#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Limits to the Rate of Adaptive Substitution in Sexual Populations


In large populations, many beneficial mutations may be simultaneously available and may compete with one another, slowing adaptation. By finding the probability of fixation of a favorable allele in a simple model of a haploid sexual population, we find limits to the rate of adaptive substitution, , that depend on simple parameter combinations. When variance in fitness is low and linkage is loose, the baseline rate of substitution is , where is the population size, is the rate of beneficial mutations per genome, and is their mean selective advantage. Heritable variance in log fitness due to unlinked loci reduces by under polygamy and under monogamy. With a linear genetic map of length Morgans, interference is yet stronger. We use a scaling argument to show that the density of adaptive substitutions depends on , , , and only through the baseline density: . Under the approximation that the interference due to different sweeps adds up, we show that , implying that interference prevents the rate of adaptive substitution from exceeding one per centimorgan per 200 generations. Simulations and numerical calculations confirm the scaling argument and confirm the additive approximation for ; for higher , the rate of adaptation grows above , but only very slowly. We also consider the effect of sweeps on neutral diversity and show that, while even occasional sweeps can greatly reduce neutral diversity, this effect saturates as sweeps become more common—diversity can be maintained even in populations experiencing very strong interference. Our results indicate that for some organisms the rate of adaptive substitution may be primarily recombination-limited, depending only weakly on the mutation supply and the strength of selection.


Vyšlo v časopise: Limits to the Rate of Adaptive Substitution in Sexual Populations. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002740
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002740

Souhrn

In large populations, many beneficial mutations may be simultaneously available and may compete with one another, slowing adaptation. By finding the probability of fixation of a favorable allele in a simple model of a haploid sexual population, we find limits to the rate of adaptive substitution, , that depend on simple parameter combinations. When variance in fitness is low and linkage is loose, the baseline rate of substitution is , where is the population size, is the rate of beneficial mutations per genome, and is their mean selective advantage. Heritable variance in log fitness due to unlinked loci reduces by under polygamy and under monogamy. With a linear genetic map of length Morgans, interference is yet stronger. We use a scaling argument to show that the density of adaptive substitutions depends on , , , and only through the baseline density: . Under the approximation that the interference due to different sweeps adds up, we show that , implying that interference prevents the rate of adaptive substitution from exceeding one per centimorgan per 200 generations. Simulations and numerical calculations confirm the scaling argument and confirm the additive approximation for ; for higher , the rate of adaptation grows above , but only very slowly. We also consider the effect of sweeps on neutral diversity and show that, while even occasional sweeps can greatly reduce neutral diversity, this effect saturates as sweeps become more common—diversity can be maintained even in populations experiencing very strong interference. Our results indicate that for some organisms the rate of adaptive substitution may be primarily recombination-limited, depending only weakly on the mutation supply and the strength of selection.


Zdroje

1. FisherRA 1930 The genetical theory of natural selection. Oxford: Oxford University Press

2. MullerH 1932 Some genetic aspects of sex. Am Nat 66 118 138

3. GerrishPJLenskiRE 1998 The fate of competing beneficial mutations in an asexual population. Genetica 102 127 144

4. RouzineIMWakeleyJCoffinJM 2003 The solitary wave of asexual evolution. Proc Natl Acad Sci U S A 100 587 92

5. WilkeCO 2004 The speed of adaptation in large asexual populations. Genetics 167 2045 2053

6. DesaiMMFisherDS 2007 Beneficial mutation selection balance and the effect of linkage on positive selection. Genetics 176 1759 98

7. ParkSKrugJ 2007 Clonal interference in large populations. Proc Natl Acad Sci U S A 104 18135 18140

8. RouzineIMBrunetEWilkeCO 2008 The traveling-wave approach to asexual evolution: Muller's ratchet and speed of adaptation. Theoretical Population Biology 73 24 46

9. BrunetERouzineIMWilkeCO 2008 The stochastic edge in adaptive evolution. Genetics 179 603 20

10. FogleCANagleJLDesaiMM 2008 Clonal interference, multiple mutations and adaptation in large asexual populations. Genetics 180 2163 73

11. ParkSSimonDKrugJ 2010 The speed of evolution in large asexual populations. Journal of Statistical Physics 138 381 410

