The Hill-Robertson effect: Evolutionary consequences of weak selection and linkage in finite populations

Heredity

Volumn 100, Issue 1, 2008, Pages 19-31

  Comeron, J M ^a   Williford, A ^a   Kliman, R M ^b  

^a UNIVERSITY OF IOWA   (United States)

^b CEDAR CREST COLLEGE   (United States)

Author keywords

Codon bias; Gene conversion bias; Gene structure; Interference selection; Recombination; Weak selection

Indexed keywords

CHROMOSOME; COMPUTER SIMULATION; FLY; GENETIC STRUCTURE; MUTATION; RECOMBINATION; SELECTION;

ANIMAL; COMPUTER SIMULATION; DROSOPHILA MELANOGASTER; GENE LINKAGE DISEQUILIBRIUM; GENETIC DRIFT; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MUTATION; POPULATION GENETICS; SHORT SURVEY;

ANIMALS; COMPUTER SIMULATION; DROSOPHILA MELANOGASTER; GENETIC DRIFT; GENETIC LINKAGE; GENETIC VARIATION; GENETICS, POPULATION; LINKAGE DISEQUILIBRIUM; MUTATION; POLYMORPHISM, GENETIC; RECOMBINATION, GENETIC; SELECTION, GENETIC;

EID: 37349011445     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/sj.hdy.6801059     Document Type: Short Survey

References (122)

