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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

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