#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Background Selection as Baseline for Nucleotide Variation across the Genome


The removal of deleterious mutations from natural populations has potential consequences on patterns of variation across genomes. Population genetic analyses, however, often assume that such effects are negligible across recombining regions of species like Drosophila. We use simple models of purifying selection and current knowledge of recombination rates and gene distribution across the genome to obtain a baseline of variation predicted by the constant input and removal of deleterious mutations. We find that purifying selection alone can explain a major fraction of the observed variance in nucleotide diversity across the genome. The use of a baseline of variation predicted by linkage to deleterious mutations as null expectation exposes genomic regions under other selective regimes, including more regions showing the signature of balancing selection than would be evident when using traditional approaches. Our study also indicates that most, if not all, nucleotides across the D. melanogaster genome are significantly influenced by the removal of deleterious mutations, even when located in the middle of highly recombining regions and distant from genes. Additionally, the study of rates of protein evolution confirms previous analyses suggesting that the recombination landscape across the genome has changed in the recent history of D. melanogaster. All these reported factors can skew current analyses designed to capture demographic events or estimate the strength and frequency of adaptive mutations, and illustrate the need for new and more realistic theoretical and modeling approaches to study naturally occurring genetic variation.


Vyšlo v časopise: Background Selection as Baseline for Nucleotide Variation across the Genome. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004434
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004434

Souhrn

The removal of deleterious mutations from natural populations has potential consequences on patterns of variation across genomes. Population genetic analyses, however, often assume that such effects are negligible across recombining regions of species like Drosophila. We use simple models of purifying selection and current knowledge of recombination rates and gene distribution across the genome to obtain a baseline of variation predicted by the constant input and removal of deleterious mutations. We find that purifying selection alone can explain a major fraction of the observed variance in nucleotide diversity across the genome. The use of a baseline of variation predicted by linkage to deleterious mutations as null expectation exposes genomic regions under other selective regimes, including more regions showing the signature of balancing selection than would be evident when using traditional approaches. Our study also indicates that most, if not all, nucleotides across the D. melanogaster genome are significantly influenced by the removal of deleterious mutations, even when located in the middle of highly recombining regions and distant from genes. Additionally, the study of rates of protein evolution confirms previous analyses suggesting that the recombination landscape across the genome has changed in the recent history of D. melanogaster. All these reported factors can skew current analyses designed to capture demographic events or estimate the strength and frequency of adaptive mutations, and illustrate the need for new and more realistic theoretical and modeling approaches to study naturally occurring genetic variation.


Zdroje

1. CharlesworthB (2012) The effects of deleterious mutations on evolution at linked sites. Genetics 190: 5–22.

2. GillespieJH (2000) Genetic drift in an infinite population. The pseudohitchhiking model. Genetics 155: 909–919.

3. BartonNH (2010) Genetic linkage and natural selection. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 365: 2559–2569.

4. StephanW (2010) Genetic hitchhiking versus background selection: the controversy and its implications. Philos Trans R Soc Lond B Biol Sci 365: 1245–1253.

5. CutterAD, PayseurBA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14: 262–274.

6. FayJC (2011) Weighing the evidence for adaptation at the molecular level. Trends Genet 27: 343–349.

7. BartonNH (2000) Genetic hitchhiking. Philos Trans R Soc Lond B Biol Sci 355: 1553–1562.

8. Maynard SmithJ, HaighJ (1974) The hitch-hiking effect of a favorable gene. Genet Res 23: 23–35.

9. StephanW, SongYS, LangleyCH (2006) The hitchhiking effect on linkage disequilibrium between linked neutral loci. Genetics 172: 2647–2663.

10. HillWG, RobertsonA (1966) The effect of linkage on limits to artificial selection. Genetical Research 8: 269–294.

11. BravermanJM, HudsonRR, KaplanNL, LangleyCH, StephanW (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140: 783–796.

12. CharlesworthB, MorganMT, CharlesworthD (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289–1303.

13. CharlesworthB (1994) The effect of background selection against deleterious mutations on weakly selected, linked variants. Genetical Research 63: 213–227.

14. CharlesworthB, BetancourtAJ, KaiserVB, GordoI (2009) Genetic recombination and molecular evolution. Cold Spring Harbor Symposia on Quantitative Biology 74: 177–186.

15. HudsonRR, KaplanNL (1995) Deleterious background selection with recombination. Genetics 141: 1605–1617.

16. NordborgM, CharlesworthB, CharlesworthD (1996) The effect of recombination on background selection. Genet Res 67: 159–174.

