Systematic Detection of Polygenic Regulatory
Evolution
The idea that most morphological adaptations can be attributed to changes in the
cis-regulation of gene expression levels has been gaining
increasing acceptance, despite the fact that only a handful of such cases have
so far been demonstrated. Moreover, because each of these cases involves only
one gene, we lack any understanding of how natural selection may act on
cis-regulation across entire pathways or networks. Here we
apply a genome-wide test for selection on cis-regulation to two
subspecies of the mouse Mus musculus. We find evidence for
lineage-specific selection at over 100 genes involved in diverse processes such
as growth, locomotion, and memory. These gene sets implicate candidate genes
that are supported by both quantitative trait loci and a validated
causality-testing framework, and they predict a number of phenotypic
differences, which we confirm in all four cases tested. Our results suggest that
gene expression adaptation is widespread and that these adaptations can be
highly polygenic, involving cis-regulatory changes at numerous
functionally related genes. These coordinated adaptations may contribute to
divergence in a wide range of morphological, physiological, and behavioral
phenotypes.
Vyšlo v časopise:
Systematic Detection of Polygenic Regulatory
Evolution. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1002023
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002023
Souhrn
The idea that most morphological adaptations can be attributed to changes in the
cis-regulation of gene expression levels has been gaining
increasing acceptance, despite the fact that only a handful of such cases have
so far been demonstrated. Moreover, because each of these cases involves only
one gene, we lack any understanding of how natural selection may act on
cis-regulation across entire pathways or networks. Here we
apply a genome-wide test for selection on cis-regulation to two
subspecies of the mouse Mus musculus. We find evidence for
lineage-specific selection at over 100 genes involved in diverse processes such
as growth, locomotion, and memory. These gene sets implicate candidate genes
that are supported by both quantitative trait loci and a validated
causality-testing framework, and they predict a number of phenotypic
differences, which we confirm in all four cases tested. Our results suggest that
gene expression adaptation is widespread and that these adaptations can be
highly polygenic, involving cis-regulatory changes at numerous
functionally related genes. These coordinated adaptations may contribute to
divergence in a wide range of morphological, physiological, and behavioral
phenotypes.
Zdroje
1. Prud'hommeBGompelNCarrollSB
2007
Emerging principles of regulatory evolution.
Proc Natl Acad Sci U S A
104
Suppl 1
8605
8612
2. HoekstraHECoyneJA
2007
The locus of evolution: Evo devo and the genetics of
adaptation.
Evolution
61
995
1016
3. FraserHB
Gene expression adaptation: from single genes to genomes.
Bioessays, accepted for publication
4. WrayGA
2007
The evolutionary significance of cis-regulatory
mutations.
Nat Rev Genet
8
206
5. SternDLOrgogozoV
2008
The loci of evolution: how predictable is genetic
evolution?
Evolution
62
2155
6. PollardKSSalamaSRLambertNLambotMACoppensS
2006
An RNA gene expressed during cortical development evolved rapidly
in humans.
Nature
443
167
172
7. HaygoodRFedrigoOHansonBYokoyamaKDWrayGA
2007
Promoter regions of many neural- and nutrition-related genes have
experienced positive selection during human evolution.
Nat Genet
39
1140
1144
8. PrabhakarSNoonanJPPääboSRubinEM
2006
Accelerated evolution of conserved noncoding sequences in
humans.
Science
314
786
9. AndolfattoP
2005
Adaptive evolution of non-coding DNA in
Drosophila.
Nature
437
1149
1152
10. GaltierNDuretL
2007
Adaptation or biased gene conversion? Extending the null
hypothesis of molecular evolution.
Trends Genet
23
273
277
11. FayJCWittkoppPJ
2008
Evaluating the role of natural selection in the evolution of gene
regulation.
Heredity
100
191
199
12. OleksiakMFChurchillGACrawfordDL
2002
Variation in gene expression within and among natural
populations.
Nat Genet
32
261
13. BlekhmanROshlackAChabotAESmythGKGiladY
2008
Gene regulation in primates evolves under tissue-specific
selection pressures.
PLoS Genet
4
e1000271
doi:10.1371/journal.pgen.1000271
14. GiladYOshlackASmythGKSpeedTPWhiteKP
2006
Expression profiling in primates reveals a rapid evolution of
human transcription factors.
Nature
440
242
15. DenverDRMorrisKStreelmanJTKimSKLynchM
2005
The transcriptional consequences of mutation and natural
selection in Caenorhabditis elegans.
Nat Genet
37
544
16. RifkinSAHouleDKimJWhiteKP
2005
A mutation accumulation assay reveals a broad capacity for rapid
evolution of gene expression.
Nature
438
220
17. LandryCRLemosBRifkinSADickinsonWJHartlDL
2007
Genetic properties influencing the evolvability of gene
expression.
Science
317
118
18. FraserHBMosesASchadtEE
2010
Evidence for widespread adaptive evolution of gene expression in
budding yeast.
Proc Natl Acad Sci U S A
107
2977
2982
19. BullardJHMostovoyYDudoitSBremRB
2010
Polygenic and directional regulatory evolution across pathways in
Saccharomyces.
Proc Natl Acad Sci U S A
107
5058
5063
20. GibsonGWeirB
2005
The quantitative genetics of transcription.
Trends Genet
21
616
623
21. SteinerCCWeberJNHoekstraHE
2007
Adaptive variation in beach mice produced by two interacting
pigmentation genes.
PLoS Biol
5
e219
doi:10.1371/journal.pbio.0050219
22. OrrHA
1998
Testing natural selection versus genetic drift in phenotypic
evolution using quantitative trait locus data.
Genetics
149
2099
2104
23. DossSSchadtEEDrakeTALusisAJ
2005
Cis-acting expression quantitative trait loci in
mice.
