Human and Non-Human Primate Genomes Share Hotspots of Positive
Selection
Among primates, genome-wide analysis of recent positive selection is currently
limited to the human species because it requires extensive sampling of genotypic
data from many individuals. The extent to which genes positively selected in
human also present adaptive changes in other primates therefore remains unknown.
This question is important because a gene that has been positively selected
independently in the human and in other primate lineages may be less likely to
be involved in human specific phenotypic changes such as dietary habits or
cognitive abilities. To answer this question, we analysed heterozygous Single
Nucleotide Polymorphisms (SNPs) in the genomes of single human, chimpanzee,
orangutan, and macaque individuals using a new method aiming to identify
selective sweeps genome-wide. We found an unexpectedly high number of
orthologous genes exhibiting signatures of a selective sweep simultaneously in
several primate species, suggesting the presence of hotspots of positive
selection. A similar significant excess is evident when comparing genes
positively selected during recent human evolution with genes subjected to
positive selection in their coding sequence in other primate lineages and
identified using a different test. These findings are further supported by
comparing several published human genome scans for positive selection with our
findings in non-human primate genomes. We thus provide extensive evidence that
the co-occurrence of positive selection in humans and in other primates at the
same genetic loci can be measured with only four species, an indication that it
may be a widespread phenomenon. The identification of positive selection in
humans alongside other primates is a powerful tool to outline those genes that
were selected uniquely during recent human evolution.
Vyšlo v časopise:
Human and Non-Human Primate Genomes Share Hotspots of Positive
Selection. PLoS Genet 6(2): e32767. doi:10.1371/journal.pgen.1000840
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000840
Souhrn
Among primates, genome-wide analysis of recent positive selection is currently
limited to the human species because it requires extensive sampling of genotypic
data from many individuals. The extent to which genes positively selected in
human also present adaptive changes in other primates therefore remains unknown.
This question is important because a gene that has been positively selected
independently in the human and in other primate lineages may be less likely to
be involved in human specific phenotypic changes such as dietary habits or
cognitive abilities. To answer this question, we analysed heterozygous Single
Nucleotide Polymorphisms (SNPs) in the genomes of single human, chimpanzee,
orangutan, and macaque individuals using a new method aiming to identify
selective sweeps genome-wide. We found an unexpectedly high number of
orthologous genes exhibiting signatures of a selective sweep simultaneously in
several primate species, suggesting the presence of hotspots of positive
selection. A similar significant excess is evident when comparing genes
positively selected during recent human evolution with genes subjected to
positive selection in their coding sequence in other primate lineages and
identified using a different test. These findings are further supported by
comparing several published human genome scans for positive selection with our
findings in non-human primate genomes. We thus provide extensive evidence that
the co-occurrence of positive selection in humans and in other primates at the
same genetic loci can be measured with only four species, an indication that it
may be a widespread phenomenon. The identification of positive selection in
humans alongside other primates is a powerful tool to outline those genes that
were selected uniquely during recent human evolution.
Zdroje
1. Kimura
M
1979
The neutral theory of molecular evolution.
Sci Am
241
98
100, 102, 108 passim
2. Eyre-Walker
A
Keightley
PD
2007
The distribution of fitness effects of new
mutations.
Nat Rev Genet
8
610
618
3. Keightley
PD
Eyre-Walker
A
2007
Joint inference of the distribution of fitness effects of
deleterious mutations and population demography based on nucleotide
polymorphism frequencies.
Genetics
177
2251
2261
4. Boyko
AR
Williamson
SH
Indap
AR
Degenhardt
JD
Hernandez
RD
2008
Assessing the evolutionary impact of amino acid mutations in the
human genome.
PLoS Genet
4
e1000083
doi:10.1371/journal.pgen.1000083
5. Charlesworth
J
Eyre-Walker
A
2006
The rate of adaptive evolution in enteric
bacteria.
Mol Biol Evol
23
1348
1356
6. Bierne
N
Eyre-Walker
A
2004
The genomic rate of adaptive amino acid substitution in
Drosophila.
Mol Biol Evol
21
1350
1360
7. Welch
JJ
2006
Estimating the genomewide rate of adaptive protein evolution in
Drosophila.
Genetics
173
821
837
8. Andolfatto
P
2005
Adaptive evolution of non-coding DNA in
Drosophila.