12. WeismannA 1889 The significance of sexual reproduction in the theory of natural selection. Essays upon heredity and kindred biological problems. Oxford: Clarendon Press

13. CrowJFKimuraM 1965 Evolution in sexual and asexual populations. Am Nat 99 439 450

14. HillWGRobertsonA 1966 The effect of linkage on limits to artificial selection. Genet Res 8 269 294

15. RobertsonA 1970 A theory of limits in artificial selection with many linked loci. Biomathematics Volume 1 Mathematical topics in population genetics 246 288

16. Maynard SmithJ 1971 What use is sex? Journal of Theoretical Biology 30 319 335

17. BartonNHOttoSP 2005 Evolution of recombination due to random drift. Genetics 169 2353 70

18. KeightleyPDOttoSP 2006 Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443 89 92

19. RozeDBartonNH 2006 The Hill-Robertson effect and the evolution of recombination. Genetics 173 1793 811

20. HartfieldMOttoSPKeightleyPD 2010 The role of advantageous mutations in enhancing the evolution of a recombination modifier. Genetics 184 1153 1164

21. OttoSP 2009 The evolutionary enigma of sex. Am Nat 174 S1 S14

22. RouzineIMCoffinJM 2005 Evolution of human immunodeficiency virus under selection and weak recombination. Genetics 170 7 18

23. CohenEKesslerDLevineH 2005 Recombination dramatically speeds up evolution of finite populations. Phys Rev Lett 94 1 4

24. CohenEKesslerDLevineH 2006 Analytic approach to the evolutionary effects of genetic exchange. Phys Rev E 73 1 7

25. RouzineIMCoffinJM 2007 Highly fit ancestors of a partly sexual haploid population. Theoretical Population Biology 71 239 250

26. RouzineIMCoffinJM 2010 Multi-site adaptation in the presence of infrequent recombination. TPB 77 189 204

27. NeherRAShraimanBIFisherDS 2010 Rate of adaptation in large sexual populations. Genetics 184 467 481

28. WylieCSTroutADKesslerDALevineH 2010 Optimal strategy for competence differentiation in bacteria. PLoS Genet 6e1001108doi:10.1371/journal.ppat.1001108

29. BatorskyRKearneyMPalmerSMaldarelliFRouzineIM 2011 Estimate of effective recombination rate and average selection coeficient for HIV in chronic infection. Proc Natl Acad Sci U S A 108 5661 5666

30. NeherRAShraimanBI 2011 Genetic draft and quasi-neutrality in large facultatively sexual populations. Genetics 188 975 996

31. MirallesRGerrishPJMoyaAElenaSF 1999 Clonal interference and the evolution of RNA viruses. Science 285 1745 7

32. BollbackJPHuelsenbeckJP 2007 Clonal interference is alleviated by high mutation rates in large populations. Mol Biol Evol 24 1397 406

33. PepinKMWichmanHA 2008 Experimental evolution and genome sequencing reveal variation in levels of clonal interference in large populations of bacteriophage φX174. BMC Evol Biol 8 85

34. BetancourtAJ 2009 Genomewide patterns of substitution in adaptively evolving populations of the RNA bacteriophage MS2. Genetics 181 1535 44

35. MillerCRJoycePWichmanHA 2011 Mutational effects and population dynamics during viral adaptation challenge current models. Genetics 187 185 202

36. LenskiRERoseMRSimpsonSTadlerSC 1991 Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138 1315 1341

37. De VisserJAGMZeylCGerrishPJBlanchardJLLenskiRE 1999 Diminishing returns from mutation supply rate in asexual populations. Science 283 404 6

38. De VisserJAGMRozenDE 2006 Clonal interference and the periodic selection of new beneficial mutations in Escherichia coli. Genetics 172 2093 100

39. HegrenessMShoreshNHartlDLKishonyR 2006 An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 311 1615 1617

40. BarrickJELenskiRE 2009 Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol 74 119 29

41. ColegraveN 2002 Sex releases the speed limit on evolution. Nature 420 664 6

42. GoddardMRGodfrayHCJBurtA 2005 Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434 636 40

43. KaoKCSherlockG 2008 Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40 1499 504

44. LangGIBotsteinDDesaiMM 2011 Genetic variation and the fate of beneficial mutations in asexual populations. Genetics 188 647 661