Genome Res
15
681
691
24. McDonaldJHKreitmanM
1991
Adaptive protein evolution at the Adh locus in
Drosophila.
Nature
351
652
25. HughesAL
2007
Looking for Darwin in all the wrong places: the misguided quest
for positive selection at the nucleotide sequence level.
Heredity
99
364
373
26. FrazerKAEskinEKangHMBogueMAHindsDA
2007
A sequence-based variation map of 8.27 million SNPs in inbred
mouse strains.
Nature
448
1050
1053
27. GeraldesABassetPGibsonBSmithKLHarrB
2008
Inferring the history of speciation in house mice from autosomal,
X-linked, Y-linked and mitochondrial genes.
Mol Ecol
17
5349
5363
28. The Gene Ontology Consortium
2000
Gene Ontology: tool for the unification of
biology.
Nat Genet
25
25
29
29. KanehisaMGotoSHattoriMAoki-KinoshitaKFItohM
2006
From genomics to chemical genomics: new developments in
KEGG.
Nucleic Acids Res
34
D354
D357
30. BabakTDevealeBArmourCRaymondCClearyMA
2008
Global survey of genomic imprinting by transcriptome
sequencing.
Curr Biol
18
1735
1741
31. WangXSunQMcGrathSDMardisERSolowayPD
2008
Transcriptome-wide identification of novel imprinted genes in
neonatal mouse brain.
PLoS ONE
3
e3839
doi:10.1371/journal.pone.0003839
32. BabakT
2010
Genetic validation of whole-transcriptome sequencing for mapping
expression affected by cis-regulatory
variation.
BMC Genomics
11
473
33. BabakTGarrett-EngelePArmourCDRaymondCKKellerMP
2009
The Mouse Genome Database genotypes::phenotypes.
Nucl Acids Res
37
D712
D719
34. BouwmanPGöllnerHElsässerHPEckhoffGKarisA
2000
Transcription factor Sp3 is essential for post-natal survival and
late tooth development.
EMBO J
19
655
661
35. SimmerFMoormanCvan der LindenAMKuijkEvan den BerghePV
2003
Genome-wide RNAi of C. elegans using the
hypersensitive rrf-3 strain reveals novel gene
functions.
PLoS Biol
1
e12
doi:10.1371/journal.pbio.0000012
36. SchadtEELambJYangXZhuJEdwardsS
2005
An integrative genomics approach to infer causal associations
between gene expression and disease.
Nat Genet
37
710
717
37. MillsteinJZhangBZhuJSchadtEE
2009
Disentangling molecular relationships with a causal inference
test.
BMC Genet
10
23
38. YangXDeignanJLQiHZhuJQianS
2009
Validation of candidate causal genes for obesity that affect
shared metabolic pathways and networks.
Nat Genet
41
415
423
39. BachmanovAAReedDRBeauchampGKTordoffMG
2002
Food intake, water intake, and drinking spout side preference of
28 mouse strains.
Behav Genet
32
435
443
40. Le RoyIRoubertouxPLJamotLMaaroufFTordjmanS
1998
Neuronal and behavioral differences between Mus musculus
domesticus (C57BL/6JBy) and Mus musculus
castaneus (CAST/Ei).
Behav Brain Res
95
135
142
41. KoideTMoriwakiKIkedaKNikiHShiroishiT
2000
Multi-phenotype behavioral characterization of inbred strains
derived from wild stocks of Mus musculus.
Mamm Genome
11
664
670
42. BrownREWongAA
2007
The influence of visual ability on learning and memory
performance in 13 strains of mice.
Learn Mem
14
134
144
43. SakaiTKikkawaYMiuraIInoueTMoriwakiK
2005
Origins of mouse inbred strains deduced from whole-genome
scanning by polymorphic microsatellite loci.
Mamm Genome
16
11
19
44. SchlosserG
2002
Modularity and the units of evolution.
Theory in Biosciences
121
1
80
45. GrazeRMMcIntyreLMMainBJWayneMLNuzhdinSV
2009
Regulatory divergence in Drosophila melanogaster
and D. simulans, a genomewide analysis of allele-specific
expression.
Genetics
183
547
561
46. ZhangXBorevitzJO
2009
Global analysis of allele-specific expression in
Arabidopsis thaliana.
Genetics
182
943
954
47. GompelNPrud'hommeBWittkoppPJKassnerVACarrollSB
2005
Chance caught on the wing: cis-regulatory evolution and the
origin of pigment patterns in Drosophila.
Nature
433
481
487
48. MillerCTBelezaSPollenAASchluterDKittlesRA
2007
cis-Regulatory changes in Kit ligand expression
and parallel evolution of pigmentation in sticklebacks and
humans.
Cell
131
1179
1189
49. ShapiroMDMarksMEPeichelCLBlackmanBKNerengKS
2004
Genetic and developmental basis of evolutionary pelvic reduction
in threespine sticklebacks.
Nature
428
717
723
50. HaygoodRBabbittCCFedrigoOWrayGA
2010
Contrasts between adaptive coding and noncoding changes during
human evolution.
Proc Natl Acad Sci U S A
107
7853
7857
51. LiaoBYWengMPZhangJ
2010
Contrasting genetic paths to morphological and physiological
evolution.
Proc Natl Acad Sci U S A
107
7353
7358
52. HeYDDaiHSchadtEECavetGEdwardsSW
2003
Microarray standard data set and figures of merit for comparing
data processing methods and experiment designs.
Bioinformatics
19
956
965
53. ZhuJLumPYLambJGuhaThakurtaDEdwardsSW
2004
An integrative genomics approach to the reconstruction of gene
networks in segregating populations. Cytogenet.
Genome Res
105
363
374
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