Evidence for Pervasive Adaptive Protein Evolution in Wild Mice
The relative contributions of neutral and adaptive substitutions to molecular evolution has been one of the most controversial issues in evolutionary biology for more than 40 years. The analysis of within-species nucleotide polymorphism and between-species divergence data supports a widespread role for adaptive protein evolution in certain taxa. For example, estimates of the proportion of adaptive amino acid substitutions (α) are 50% or more in enteric bacteria and Drosophila. In contrast, recent estimates of α for hominids have been at most 13%. Here, we estimate α for protein sequences of murid rodents based on nucleotide polymorphism data from multiple genes in a population of the house mouse subspecies Mus musculus castaneus, which inhabits the ancestral range of the Mus species complex and nucleotide divergence between M. m. castaneus and M. famulus or the rat. We estimate that 57% of amino acid substitutions in murids have been driven by positive selection. Hominids, therefore, are exceptional in having low apparent levels of adaptive protein evolution. The high frequency of adaptive amino acid substitutions in wild mice is consistent with their large effective population size, leading to effective natural selection at the molecular level. Effective natural selection also manifests itself as a paucity of effectively neutral nonsynonymous mutations in M. m. castaneus compared to humans.
Vyšlo v časopise:
Evidence for Pervasive Adaptive Protein Evolution in Wild Mice. PLoS Genet 6(1): e32767. doi:10.1371/journal.pgen.1000825
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000825
Souhrn
The relative contributions of neutral and adaptive substitutions to molecular evolution has been one of the most controversial issues in evolutionary biology for more than 40 years. The analysis of within-species nucleotide polymorphism and between-species divergence data supports a widespread role for adaptive protein evolution in certain taxa. For example, estimates of the proportion of adaptive amino acid substitutions (α) are 50% or more in enteric bacteria and Drosophila. In contrast, recent estimates of α for hominids have been at most 13%. Here, we estimate α for protein sequences of murid rodents based on nucleotide polymorphism data from multiple genes in a population of the house mouse subspecies Mus musculus castaneus, which inhabits the ancestral range of the Mus species complex and nucleotide divergence between M. m. castaneus and M. famulus or the rat. We estimate that 57% of amino acid substitutions in murids have been driven by positive selection. Hominids, therefore, are exceptional in having low apparent levels of adaptive protein evolution. The high frequency of adaptive amino acid substitutions in wild mice is consistent with their large effective population size, leading to effective natural selection at the molecular level. Effective natural selection also manifests itself as a paucity of effectively neutral nonsynonymous mutations in M. m. castaneus compared to humans.
Zdroje
1. AndolfattoP
2001 Adaptive hitchhiking effects on genome variability. Curr Opin Genet Dev 11 635 641
2. NielsenR
2005 Molecular signatures of natural selection. Annu Rev Genet 39 197 218
3. MacphersonJM
SellaG
DavisJC
PetrovDA
2007 Genomewide spatial correspondence between nonsynonymous divergence and neutral polymorphism reveals extensive adaptation in Drosophila. Genetics 177 2083 2099
4. McVickerG
GordonD
DavisC
GreenP
2009 Widespread genomic signatures of natural selection in hominid evolution. PLoS Genet 5 e1000471 doi:10.1371/journal.pgen.1000471
5. HindsDA
StuveLL
NilsenGB
HalperinE
EskinE
2005 Whole-genome patterns of common DNA variation in three human populations. Science 307 1072 1079
6. CoopG
PickrellJK
NovembreJ
KudaravalliS
LiJ
2009 The Role of Geography in Human Adaptation. PLoS Genet 5 e1000500 doi:10.1371/journal.pgen.1000500
7. McDonaldJH
KreitmanM
1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 652 654
8. FayJC
WyckoffGJ
WuCI
2001 Positive and negative selection on the human genome. Genetics 158 1227 1234
9. SmithNG
Eyre-WalkerA
2002 Adaptive protein evolution in Drosophila. Nature 415 1022 1024
10. CharlesworthJ
Eyre-WalkerA
2006 The rate of adaptive evolution in enteric bacteria. Mol Biol Evol 23 1348 1356
11. ShapiroJA
HuangW
ZhangC
HubiszMJ
LuJ
2007 Adaptive genic evolution in the Drosophila genomes. Proc Natl Acad Sci U S A 104 2271 2276
12. MasideX
CharlesworthB
2007 Patterns of molecular variation and evolution in Drosophila americana and its relatives. Genetics 176 2293 2305
13. BachtrogD
2008 Similar rates of protein adaptation in Drosophila miranda and D. melanogaster, two species with different current effective population sizes. BMC Evol Biol 8 334 334
14. DonigerSW
KimHS
SwainD
CorcueraD
WilliamsM
2008 A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet 4 e1000183 doi:10.1371/journal.pgen.1000183
15. LitiG
CarterDM
MosesAM
WarringerJ
PartsL
2009 Population genomics of domestic and wild yeasts. Nature 458 337 341
16. FoxeJP
DarVU
