated study groups  = 9. Error bars represent ± one standard deviation.</p>", "links"=>[], "tags"=>["groups", "chimpanzees"], "article_id"=>429873, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Grit Schubert", "Colin J. Stoneking", "Mimi Arandjelovic", "Christophe Boesch", "Nadin Eckhardt", "Gottfried Hohmann", "Kevin Langergraber", "Dieter Lukas", "Linda Vigilant"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0021514.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simulations_of_Y_8211_chromosomal_variation_in_social_groups_of_western_chimpanzees_and_bonobos_/429873", "title"=>"Simulations of Y–chromosomal variation in social groups of western chimpanzees and bonobos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-01 02:44:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/759627"], "description"=>"<p>*We examined genetic differentiation for a more locally restricted subset of chimpanzee social groups (Central Region, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone-0021514-g001\" target=\"_blank\">Figure 1</a>) which was comparable to the bonobo sample, and for the entire chimpanzee sample. Results, however, did not qualitatively change. To minimize stochasticity, for all analyses of genetic differentiation between communities we excluded social groups with fewer than four individuals genotyped at the respective marker (autosomal/Y-chromosomal). Therefore, the number of pairwise comparisons differs between the autosomal and Y-chromosomal data (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone-0021514-t002\" target=\"_blank\">Table 2</a>).</p>", "links"=>[], "tags"=>["differentiation", "bonobo", "chimpanzee"], "article_id"=>429995, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Grit Schubert", "Colin J. Stoneking", "Mimi Arandjelovic", "Christophe Boesch", "Nadin Eckhardt", "Gottfried Hohmann", "Kevin Langergraber", "Dieter Lukas", "Linda Vigilant"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0021514.t001", "stats"=>{"downloads"=>9, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Autosomal_genetic_differentiation_with_95_confidence_interval_in_bonobo_and_chimpanzee_groups_/429995", "title"=>"Autosomal genetic differentiation (with 95% confidence interval) in bonobo and chimpanzee groups.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-07-01 02:46:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/759706"], "description"=>"<p>*We examined genetic differentiation for a more locally restricted subset of chimpanzee social groups (Central Region, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone-0021514-g001\" target=\"_blank\">Figure 1</a>) which was comparable to the bonobo sample, and for the entire chimpanzee sample. Results, however, did not qualitatively change. **Eastern chimpanzee data taken from Langergraber and colleagues <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone.0021514-Langergraber1\" target=\"_blank\">[62]</a>. To minimize stochasticity, for all analyses of genetic differentiation between communities we excluded social groups with fewer than four individuals genotyped at the respective marker (autosomal/Y-chromosomal). Therefore, the number of pairwise comparisons differs between the Y-chromosomal and autosomal data (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone-0021514-t001\" target=\"_blank\">Table 1</a>).</p>", "links"=>[], "tags"=>["standardized", "differentiation", "bonobo", "chimpanzee"], "article_id"=>430073, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Grit Schubert", "Colin J. Stoneking", "Mimi Arandjelovic", "Christophe Boesch", "Nadin Eckhardt", "Gottfried Hohmann", "Kevin Langergraber", "Dieter Lukas", "Linda Vigilant"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0021514.t002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Unstandardized_and_standardized_Y_8211_chromosomal_genetic_differentiation_with_95_confidence_interval_in_bonobo_and_chimpanzee_groups_/430073", "title"=>"Unstandardized and standardized Y–chromosomal genetic differentiation (with 95% confidence interval) in bonobo and chimpanzee groups.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-07-01 00:01:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/759339"], "description"=>"<p>Western chimpanzee samples were collected within Taï National Park, Côte d'Ivoire, and bonobo samples at the border of Salonga National Park, DRC. Labels designate known (C1, East, Middle, North, South) and assumed (C2–6, G2, G4, GTZ, Meteo, N1– 2) social groups. The Central Region in Taï National Park represents a geographically limited subsample of chimpanzee groups analyzed in addition to the full data set (see also <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone-0021514-t001\" target=\"_blank\">Table 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone-0021514-t002\" target=\"_blank\">2</a>). Y-chromosomal data from bonobo group C3 were taken from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0021514#pone.0021514-Eriksson2\" target=\"_blank\">[61]</a>, while autosomal data were not available for that group. Sample sizes of individuals with an estimated minimum age of 5 for each group are the following (females typed at autosomal loci/males typed at autosomal loci/males typed at Y-chromosomal loci): bonobo, C1 (17/11/10), C2 (14/10/15), C3 (0/0/6), C4 (12/9/6), C5 (4/3/2), C6 (8/3/3); chimpanzee, East (8/10/8), G2 (10/7/7), G4 (4/3/3), GTZ (3/8/6), Meteo (13/6/3), Middle (7/4/4), N1 (2/2/2), N2 (6/2/2), North (14/9/4), South (31/26/15).</p>", "links"=>[], "tags"=>["locations", "genotyped", "individuals", "groups", "chimpanzees"], "article_id"=>429706, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Grit Schubert", "Colin J. Stoneking", "Mimi Arandjelovic", "Christophe Boesch", "Nadin Eckhardt", "Gottfried Hohmann", "Kevin Langergraber", "Dieter Lukas", "Linda Vigilant"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0021514.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Geographical_locations_of_genotyped_individuals_from_social_groups_of_western_chimpanzees_and_bonobos_/429706", "title"=>"Geographical locations of genotyped individuals from social groups of western chimpanzees and bonobos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-01 02:41:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/759664"], "description"=>"<p>Estimated rates of male–mediated gene flow in bonobos and western chimpanzees for different male group sizes.</p>", "links"=>[], "tags"=>["rates", "bonobos", "chimpanzees"], "article_id"=>430039, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Grit Schubert", "Colin J. Stoneking", "Mimi Arandjelovic", "Christophe Boesch", "Nadin Eckhardt", "Gottfried Hohmann", "Kevin Langergraber", "Dieter Lukas", "Linda Vigilant"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0021514.t003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimated_rates_of_male_8211_mediated_gene_flow_in_bonobos_and_western_chimpanzees_for_different_male_group_sizes_/430039", "title"=>"Estimated rates of male–mediated gene flow in bonobos and western chimpanzees for different male group sizes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-07-01 00:00:39"}

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Relative Metric

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