Nature
437
1149
1152
9. Cai
JJ
Macpherson
JM
Sella
G
Petrov
DA
2009
Pervasive hitchhiking at coding and regulatory sites in
humans.
PLoS Genet
5
e1000336
doi:10.1371/journal.pgen.1000336
10. Gojobori
J
Tang
H
Akey
JM
Wu
CI
2007
Adaptive evolution in humans revealed by the negative correlation
between the polymorphism and fixation phases of evolution.
Proc Natl Acad Sci U S A
104
3907
3912
11. Williamson
SH
Hubisz
MJ
Clark
AG
Payseur
BA
Bustamante
CD
2007
Localizing recent adaptive evolution in the human
genome.
PLoS Genet
3
e90
doi:10.1371/journal.pgen.0030090
12. Voight
BF
Kudaravalli
S
Wen
X
Pritchard
JK
2006
A map of recent positive selection in the human
genome.
PLoS Biol
4
e72
doi:10.1371/journal.pbio.0040072
13. Carlson
CS
Thomas
DJ
Eberle
MA
Swanson
JE
Livingston
RJ
2005
Genomic regions exhibiting positive selection identified from
dense genotype data.
Genome Res
15
1553
1565
14. Tang
K
Thornton
KR
Stoneking
M
2007
A New Approach for Using Genome Scans to Detect Recent Positive
Selection in the Human Genome.
PLoS Biol
5
e171
doi:10.1371/journal.pbio.0050171
15. Pickrell
JK
Coop
G
Novembre
J
Kudaravalli
S
Li
JZ
2009
Signals of recent positive selection in a worldwide sample of
human populations.
Genome Res
19
826
837
16. Bustamante
CD
Fledel-Alon
A
Williamson
S
Nielsen
R
Hubisz
MT
2005
Natural selection on protein-coding genes in the human
genome.
Nature
437
1153
1157
17. Sabeti
PC
Varilly
P
Fry
B
Lohmueller
J
Hostetter
E
2007
Genome-wide detection and characterization of positive selection
in human populations.
Nature
449
913
918
18. Barreiro
LB
Laval
G
Quach
H
Patin
E
Quintana-Murci
L
2008
Natural selection has driven population differentiation in modern
humans.
Nat Genet
40
340
345
19. Hellmann
I
Mang
Y
Gu
Z
Li
P
de la Vega
FM
2008
Population genetic analysis of shotgun assemblies of genomic
sequences from multiple individuals.
Genome Res
18
1020
1029
20. Yang
Z
1997
PAML: a program package for phylogenetic analysis by maximum
likelihood.
Comput Appl Biosci
13
555
556
21. Zhang
J
Nielsen
R
Yang
Z
2005
Evaluation of an improved branch-site likelihood method for
detecting positive selection at the molecular level.
Mol Biol Evol
22
2472
2479
22. Kosiol
C
Vinar
T
da Fonseca
RR
Hubisz
MJ
Bustamante
CD
2008
Patterns of positive selection in six Mammalian
genomes.
PLoS Genet
4
e1000144
doi:10.1371/journal.pgen.1000144
23. Bakewell
MA
Shi
P
Zhang
J
2007
More genes underwent positive selection in chimpanzee evolution
than in human evolution.
Proc Natl Acad Sci U S A
104
7489
7494
24. Mallick
S
Gnerre
S
Muller
P
Reich
D
2009
The difficulty of avoiding false positives in genome scans for
natural selection.
Genome Res
19
922
933
25. Zhang
J
2003
Parallel functional changes in the digestive RNases of ruminants
and colobines by divergent amino acid substitutions.
Mol Biol Evol
20
1310
1317
26. Colosimo
PF
Peichel
CL
Nereng
K
Blackman
BK
Shapiro
MD
2004
The genetic architecture of parallel armor plate reduction in
threespine sticklebacks.
PLoS Biol
2
e109
doi:10.1371/journal.pbio.0020109
27. Shapiro
MD
Marks
ME
Peichel
CL
Blackman
BK
Nereng
KS
2004
Genetic and developmental basis of evolutionary pelvic reduction
in threespine sticklebacks.
