Limits...
Insights into hominid evolution from the gorilla genome sequence.

Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, McCarthy S, Montgomery SH, Schwalie PC, Tang YA, Ward MC, Xue Y, Yngvadottir B, Alkan C, Andersen LN, Ayub Q, Ball EV, Beal K, Bradley BJ, Chen Y, Clee CM, Fitzgerald S, Graves TA, Gu Y, Heath P, Heger A, Karakoc E, Kolb-Kokocinski A, Laird GK, Lunter G, Meader S, Mort M, Mullikin JC, Munch K, O'Connor TD, Phillips AD, Prado-Martinez J, Rogers AS, Sajjadian S, Schmidt D, Shaw K, Simpson JT, Stenson PD, Turner DJ, Vigilant L, Vilella AJ, Whitener W, Zhu B, Cooper DN, de Jong P, Dermitzakis ET, Eichler EE, Flicek P, Goldman N, Mundy NI, Ning Z, Odom DT, Ponting CP, Quail MA, Ryder OA, Searle SM, Warren WC, Wilson RK, Schierup MH, Rogers J, Tyler-Smith C, Durbin R - Nature (2012)

Bottom Line: A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing.We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species.The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

View Article: PubMed Central - PubMed

Affiliation: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1SA, UK.

ABSTRACT
Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

Show MeSH
Genome-wide ILS and selectiona, Variation in incomplete lineage sorting. Each vertical blue line represents the fraction of ILS between human, chimpanzee and gorilla estimated in a 1 Mbp region. Dashed black lines show the average ILS across the autosomes and on X; the red line shows the expected ILS on X, given the autosomal average and assuming neutral evolution. b, Reduction in ILS around protein coding genes. The blue line shows the mean rate of ILS sites normalised by mutation rate as a function of distance upstream or downstream of the nearest gene (see Supplementary Information). The horizontal dashed line indicates the average value outside 300 kbp from the nearest gene; error bars are s.e.m.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3303130&req=5

Figure 2: Genome-wide ILS and selectiona, Variation in incomplete lineage sorting. Each vertical blue line represents the fraction of ILS between human, chimpanzee and gorilla estimated in a 1 Mbp region. Dashed black lines show the average ILS across the autosomes and on X; the red line shows the expected ILS on X, given the autosomal average and assuming neutral evolution. b, Reduction in ILS around protein coding genes. The blue line shows the mean rate of ILS sites normalised by mutation rate as a function of distance upstream or downstream of the nearest gene (see Supplementary Information). The horizontal dashed line indicates the average value outside 300 kbp from the nearest gene; error bars are s.e.m.

Mentions: The genealogy relating human (H), chimpanzee (C) and gorilla (G) varies between loci across the genome. CoalHMM explicitly models this and infers the genealogy at each position: either the standard ((H,C),G) relationship or the alternatives ((H,G),C) or ((C,G),H), which are the consequences of incomplete lineage sorting (ILS) in the ancestral HC population. We can use the pattern of ILS to explore evolutionary forces during the HCG speciation period. Across the genome we find 30% of bases exhibiting ILS, with no significant difference between the number sorting as ((H,G),C) and ((C,G),H). However, the fraction of ILS varies with respect to genomic position (Fig. 2a) by more than expected under a model of genome-wide neutral evolution (Fig. SF5.1). This variation reflects local differences in the ancestral effective population size Ne during the period between the gorilla and chimpanzee speciation events, most likely due to natural selection reducing Ne and making ILS less likely. Within coding exons mean ILS drops to 22%, and the suppression of ILS extends out to several hundred kbp from coding genes, evident even in raw site patterns before any model inference (Fig. 2b). An analysis of ILS sites in human segmental duplications suggests that assembly errors do not contribute significantly to this signal (Supplementary Information). We therefore attribute it to the effects of linkage around selected mutations, most likely in the form of background selection17, observing that it is greater around genes with lower dN/dS ratios (Fig. SF8.4). Given that more than 90% of the genome lies within 300 kbp of a coding gene, and noting the similar phenomenon reported for recent human evolution11, this supports the suggestion that selection has affected almost all of the genome throughout hominid evolution18.


