Analysis of Chimpanzee History Based on Genome Sequence Alignments

Department of Genetics, Harvard Medical School, Boston, Massachusetts, United States of America.
PLoS Genetics (Impact Factor: 8.17). 05/2008; 4(4):e1000057. DOI: 10.1371/journal.pgen.1000057
Source: PubMed

ABSTRACT Population geneticists often study small numbers of carefully chosen loci, but it has become possible to obtain orders of magnitude for more data from overlaps of genome sequences. Here, we generate tens of millions of base pairs of multiple sequence alignments from combinations of three western chimpanzees, three central chimpanzees, an eastern chimpanzee, a bonobo, a human, an orangutan, and a macaque. Analysis provides a more precise understanding of demographic history than was previously available. We show that bonobos and common chimpanzees were separated approximately 1,290,000 years ago, western and other common chimpanzees approximately 510,000 years ago, and eastern and central chimpanzees at least 50,000 years ago. We infer that the central chimpanzee population size increased by at least a factor of 4 since its separation from western chimpanzees, while the western chimpanzee effective population size decreased. Surprisingly, in about one percent of the genome, the genetic relationships between humans, chimpanzees, and bonobos appear to be different from the species relationships. We used PCR-based resequencing to confirm 11 regions where chimpanzees and bonobos are not most closely related. Study of such loci should provide information about the period of time 5-7 million years ago when the ancestors of humans separated from those of the chimpanzees.

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Available from: Christine Schirmer, Aug 29, 2015
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    • "Chimpanzees and bonobos are the closest living relatives of humans. Population genetic data from chimpanzee subspecies have until recently been scarce and mainly based on either mitogenomes (Stone et al. 2010; Hvilsom et al. 2014), microsatellite markers (Becquet et al. 2007; Wegmann and Excoffier 2010; Gonder et al. 2011; Hvilsom et al. 2013) or on nuclear fragments (Fischer et al. 2004; Caswell et al. 2008). "
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    ABSTRACT: We study genome-wide nucleotide diversity in three subspecies of extant chimpanzees using exome capture. After strict filtering, SNVs and indels were called and genotyped for >50% of exons at a mean coverage of 35x per individual. Central chimpanzees (P. t. troglodytes) are the most polymorphic (nucleotide diversity, θw= 0.0023 per site) followed by Eastern (P. t. schweinfurthii) chimpanzees (θw = 0.0016) and Western (P. t. verus) chimpanzees (θw = 0.0008). A demographic scenario of divergence without gene flow fits the patterns of autosomal synonymous nucleotide diversity well except for a signal of recent gene flow from Western into Eastern chimpanzees. The striking contrast in X-linked vs. autosomal polymorphism and divergence previously reported in Central chimpanzees is also found in Eastern and Western chimpanzees. We show that the direction of selection (DoS) statistic exhibits a strong non-monotonic relationship with the strength of purifying selection S, making it inappropriate for estimating S. We instead use counts in synonymous vs. non-synonymous frequency classes to infer the distribution of S coefficients acting on non-synonymous mutations in each subspecies. The strength of purifying selection we infer is congruent with the differences in effective sizes of each subspecies: Central chimpanzees are undergoing the strongest purifying selection followed by Eastern and Western chimpanzees. Coding indels show stronger selection against indels changing the reading frame than observed in human populations. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Genome Biology and Evolution 03/2015; 7(4). DOI:10.1093/gbe/evv058 · 4.53 Impact Factor
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    • "The most likely explanation of this is incomplete lineage sorting in human–chimpanzee lineage for these variants (Caswell et al. 2008). Albeit interesting, deletions that are explained by these two scenarios constitute less than 1% of the deletions that are shared with Neandertal and Denisovan genomes and will be referred to as the " other deletions. "
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    ABSTRACT: Allele sharing between modern and archaic hominin genomes has been variously interpreted to have originated from ancestral genetic structure or through non-African introgression from archaic hominins. However, evolution of polymorphic human deletions that are shared with archaic hominin genomes have yet to be studied. We identified 427 polymorphic human deletions that are shared with archaic hominin genomes, ~87% of which originated before the Human-Neandertal divergence (ancient) and only ~9% of which have been introgressed from Neandertals (introgressed). Recurrence, incomplete lineage sorting between human and chimp lineages, and hominid-specific insertions constitute the remaining ~4% of allele sharing between humans and archaic hominins. We observed that ancient deletions correspond to more than 13% of all common (>5% allele frequency) deletion variation among modern humans. Our analyses indicate that the genomic landscapes of both ancient and introgressed deletion variants were primarily shaped by purifying selection, eliminating large and exonic variants. We found 17 exonic deletions that are shared with archaic hominin genomes, including those leading to 3 fusion transcripts. The affected genes are involved in metabolism of external and internal compounds, growth and sperm formation, as well as susceptibility to psoriasis and Crohn's disease. Our analyses suggest that these exonic deletion variants have evolved through different adaptive forces, including balancing and population specific positive selection. Our findings reveal that genomic structural variants that are shared between humans and archaic hominin genomes are common among modern humans and can influence biomedically and evolutionarily important phenotypes. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Molecular Biology and Evolution 01/2015; 32(4). DOI:10.1093/molbev/msu405 · 14.31 Impact Factor
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    • "The timing and magnitude of past demographic events were inferred through Bayesian Markov chain Monte Carlo (MCMC) coalescent-based analysis of the mitogenomes using the program BEAST v.1.6.1 (Drummond and Rambaut 2007). As dates are completely dependent on the substitution rates used, we inferred the rates (see Online Resources 3 and 6 in the ESM), using a root time calibration with a normally distributed prior mean of 1.2 million years (My), and with 95 % of the density between 0.87 and 1.53 My ago, on the basis of the earliest well-supported date for Pan divergence (Won and Hey 2005; Becquet and Przeworski 2007; Becquet et al. 2007; Caswell et al. 2008; Hey 2010; Wegmann and Excoffier 2010; Stone et al. 2010). Subsequently, the substitution rates were used to estimate changes in population size over time for the four chimpanzee subspecies and the bonobo using a separate concatenated partition, comprising rRNA, CDS, and D-loop to permit a separate evolutionary model for each partition and allow for different patterns of rate heterogeneity. "
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    Primates 08/2013; 55(1). DOI:10.1007/s10329-013-0373-3 · 1.40 Impact Factor
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