17. McVickerG, GordonD, DavisC, GreenP (2009) Widespread genomic signatures of natural selection in hominid evolution. PLoS Genet 5: e1000471.

18. HernandezRD, KelleyJL, ElyashivE, MeltonSC, AutonA, et al. (2011) Classic selective sweeps were rare in recent human evolution. Science 331: 920–924.

19. LohmuellerKE, AlbrechtsenA, LiY, KimSY, KorneliussenT, et al. (2011) Natural selection affects multiple aspects of genetic variation at putatively neutral sites across the human genome. PLoS Genet 7: e1002326.

20. ChunS, FayJC (2011) Evidence for hitchhiking of deleterious mutations within the human genome. PLoS Genet 7: e1002240.

21. ReedFA, AkeyJM, AquadroCF (2005) Fitting background-selection predictions to levels of nucleotide variation and divergence along the human autosomes. Genome Res 15: 1211–1221.

22. SellaG, PetrovDA, PrzeworskiM, AndolfattoP (2009) Pervasive natural selection in the Drosophila genome? PLoS Genet 5: e1000495.

23. MacphersonJM, SellaG, DavisJC, PetrovDA (2007) Genomewide spatial correspondence between nonsynonymous divergence and neutral polymorphism reveals extensive adaptation in Drosophila. Genetics 177: 2083–2099.

24. BegunDJ, HollowayAK, StevensK, HillierLW, PohYP, et al. (2007) Population genomics: Whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5: e310.

25. AndolfattoP (2007) Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Res 17: 1755–1762.

26. LangleyCH, StevensK, CardenoC, LeeYC, SchriderDR, et al. (2012) Genomic variation in natural populations of Drosophila melanogaster. Genetics 195: 7–8.

27. WrightSI, AndolfattoP (2008) The impact of natural selection on the genome: Emerging patterns in Drosophila and Arabidopsis. Annual Review of Ecology Evolution and Systematics 39: 193–213.

28. HahnMW (2008) Toward a selection theory of molecular evolution. Evolution 62: 255–265.

29. JensenJD, ThorntonKR, AndolfattoP (2008) An approximate bayesian estimator suggests strong, recurrent selective sweeps in Drosophila. PLoS Genet 4: e1000198.

30. CharlesworthB (1996) Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet Res 68: 131–149.

31. ComeronJM, RatnappanR, BailinS (2012) The many landscapes of recombination in Drosophila melanogaster. PLoS Genet 8: e1002905.

32. SinghND, StoneEA, AquadroCF, ClarkAG (2013) Fine-scale heterogeneity in crossover rate in the garnet-scalloped region of the Drosophila melanogaster X chromosome. Genetics 194: 375–387.

33. CharlesworthB (2012) The role of background selection in shaping patterns of molecular evolution and variation: evidence from variability on the Drosophila X chromosome. Genetics 191: 233–246.

34. MesserPW, PetrovDA (2013) Frequent adaptation and the McDonald-Kreitman test. Proc Natl Acad Sci U S A 110: 8615–8620.

35. WeissmanDB, BartonNH (2012) Limits to the rate of adaptive substitution in sexual populations. PLoS Genet 8: e1002740.

36. AndolfattoP (2005) Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149–1152.

37. CasillasS, BarbadillaA, BergmanCM (2007) Purifying selection maintains highly conserved noncoding sequences in Drosophila. Mol Biol Evol 24: 2222–2234.

38. HaddrillPR, LoeweL, CharlesworthB (2010) Estimating the parameters of selection on nonsynonymous mutations in Drosophila pseudoobscura and D. miranda. Genetics 185: 1381–1396.

39. SawyerSA, KulathinalRJ, BustamanteCD, HartlDL (2003) Bayesian analysis suggests that most amino acid replacements in Drosophila are driven by positive selection. J Mol Evol 57: S154–S164.

40. LoeweL, CharlesworthB, BartolomeC, NoelV (2006) Estimating selection on nonsynonymous mutations. Genetics 172: 1079–1092.

41. PiganeauG, Eyre-WalkerA (2003) Estimating the distribution of fitness effects from DNA sequence data: implications for the molecular clock. Proc Natl Acad Sci U S A 100: 10335–10340.

42. NielsenR, YangZ (2003) Estimating the distribution of selection coefficients from phylogenetic data with applications to mitochondrial and viral DNA. Mol Biol Evol 20: 1231–1239.

43. BustamanteCD, NielsenR, HartlDL (2003) Maximum likelihood and Bayesian methods for estimating the distribution of selective effects among classes of mutations using DNA polymorphism data. Theor Popul Biol 63: 91–103.