45. FelsensteinJ 1974 The evolutionary advantage of recombination. Genetics 78 737 756

46. BartonNH 2009 Why sex and recombination? Cold Spring Harb Symp Quant Biol 74 187 95

47. FisherRA 1922 On the dominance ratio. Proc Roy Soc Edin 42 321 341

48. HaldaneJBS 1927 A mathematical theory of natural and artificial selection V: selection and mutation. Proc Camb Phil Soc 23 838 844

49. BartonNHEtheridgeAM 2011 The relation between reproductive value and genetic contribution. Genetics 1 51

50. EwensWJ 2004 Mathematical Population Genetics. New York: Springer-Verlag, 2nd edition

51. MitchellM 1998 An introduction to genetic algorithms. Cambridge, MA: MIT Press

52. BulmerM 1980 The mathematical theory of quantitative genetics. Oxford: Oxford University Press

53. WalshJB LynchM 2012 Evolution and selection of quantitative traits I. Foundations. Available: http://nitro.biosci.arizona.edu/zbook/NewVolume 2/newvol2.html.

54. RobertsonA 1961 Inbreeding in artificial selection programmes. Genet Res 2 189 194

55. BartonNH 1995 Linkage and the limits to natural selection. Genetics 140 821 41

56. MaruyamaT 1970 On the fixation probability of mutant genes in a subdivided population. Genet Res 15 221 225

57. MaruyamaT 1971 An invariant property of a structured population. Genet Res 18 81 84

58. WhitlockMC 2003 Fixation probability and time in subdivided populations. Genetics 164 767 779

59. MaruyamaT 1974 The age of an allele in a finite population. Genet Res 23 137 143

60. GillespieJH 2000 Genetic drift in an infinite population. the pseudohitchhiking model. Genetics 155 909 19

61. LewontinRC 1974 Genetic Basis of Evolutionary Change. New York: Columbia University Press

62. SmithJMHaighJ 1974 The hitch-hiking effect of a favourable gene. Genet Res 23 23 35

63. GillespieJH 2000 The neutral theory in an infinite population. Gene 261 11 8

64. GillespieJH 2001 Is the population size of a species relevant to its evolution? Evolution 55 2161 2169

65. BartonNHEtheridgeAM 2004 The effect of selection on genealogies. Genetics 166 1115 1131

66. KimYStephanW 2003 Selective sweeps in the presence of interference among partially linked loci. Genetics 164 389 98

67. ChevinLMBilliardS Hospital F 2008 Hitchhiking both ways: Effect of two interfering selective sweeps on linked neutral variation. Genetics 180 301 316

68. KaplanNLHudsonRRLangleyCH 1989 The “hitchhiking effect” revisited. Genetics 123 887 899

69. WieheTHEStephanW 1993 Analysis of a genetic hitchhiking model, and its application to DNA polymorphism data from Drosophila melanogaster. Mol Biol Evol 10 842 854

70. StephanWWieheTHELenzMW 1992 The effect of strongly selected substitutions on neutral polymorphism: analytical results based on diffusion theory. Theoretical Population Biology 41

71. BartonNH 1998 The effect of hitch-hiking on neutral genealogies. Genet Res 72 123 133

72. DurrettRSchweinsbergJ 2004 Approximating selective sweeps. Theoretical Population Biology 66 129 138

73. BartonNH 2010 Mutation and the evolution of recombination. Phil Trans R Soc B 365 1281 1294

74. SantiagoECaballeroA 1995 Effective size of populations under selection. Genetics 139 1013 30

75. KarasovTMesserPWPetrovDA 2010 Evidence that adaptation in Drosophila is not limited by mutation at single sites. PLoS Genet 6e1000924doi:10.1371/journal.pgen.1000924

76. McVeanGCharlesworthB 2000 The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155 929 944

77. KaiserVBCharlesworthB 2009 The effects of deleterious mutations on evolution in nonrecombining genomes. Trends in Genetics 25 9 12