ZhengH
NordborgM
GautBS
2008 Selection on amino acid substitutions in Arabidopsis. Mol Biol Evol 25 1375 1383
17. Chimpanzee Sequencing and Analysis Consortium 2005 Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437 69 87
18. ZhangL
LiWH
2005 Human SNPs reveal no evidence of frequent positive selection. Mol Biol Evol 22 2504 2507
19. GojoboriJ
TangH
AkeyJM
WuCI
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
20. BoykoAR
WilliamsonSH
IndapAR
DegenhardtJD
HernandezRD
2008 Assessing the evolutionary impact of amino acid mutations in the human genome. PLoS Genet 4 e1000083 doi:10.1371/journal.pgen.1000083
21. CharlesworthJ
Eyre-WalkerA
2008 The McDonald-Kreitman test and slightly deleterious mutations. Mol Biol Evol 25 1007 1015
22. Eyre-WalkerA
KeightleyPD
2009 Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size changes. Mol Biol Evol 26 2097 2108
23. TakahataN
1993 Allelic genealogy and human evolution. Mol Biol Evol 10 2 22
24. PatwaZ
WahlL
2008 The fixation probability of beneficial mutations. J R Soc Interface 5 1279 1289
25. DinW
AnandR
BoursotP
DarvicheD
DodB
1996 Origin and radiation of the house mouse: clues from nuclear genes. J Evol Biol 9 519 539
26. BainesJF
HarrB
2007 Reduced X-linked diversity in derived populations of house mice. Genetics 175 1911 1921
27. KeightleyPD
Eyre-WalkerA
2000 Deleterious mutations and the evolution of sex. Science 290 331 333
28. LivingstonRJ
von NiederhausernA
JeggaAG
CrawfordDC
CarlsonCS
2004 Pattern of sequence variation across 213 environmental response genes. Genome Res 14 1821 1831
29. TajimaF
1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 585 595
30. GeraldesA
BassetP
GibsonB
SmithKL
HarrB
2008 Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol Ecol 17 5349 5363
31. SalcedoT
GeraldesA
NachmanMW
2007 Nucleotide variation in wild and inbred mice. Genetics 177 2277 2291
32. KeightleyPD
Eyre-WalkerA
2007 Joint inference of the distribution of fitness effects of deleterious mutations and population demography based on nucleotide polymorphism frequencies. Genetics 177 2251 2261
33. AkeyJM
EberleMA
RiederMJ
CarlsonCS
ShriverMD
2004 Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol 2 e286 doi:10.1371/journal.pbio.0020286
34. BegunDJ
HollowayAK
StevensK
HillierLW
PohYP
2007 Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5 e310 doi:10.1371/journal.pbio.0050310
35. AndolfattoP
2007 Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Res 12 1755 1762
36. PritchardJK
StephensM
DonnellyP
2000 Inference of population structure using multilocus genotype data. Genetics 155 945 959
37. BronsonFH
1979 The reproductive ecology of the house mouse. Q Rev Biol 54 265 299
38. WeirB
CockerhamCC
1984 Estimating F-statistics for the analysis of population structure. Evolution 38 1358 1370
39. CaswellJL
MallickS
RichterDJ
NeubauerJ
SchirmerC
2008 Analysis of chimpanzee history based on genome sequence alignments. PLoS Genet 4 e1000057 doi:10.1371/journal.pgen.1000057
40. YuN
Jensen-SeamanMI
ChemnickL
RyderO
LiWH
2004 Nucleotide diversity in gorillas. Genetics 166 1375 1383
41. HaygoodR
FedrigoO
HansonB
YokoyamaKD
WrayGA
2007 Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet 39 1140 1144
42. Eyre-WalkerA
2002 Changing effective population size and the McDonald-Kreitman test. Genetics 162 2017 2024
43. BurgessR
YangZ
1994 Estimation of hominoid ancestral population sizes under bayesian coalescent models incorporating mutation rate variation and sequencing errors. Mol Biol Evol 25 1979 1994
44. Eyre-WalkerA
WoolfitM
PhelpsT
2006 The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173 891 900
45. RozenS
SkaletskyH
2000 Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132 365 386
46. AltschulSF
GishW
MillerW
MyersEW
LipmanDJ
1990 Basic local alignment search tool. J Mol Evol 215 403 410
47. BrayN
PachterL
2004 MAVID: Constrained ancestral alignment of multiple sequences. Genome Res 14 693 699
48. WattersonGA
1975 On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7 256 276
49. TajimaF
1983 Evolutionary relationship of DNA sequences in finite populations. Genetics 105 437 460
50. KimuraM
1957 Some problems of stochastic processes in genetics. Ann Math Stat 28 882 901
51. BonhommeF
RivalsE
OrthA
GrantGR
JeffreysAJ
2007 Species-wide distribution of highly polymorphic minisatellite markers suggests past and present genetic exchanges among house mouse subspecies. Genome Biol 8 R80
52. NachmanMW
CrowellSL
2000 Estimate of the mutation rate per nucleotide in humans. Genetics 156 297 304
53. Haag-LiautardC
DorrisM
MasideX
MacaskillS
HalliganDL
2007 Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445 82 85
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 1
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- A Major Role of the RecFOR Pathway in DNA Double-Strand-Break Repair through ESDSA in
- Kidney Development in the Absence of and Requires
- The Werner Syndrome Protein Functions Upstream of ATR and ATM in Response to DNA Replication Inhibition and Double-Strand DNA Breaks
- Alternative Epigenetic Chromatin States of Polycomb Target Genes