44. Eyre-WalkerA, KeightleyPD (2007) The distribution of fitness effects of new mutations. Nat Rev Genet 8: 610–618.

45. LoeweL, CharlesworthB (2007) Background selection in single genes may explain patterns of codon bias. Genetics 175: 1381–1393.

46. KousathanasA, KeightleyPD (2013) A comparison of models to infer the distribution of fitness effects of new mutations. Genetics 193: 1197–1208.

47. Haag-LiautardC, DorrisM, MasideX, MacaskillS, HalliganDL, et al. (2007) Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445: 82–85.

48. SchriderDR, HouleD, LynchM, HahnMW (2013) Rates and genomic consequences of spontaneous mutational events in Drosophila melanogaster. Genetics 194: 937–954.

49. KeightleyPD, TrivediU, ThomsonM, OliverF, KumarS, et al. (2009) Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res 19: 1195–1201.

50. KeightleyPD, NessRW, HalliganDL, HaddrillPR (2014) Estimation of the spontaneous mutation rate per nucleotide site in a Drosophila melanogaster full-sib family. Genetics 196: 313–320.

51. MontgomeryEA, LangleyCH (1983) Transposable elements in mendelian populations. II. Distribution of three COPIA-like elements in a natural population of Drosophila melanogaster. Genetics 104: 473–483.

52. KaplanN, DardenT, LangleyCH (1985) Evolution and extinction of transposable elements in Mendelian populations. Genetics 109: 459–480.

53. CharlesworthB, LangleyCH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 23: 251–287.

54. CharlesworthB, LapidA, CanadaD (1992) The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genet Res 60: 103–114.

55. NuzhdinSV, MackayTF (1995) The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol 12: 180–181.

56. SacktonTB, KulathinalRJ, BergmanCM, QuinlanAR, DopmanEB, et al. (2009) Population genomic inferences from sparse high-throughput sequencing of two populations of Drosophila melanogaster. Genome Biol Evol 1: 449–465.

57. LeeYC, LangleyCH (2010) Transposable elements in natural populations of Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci 365: 1219–1228.

58. PetrovDA, Fiston-LavierAS, LipatovM, LenkovK, GonzalezJ (2011) Population genomics of transposable elements in Drosophila melanogaster. Mol Biol Evol 28: 1633–1644.

59. KoflerR, BetancourtAJ, SchlottererC (2012) Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet 8: e1002487.

60. CridlandJM, MacdonaldSJ, LongAD, ThorntonKR (2013) Abundance and distribution of transposable elements in two Drosophila QTL mapping resources. Mol Biol Evol 30: 2311–2327.

61. VicosoB, CharlesworthB (2009) Recombination rates may affect the ratio of X to autosomal noncoding polymorphism in African populations of Drosophila melanogaster. Genetics 181: 1699–1701; author reply 1703.

62. PoolJE, Corbett-DetigRB, SuginoRP, StevensKA, CardenoCM, et al. (2012) Population genomics of sub-saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet 8: e1003080.

63. KaplanNL, HudsonRR, LangleyCH (1989) The “hitchhiking effect” revisited. Genetics 123: 887–899.

64. KolaczkowskiB, KernAD, HollowayAK, BegunDJ (2011) Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 187: 245–260.

65. PasyukovaEG, VieiraC, MackayTF (2000) Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics 156: 1129–1146.

66. De LucaM, RoshinaNV, Geiger-ThornsberryGL, LymanRF, PasyukovaEG, et al. (2003) Dopa decarboxylase (Ddc) affects variation in Drosophila longevity. Nat Genet 34: 429–433.

67. NuzhdinSV, KhazaeliAA, CurtsingerJW (2005) Survival analysis of life span quantitative trait loci in Drosophila melanogaster. Genetics 170: 719–731.

68. CirulliET, KlimanRM, NoorMAF (2007) Fine-scale crossover rate heterogeneity in Drosophila pseudoobscura. J Mol Evol 64: 129–135.

69. TajimaF (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

70. FelsensteinJ (1974) The evolutionary advantage of recombination. Genetics 78: 737–756.

71. KlimanRM, HeyJ (1993) Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol 10: 1239–1258.

72. McVeanGA, CharlesworthB (2000) The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155: 929–944.

73. ComeronJM, KreitmanM (2002) Population, evolutionary and genomic consequences of interference selection. Genetics 161: 389–410.

74. HeyJ, KlimanRM (2002) Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics 160: 595.

75. ComeronJM, WillifordA, KlimanRM (2008) The Hill-Robertson effect: evolutionary consequences of weak selection and linkage in finite populations. Heredity (Edinb) 100: 19–31.