78. SchiffelsSSzöllösiGMustonenVLässigM 2011 Emergent neutrality in adaptive asexual evolution. Genetics : in press

79. BartonNH 1994 The reduction in fixation probability caused by substitutions at linked loci. Genet Res 64 199 208

80. GoodBHRouzineIMBalickDJHallatschekODesaiMM 2012 The rate of adaptation and the distribution of fixed beneficial mutations in asexual populations. Proc Natl Acad Sci U S A: in press

81. LevyDNAldrovandiGMKutschOShawGM 2004 Dynamics of HIV-1 recombination in its natural target cells. Proc Natl Acad Sci U S A 101 4204 9

82. NeherRALeitnerT 2010 Recombination rate and selection strength in HIV intra-patient evolution. PLoS Comput Biol 6e1000660doi:10.1371/journal. pcbi.1000660

83. SantiagoECaballeroA 1998 Effective size and polymorphism of linked neutral loci in populations under directional selection. Genetics 149 2105 2117

84. MartensEAHallatschekO 2012 Interfering waves of adaptation promote spatial mixing. Genetics: in press

85. HillWG 1982 Predictions of response to artificial selection from new mutations. Genet Res 40 255 278

86. HillWG 1982 Rates of change in quantitative traits from fixation of new mutations. Proc Natl Acad Sci U S A 79 142 5

87. TurelliM 1984 Heritable genetic variation via mutation-selection balance: Lerch's zeta meets the abdominal bristle. Theoretical Population Biology 25 138 93

88. BartonNHKeightleyPD 2002 Understanding quantitative genetic variation. Nat Rev Genet 3 11 21

89. HalliganDLKeightleyPD 2009 Spontaneous mutation accumulation studies in evolutionary genetics. Annu Rev Ecol Evol & Sys 40 151 172

90. LaurieCChasalowSLeDeauxJMcCarrollRBushD 2004 The genetic architecture of response to long-term artificial selection for oil concentration in the maize kernel. Genetics 168 2141 2155

91. WalshJB 2004 Population- and quantitative-genetic models of selection limits. Plant Breeding Reviews 24 177 225

92. BurkeMKDunhamJPShahrestaniPThorntonKRRoseMR 2010 Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467 587 90

93. HernandezRDKelleyJLElyashivEMeltonSCAutonA 2011 Classic selective sweeps were rare in recent human evolution. Science 331 920 924

94. AndolfattoP 2005 Adaptive evolution of non-coding DNA in Drosophila. Nature 437 1149 1152

95. AshburnerMGolicKGHawleyRS 2004 Drosophila: a laboratory handbook. New York: Cold Spring Harbor Laboratory Press, 2nd edition

96. Fiston-LavierASSinghNDLipatovMPetrovDA 2010 Drosophila melanogaster recombination rate calculator. Gene 463 18 20

97. NolteVSchlöttererC 2008 African Drosophila melanogaster and D. simulans populations have similar levels of sequence variability, suggesting comparable effective population sizes. Genetics 178 405 412

98. AndolfattoPWongKMBachtrogD 2011 Effective population size and the effcacy of selection on the X chromosomes of two closely related Drosophila species. Genome Biology and Evolution 3 114 128

99. Haag-LiautardCDorrisMMasideXMacaskillSHalliganDL 2007 Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445 82 85

100. SattathSElyashivEKolodnyORinottYSellaG 2011 Pervasive adaptive protein evolution apparent in diversity patterns around amino acid substitutions in Drosophila simulans. PLoS Genet 7 e1001302doi:10.1371/journal.pgen.1001302

101. SellaGPetrovDAPrzeworskiMAndolfattoP 2009 Pervasive natural selection in the Drosophila genome? PLoS Genet 5 e1000495doi:10.1371/journal.pgen.1000495

102. MesserPW 2009 Measuring the rates of spontaneous mutation from deep and large-scale polymorphism data. Genetics 182 1219 1232

103. OttoSPBartonNH 2001 Selection for recombination in small populations. Evolution 55 1921 31

104. IlesMMWaltersKCanningsC 2003 Recombination can evolve in large finite populations given selection on sufficient loci. Genetics 165 2249 58

105. NagylakiT 1974 The moments of stochastic integrals and the distribution of sojourn times. Proc Natl Acad Sci U S A 71 746 9

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 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#