Nature
428
717
723
28. Colosimo
PF
Hosemann
KE
Balabhadra
S
Villarreal
G
Jr
Dickson
M
2005
Widespread parallel evolution in sticklebacks by repeated
fixation of Ectodysplasin alleles.
Science
307
1928
1933
29. Hoekstra
HE
2006
Genetics, development and evolution of adaptive pigmentation in
vertebrates.
Heredity
97
222
234
30. Zhang
J
2006
Parallel adaptive origins of digestive RNases in Asian and
African leaf monkeys.
Nat Genet
38
819
823
31. Miller
CT
Beleza
S
Pollen
AA
Schluter
D
Kittles
RA
2007
cis-Regulatory changes in Kit ligand expression and parallel
evolution of pigmentation in sticklebacks and humans.
Cell
131
1179
1189
32. Tishkoff
SA
Reed
FA
Ranciaro
A
Voight
BF
Babbitt
CC
2007
Convergent adaptation of human lactase persistence in Africa and
Europe.
Nat Genet
39
31
40
33. Frazer
KA
Ballinger
DG
Cox
DR
Hinds
DA
Stuve
LL
2007
A second generation human haplotype map of over 3.1 million
SNPs.
Nature
449
851
861
34. Hinds
DA
Stuve
LL
Nilsen
GB
Halperin
E
Eskin
E
2005
Whole-genome patterns of common DNA variation in three human
populations.
Science
307
1072
1079
35. Smith
JM
Haigh
J
1974
The hitch-hiking effect of a favourable gene.
Genet Res
23
23
35
36. Hudson
RR
Kreitman
M
Aguade
M
1987
A test of neutral molecular evolution based on nucleotide
data.
Genetics
116
153
159
37. Hoggart
CJ
Chadeau-Hyam
M
Clark
TG
Lampariello
R
Whittaker
JC
2007
Sequence-level population simulations over large genomic
regions.
Genetics
177
1725
1731
38. Chadeau-Hyam
M
Hoggart
CJ
O'Reilly
PF
Whittaker
JC
De Iorio
M
2008
Fregene: simulation of realistic sequence-level data in
populations and ascertained samples.
BMC Bioinformatics
9
364
39. Schaffner
SF
Foo
C
Gabriel
S
Reich
D
Daly
MJ
2005
Calibrating a coalescent simulation of human genome sequence
variation.
Genome Res
15
1576
1583
40. Zhai
W
Nielsen
R
Slatkin
M
2009
An investigation of the statistical power of neutrality tests
based on comparative and population genetic data.
Mol Biol Evol
26
273
283
41. Levy
S
Sutton
G
Ng
PC
Feuk
L
Halpern
AL
2007
The diploid genome sequence of an individual
human.
PLoS Biol
5
e254
doi:10.1371/journal.pbio.0050254
42. Wheeler
DA
Srinivasan
M
Egholm
M
Shen
Y
Chen
L
2008
The complete genome of an individual by massively parallel DNA
sequencing.
Nature
452
872
876
43. Enard
W
Przeworski
M
Fisher
SE
Lai
CS
Wiebe
V
2002
Molecular evolution of FOXP2, a gene involved in speech and
language.
Nature
418
869
872
44. Sturm
RA
Duffy
DL
Zhao
ZZ
Leite
FP
Stark
MS
2008
A single SNP in an evolutionary conserved region within intron 86
of the HERC2 gene determines human blue-brown eye color.
Am J Hum Genet
82
424
431
45. Izagirre
N
Garcia
I
Junquera
C
de la Rua
C
Alonso
S
2006
A scan for signatures of positive selection in candidate loci for
skin pigmentation in humans.
Mol Biol Evol
23
1697
1706
46. Bersaglieri
T
Sabeti
PC
Patterson
N
Vanderploeg
T
Schaffner
SF
2004
Genetic signatures of strong recent positive selection at the
lactase gene.
Am J Hum Genet
74
1111
1120
47. Liao
BY
Zhang
J
2006
Evolutionary conservation of expression profiles between human
and mouse orthologous genes.
Mol Biol Evol
23
530
540
48. Al-Shahrour
F
Diaz-Uriarte
R
Dopazo
J
2004
FatiGO: a web tool for finding significant associations of Gene
Ontology terms with groups of genes.