76. WillifordA, ComeronJM (2010) Local effects of limited recombination: historical perspective and consequences for population estimates of adaptive evolution. J Hered 101(Suppl 1): S127–134.

77. HaddrillPR, HalliganDL, TomarasD, CharlesworthB (2007) Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol 8: R18.

78. CamposJL, CharlesworthB, HaddrillPR (2012) Molecular evolution in nonrecombining regions of the Drosophila melanogaster genome. Genome Biol Evol 4: 278–288.

79. PresgravesDC (2005) Recombination enhances protein adaptation in Drosophila melanogaster. Current Biology 15: 1651–1656.

80. BetancourtAJ, PresgravesDC (2002) Linkage limits the power of natural selection in Drosophila. Proceedings of the National Academy of Sciences, USA 99: 13616–13620.

81. ZhangZ, ParschJ (2005) Positive correlation between evolutionary rate and recombination rate in Drosophila genes with male-biased expression. Mol Biol Evol 22: 1945–1947.

82. MaraisG, Domazet-LosoT, TautzD, CharlesworthB (2004) Correlated evolution of synonymous and nonsynonymous sites in Drosophila. Journal of Molecular Evolution 59: 771–779.

83. ComeronJM, KreitmanM, AguadeM (1999) Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151: 239–249.

84. LarracuenteAM, SacktonTB, GreenbergAJ, WongA, SinghND, et al. (2008) Evolution of protein-coding genes in Drosophila. Trends Genet 24: 114–123.

85. BetancourtAJ, WelchJJ, CharlesworthB (2009) Reduced effectiveness of selection caused by a lack of recombination. Current Biology 19: 655–660.

86. TamuraK, SubramanianS, KumarS (2004) Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21: 36–44.

87. TrueJR, MercerJM, LaurieCC (1996) Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142: 507–523.

88. McGaughSE, HeilCS, Manzano-WinklerB, LoeweL, GoldsteinS, et al. (2012) Recombination modulates how selection affects linked sites in Drosophila. PLoS Biol 10: e1001422.

89. SmukowskiCS, NoorMA (2011) Recombination rate variation in closely related species. Heredity (Edinb) 107: 496–508.

90. FayJC, WyckoffGJ, WuCI (2002) Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415: 1024–1026.

91. Eyre-WalkerA, KeightleyPD (2009) Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Mol Biol Evol 26: 2097–2108.

92. SmithNG, Eyre-WalkerA (2002) Adaptive protein evolution in Drosophila. Nature 415: 1022–1024.

93. WrightS (1938) Size of population and breeding structure in relation to evolution. Science 87: 430–431.

94. MesserPW (2013) SLiM: simulating evolution with selection and linkage. Genetics 194: 1037–1039.

95. KeightleyPD, Eyre-WalkerA (2012) Estimating the rate of adaptive molecular evolution when the evolutionary divergence between species is small. J Mol Evol 74: 61–68.

96. KaiserVB, CharlesworthB (2009) The effects of deleterious mutations on evolution in non-recombining genomes. Trends Genet 25: 9–12.

97. SegerJ, SmithWA, PerryJJ, HunnJ, KaliszewskaZA, et al. (2010) Gene genealogies strongly distorted by weakly interfering mutations in constant environments. Genetics 184: 529–545.

98. FuYX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.

99. GordoI, NavarroA, CharlesworthB (2002) Muller's ratchet and the pattern of variation at a neutral locus. Genetics 161: 835–848.

100. CharlesworthD, CharlesworthB, MorganMT (1995) The pattern of neutral molecular variation under the background selection model. Genetics 141: 1619–1632.

101. FayJC, WuCI (1999) A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol Biol Evol 16: 1003–1005.

102. WalczakAM, NicolaisenLE, PlotkinJB, DesaiMM (2012) The structure of genealogies in the presence of purifying selection: a fitness-class coalescent. Genetics 190: 753–779.

103. HermissonJ, PenningsPS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335–2352.

104. MesserPW, PetrovDA (2013) Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol Evol 28: 659–669.

105. LeeYC, LangleyCH, BegunDJ (2014) Differential strengths of positive selection revealed by hitchhiking effects at small physical scales in Drosophila melanogaster. Mol Biol Evol 31: 804–816.

106. SattathS, ElyashivE, KolodnyO, RinottY, SellaG (2011) Pervasive adaptive protein evolution apparent in diversity patterns around amino acid substitutions in Drosophila simulans. PLoS Genet 7: e1001302.

107. CharlesworthD (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2: e64.

108. HedrickPW (2006) Genetic polymorphism in heterogeneous environments: The age of genomics. Annual Review of Ecology, Evolution, and Systematics 37: 67–93.