Insights into hominid evolution from the gorilla genome sequence.

Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, McCarthy S, Montgomery SH, Schwalie PC, Tang YA, Ward MC, Xue Y, Yngvadottir B, Alkan C, Andersen LN, Ayub Q, Ball EV, Beal K, Bradley BJ, Chen Y, Clee CM, Fitzgerald S, Graves TA, Gu Y, Heath P, Heger A, Karakoc E, Kolb-Kokocinski A, Laird GK, Lunter G, Meader S, Mort M, Mullikin JC, Munch K, O'Connor TD, Phillips AD, Prado-Martinez J, Rogers AS, Sajjadian S, Schmidt D, Shaw K, Simpson JT, Stenson PD, Turner DJ, Vigilant L, Vilella AJ, Whitener W, Zhu B, Cooper DN, de Jong P, Dermitzakis ET, Eichler EE, Flicek P, Goldman N, Mundy NI, Ning Z, Odom DT, Ponting CP, Quail MA, Ryder OA, Searle SM, Warren WC, Wilson RK, Schierup MH, Rogers J, Tyler-Smith C, Durbin R - Nature (2012)

Genome-wide ILS and selectiona, Variation in incomplete lineage sorting. Each vertical blue line represents the fraction of ILS between human, chimpanzee and gorilla estimated in a 1 Mbp region. Dashed black lines show the average ILS across the autosomes and on X; the red line shows the expected ILS on X, given the autosomal average and assuming neutral evolution. b, Reduction in ILS around protein coding genes. The blue line shows the mean rate of ILS sites normalised by mutation rate as a function of distance upstream or downstream of the nearest gene (see Supplementary Information). The horizontal dashed line indicates the average value outside 300 kbp from the nearest gene; error bars are s.e.m.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3303130&req=5

Figure 2: Genome-wide ILS and selectiona, Variation in incomplete lineage sorting. Each vertical blue line represents the fraction of ILS between human, chimpanzee and gorilla estimated in a 1 Mbp region. Dashed black lines show the average ILS across the autosomes and on X; the red line shows the expected ILS on X, given the autosomal average and assuming neutral evolution. b, Reduction in ILS around protein coding genes. The blue line shows the mean rate of ILS sites normalised by mutation rate as a function of distance upstream or downstream of the nearest gene (see Supplementary Information). The horizontal dashed line indicates the average value outside 300 kbp from the nearest gene; error bars are s.e.m.
Mentions: The genealogy relating human (H), chimpanzee (C) and gorilla (G) varies between loci across the genome. CoalHMM explicitly models this and infers the genealogy at each position: either the standard ((H,C),G) relationship or the alternatives ((H,G),C) or ((C,G),H), which are the consequences of incomplete lineage sorting (ILS) in the ancestral HC population. We can use the pattern of ILS to explore evolutionary forces during the HCG speciation period. Across the genome we find 30% of bases exhibiting ILS, with no significant difference between the number sorting as ((H,G),C) and ((C,G),H). However, the fraction of ILS varies with respect to genomic position (Fig. 2a) by more than expected under a model of genome-wide neutral evolution (Fig. SF5.1). This variation reflects local differences in the ancestral effective population size Ne during the period between the gorilla and chimpanzee speciation events, most likely due to natural selection reducing Ne and making ILS less likely. Within coding exons mean ILS drops to 22%, and the suppression of ILS extends out to several hundred kbp from coding genes, evident even in raw site patterns before any model inference (Fig. 2b). An analysis of ILS sites in human segmental duplications suggests that assembly errors do not contribute significantly to this signal (Supplementary Information). We therefore attribute it to the effects of linkage around selected mutations, most likely in the form of background selection17, observing that it is greater around genes with lower dN/dS ratios (Fig. SF8.4). Given that more than 90% of the genome lies within 300 kbp of a coding gene, and noting the similar phenomenon reported for recent human evolution11, this supports the suggestion that selection has affected almost all of the genome throughout hominid evolution18.

Bottom Line: A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing.We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species.The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

View Article: PubMed Central - PubMed

Affiliation: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1SA, UK.

ABSTRACT
Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

Show MeSH