Bioinformatics
20
578
580
49. Al-Shahrour
F
Minguez
P
Vaquerizas
JM
Conde
L
Dopazo
J
2005
BABELOMICS: a suite of web tools for functional annotation and
analysis of groups of genes in high-throughput experiments.
Nucleic Acids Res
33
W460
464
50. Nielsen
R
Bustamante
C
Clark
AG
Glanowski
S
Sackton
TB
2005
A scan for positively selected genes in the genomes of humans and
chimpanzees.
PLoS Biol
3
e170
doi:10.1371/journal.pbio.0030170
51. 2005
Initial sequence of the chimpanzee genome and comparison with the
human genome.
Nature
437
69
87
52. Gibbs
RA
Rogers
J
Katze
MG
Bumgarner
R
Weinstock
GM
2007
Evolutionary and biomedical insights from the rhesus macaque
genome.
Science
316
222
234
53. Ning
Z
Cox
AJ
Mullikin
JC
2001
SSAHA: a fast search method for large DNA
databases.
Genome Res
11
1725
1729
54. Myers
S
Bottolo
L
Freeman
C
McVean
G
Donnelly
P
2005
A fine-scale map of recombination rates and hotspots across the
human genome.
Science
310
321
324
55. Duret
L
Arndt
PF
2008
The impact of recombination on nucleotide substitutions in the
human genome.
PLoS Genet
4
e1000071
doi:10.1371/journal.pgen.1000071
56. O'Reilly
PF
Birney
E
Balding
DJ
2008
Confounding between recombination and selection, and the Ped/Pop
method for detecting selection.
Genome Res
18
1304
1313
57. Waterston
RH
Lindblad-Toh
K
Birney
E
Rogers
J
Abril
JF
2002
Initial sequencing and comparative analysis of the mouse
genome.
Nature
420
520
562
58. Akey
JM
2009
Constructing genomic maps of positive selection in humans: where
do we go from here?
Genome Res
19
711
722
59. Barreiro
LB
Ben-Ali
M
Quach
H
Laval
G
Patin
E
2009
Evolutionary dynamics of human Toll-like receptors and their
different contributions to host defense.
PLoS Genet
5
e1000562
doi:10.1371/journal.pgen.1000562
60. Oh
B
Hwang
SY
Solter
D
Knowles
BB
1997
Spindlin, a major maternal transcript expressed in the mouse
during the transition from oocyte to embryo.
Development
124
493
503
61. Anderson
RA
Cambray
N
Hartley
PS
McNeilly
AS
2002
Expression and localization of inhibin alpha, inhibin/activin
betaA and betaB and the activin type II and inhibin beta-glycan receptors in
the developing human testis.
Reproduction
123
779
788
62. Chiriva-Internati
M
Gagliano
N
Donetti
E
Costa
F
Grizzi
F
2009
Sperm protein 17 is expressed in the sperm fibrous
sheath.
J Transl Med
7
61
63. Zhang
J
Webb
DM
Podlaha
O
2002
Accelerated protein evolution and origins of human-specific
features: Foxp2 as an example.
Genetics
162
1825
1835
64. Charlesworth
B
Morgan
MT
Charlesworth
D
1993
The effect of deleterious mutations on neutral molecular
variation.
Genetics
134
1289
1303
65. Charlesworth
D
Charlesworth
B
Morgan
MT
1995
The pattern of neutral molecular variation under the background
selection model.
Genetics
141
1619
1632
66. Teshima
KM
Coop
G
Przeworski
M
2006
How reliable are empirical genomic scans for selective
sweeps?
Genome Res
16
702
712
67. Schwartz
S
Kent
WJ
Smit
A
Zhang
Z
Baertsch
R
2003
Human-mouse alignments with BLASTZ.
Genome Res
13
103
107
68. Kent
WJ
2002
BLAT–the BLAST-like alignment tool.
Genome Res
12
656
664
69. Flicek
P
Aken
BL
Beal
K
Ballester
B
Caccamo
M
2008
Ensembl 2008.
Nucleic Acids Res
36
D707
714
70. Katoh
K
Misawa
K
Kuma
K
Miyata
T
2002
MAFFT: a novel method for rapid multiple sequence alignment based
on fast Fourier transform.
Nucleic Acids Res
30
3059
3066
71. 2008
The Gene Ontology project in 2008.
Nucleic Acids Res
36
D440
444
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