109. TurelliM, SchemskeDW, BierzychudekP (2001) Stable two-allele polymorphisms maintained by fluctuating fitnesses and seed banks: protecting the blues in Linanthus parryae. Evolution 55: 1283–1298.

110. TurnerTL, LevineMT, EckertML, BegunDJ (2008) Genomic analysis of adaptive differentiation in Drosophila melanogaster. Genetics 179: 455–473.

111. FabianDK, KapunM, NolteV, KoflerR, SchmidtPS, et al. (2012) Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol Ecol 21: 4748–4769.

112. CamposJL, ZengK, ParkerDJ, CharlesworthB, HaddrillPR (2013) Codon usage bias and effective population sizes on the X chromosome versus the autosomes in Drosophila melanogaster. Mol Biol Evol 30: 811–823.

113. HershbergR, PetrovDA (2008) Selection on codon bias. Annu Rev Genet 42: 287–299.

114. SinghND, DavisJC, PetrovDA (2005) X-linked genes evolve higher codon bias in Drosophila and Caenorhabditis. Genetics 171: 145–155.

115. SinghND, LarracuenteAM, ClarkAG (2008) Contrasting the efficacy of selection on the X and autosomes in Drosophila. Mol Biol Evol 25: 454–467.

116. HuTT, EisenMB, ThorntonKR, AndolfattoP (2013) A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res 23: 89–98.

117. BetancourtAJ, KimY, OrrHA (2004) A pseudohitchhiking model of X vs. autosomal diversity. Genetics 168: 2261–2269.

118. CharlesworthB, CoyneJA, BartonNH (1987) The relative rates of evolution of sex chromosomes and autosomes. American Nat 130: 113–146.

119. AndolfattoP, WongKM, BachtrogD (2011) Effective population size and the efficacy of selection on the X chromosomes of two closely related Drosophila species. Genome Biol Evol 3: 114–128.

120. BainesJF, SawyerSA, HartlDL, ParschJ (2008) Effects of X-linkage and sex-biased gene expression on the rate of adaptive protein evolution in Drosophila. Mol Biol Evol 25: 1639–1650.

121. 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.

122. LlopartA (2012) The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea, and their hybrids. Mol Biol Evol 29: 3873–3886.

123. MeiselRP, MaloneJH, ClarkAG (2012) Faster-X evolution of gene expression in Drosophila. PLoS Genet 8: e1003013.

124. CallahanB, NeherRA, BachtrogD, AndolfattoP, ShraimanBI (2011) Correlated evolution of nearby residues in Drosophilid proteins. PLoS Genet 7: e1001315.

125. SinghND, ArndtPF, ClarkAG, AquadroCF (2009) Strong evidence for lineage and sequence specificity of substitution rates and patterns in Drosophila. Mol Biol Evol 26: 1591–1605.

126. Eyre-WalkerA (2002) Changing effective population size and the McDonald-Kreitman test. Genetics 162: 2017–2024.

127. LoeweL, CharlesworthB (2006) Inferring the distribution of mutational effects on fitness in Drosophila. Biol Lett 2: 426–430.

128. BoykoAR, WilliamsonSH, IndapAR, DegenhardtJD, HernandezRD, et al. (2008) Assessing the evolutionary impact of amino acid mutations in the human genome. PLoS Genet 4: e1000083.

129. MacdonaldSJ, LongAD (2007) Joint estimates of quantitative trait locus effect and frequency using synthetic recombinant populations of Drosophila melanogaster. Genetics 176: 1261–1281.

130. NordborgM, CharlesworthB, CharlesworthD (1996) The effect of recombination on background selection. Genetical Research 67: 159–174.

131. LangleyCH, LazzaroBP, PhillipsW, HeikkinenE, BravermanJM (2000) Linkage disequilibria and the site frequency spectra in the su(s) and su(w(a)) regions of the Drosophila melanogaster X chromosome. Genetics 156: 1837–1852.

132. AndolfattoP, NordborgM (1998) The effect of gene conversion on intralocus associations. Genetics 148: 1397–1399.

133. Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. San Diego, CA: Academic Press.

134. PoolJE, AquadroCF (2006) History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics 174: 915–929.

135. SchaefferSW (2002) Molecular population genetics of sequence length diversity in the Adh region of Drosophila pseudoobscura. Genet Res 80: 163–175.

136. MackayTF, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173–178.

137. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.

138. YangZ (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555–556.

139. WongWS, YangZ, GoldmanN, NielsenR (2004) Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168: 1041–1051.

140. YangZ, WongWS, NielsenR (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107–1118.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 6
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#