1. Aguadé M, Langley CH (1994). Polymorphism and divergence in regions of low recombination in Drosophila. In: Golding GB (ed). Non-Neutral Evolution: Theories and Molecular Data. Chapman & Hall: New York, pp 67-76.
2. Aguadé M, Miyashita N, Langley CH (1989). Restriction-map variation at the zeste-tko region in natural populations of Drosophila melanogaster. Mol Biol Evol 6: 123-130.
3. Akashi H (1995). Inferring weak selection from patterns of polymorphism and divergence at 'silent' sites in Drosophila DNA. Genetics 139: 1067-1076.
4. Akashi H (1996). Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics 144: 1297-1307.
5. Akashi H, Ko WY, Piao S, John A, Goel P, Lin CF et al. (2006). Molecular evolution in the Drosophila melanogaster species subgroup: frequent parameter fluctuations on the timescale of molecular divergence. Genetics 172: 1711-1726.
6. Akashi H, Schaeffer SW (1997). Natural selection and the frequency distributions of 'silent' DNA polymorphism in Drosophila. Genetics 146: 295-307.
7. Andolfatto P (2005). Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
8. Andolfatto P, Przeworski M (2001). Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics 158: 657-665.
9. Aquadro CF, Begun DJ, Kindahl EC (1994). Selection, recombination and DNA polymorphism in Drosophila. In: Golding B (ed). Non-Neutral Evolution: Theories and Molecular Data. Chapman & Hall: New York.
10. Bachtrog D (2003). Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes in Drosophila. Nat Genet 34: 215-219.
11. Bachtrog D, Charlesworth B (2000). Reduced levels of microsatellite variability on the neo-Y chromosome of Drosophila miranda. Curr Biol 10: 1025-1031.
12. Bachtrog D, Charlesworth B (2002). Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416: 323-326.
13. Barton N (1995a). Linkage and the limits to natural selection. Genetics 140: 821-841.
14. Barton NH (1995b). A general model for the evolution of recombination. Genet Res 65: 123-145.
15. Barton NH (1998). The effect of hitch-hiking on neutral genealogies. Genet Res 72: 123-133.
16. Barton NH, Charlesworth B (1998). Why sex and recombination? Science 281: 1986-1990.
17. Barton NH, Otto SP (2005). Evolution of recombination due to random drift. Genetics 169: 2353-2370.
18. Baudry E, Kerdelhue C, Innan H, Stephan W (2001). Species and recombination effects on DNA variability in the tomato genus. Genetics 158: 1725-1735.
19. Begun DJ (2001). The frequency distribution of nucleotide variation in Drosophila simulans. Mol Biol Evol 18: 1343-1352.
20. Begun DJ, Aquadro CF (1992). Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356: 519-520.
21. Berry AJ, Ajioka JW, Kreitman M (1991). Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129: 1111-1117.
22. Betancourt AJ, Presgraves DC (2002). Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci USA 99: 13616-13620.
23. Birky Jr CW, Walsh JB (1988). Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci USA 85: 6414-6418.
24. Bulmer M (1988). Codon usage and intragenic position. J Theor Biol 133: 67-71.
25. Bulmer M (1991). The selection-mutation-drift theory of synonymous codon usage. Genetics 129: 897-907.
26. Caballero A, Santiago E (1995). Response to selection from new mutation and effective size of partially inbred populations. I. Theoretical results. Genet Res 66: 213-225.
27. Carson HL (1958). Response to selection under different conditions of recombination in Drosophila. Cold Spring Harb Symp Quant Biol 23: 291-306.
28. Charlesworth B (1994). The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet Res 63: 213-227.
29. Charlesworth B, Morgan MT, Charlesworth D (1993). The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289-1303.
30. Cirulli ET, Kliman RM, Noor MA (2007). Fine-scale crossover rate heterogeneity in Drosophila pseudoobscura. J Mol Evol 64: 129-135.
31. Cohan FM (1984). Can uniform selection retard random genetic divergence between isolated conspecific populations? Evolution 38: 495-504.
32. Comeron JM, Aguade M (1996). Synonymous substitutions in the Xdh gene of Drosophila: heterogeneous distribution along the coding region. Genetics 144: 1053-1062.
33. Comeron JM, Guthrie TB (2005). Intragenic Hill-Robertson interference influences selection intensity on synonymous mutations in Drosophila. Mol Biol Evol 22: 2519-2530.
34. Comeron JM, Kreitman M (2000). The correlation between intron length and recombination in Drosophila. Dynamic equilibrium between mutational and selective forces. Genetics 156: 1175-1190.
35. Comeron JM, Kreitman M (2002). Population, evolutionary and genomic consequences of interference selection. Genetics 161: 389-410.
36. Comeron JM, Kreitman M, Aguade M (1999). Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151: 239-249.
37. Cutter AD, Payseur BA (2003). Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol Biol Evol 20: 665-673.
38. Duret L, Mouchiroud D (1999). Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci USA 96: 4482-4487.
39. Dvorak J, Luo MC, Yang ZL (1998). Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing aegilops species. Genetics 148: 423-434.
40. Ewens WJ (1979). Mathematical Population Genetics. Springer-Verlag: Berlin.
41. Eyre-Walker A (1996). The close proximity of Escherichia coli genes: consequences for stop codon and synonymous codon use. J Mol Evol 42: 73-78.
42. Eyre-Walker A, Bulmer M (1993). Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res 21: 4599-4603.
43. Felsenstein J (1965). The effect of linkage on directional selection. Genetics 52: 349-363.
44. Felsenstein J (1974). The evolutionary advantage of recombination. Genetics 78: 737-756.
45. Felsenstein J, Yokoyama S (1976). The evolutionary advantage of recombination. II. Individual selection for recombination. Genetics 83: 845-859.
46. Fisher RA (1930). The Genetical Theory of Natural Selection. Oxford University Press: New York.
47. Fridolfsson A-K, Ellegren H (2000). Molecular Evolution of the avian CHD1 genes on the Z and W sex chromosomes. Genetics 155: 1903-1912.
48. Gillespie JH (1994). Alternatives to the neutral theory. In: Golding B (ed). Non-Neutral Evolution: Theories and Molecular Data. Chapman and Hall: New York, pp 1-17.
49. Gillespie JH (2000). Genetic drift in an infinite population. The pseudohitchhiking model. Genetics 155: 909-919.
50. Haddrill PR, Halligan DL, Tomaras D, Charlesworth B (2007). Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol 8: R18.
51. Haldane JBS (1957). The cost of natural selection. J Genet 55: 511-524.
52. Hellmann I, Ebersberger I, Ptak SE, Paabo S, Przeworski M (2003). A neutral explanation for the correlation of diversity with recombination rates in humans. Am J Hum Genet 72: 1527-1535.
53. Hey J (1998). Selfish genes, pleiotropy and the origin of recombination. Genetics 149: 2089-2097.
54. Hey J, Kliman RM (2002). Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics 160: 595-608.
55. Hill WG, Robertson A (1966). The effect of linkage on limits to artificial selection. Genet Res 8: 269-294.
56. Hilton H, Kliman RM, Hey J (1994). Using hitchhiking genes to study adaptation and divergence during speciation within the Drosophila melanogaster species complex. Evolution 48: 1900-1913.
57. Hudson RR, Kaplan NL (1995). Deleterious background selection with recombination. Genetics 141: 1605-1617.
58. Iles MM, Walters K, Cannings C (2003). Recombination can evolve in large finite populations given selection on sufficient loci. Genetics 165: 2249-2258.
59. Jensen MA, Charlesworth B, Kreitman M (2002). Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D. simulans. Genetics 160: 493-507.
60. Kaplan NL, Hudson RR, Langley CH (1989). The "hitchhiking effect" revisited. Genetics 123: 887-899.
61. Keightley PD, Otto SP (2006). Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443: 89-92.
62. Kern AD, Begun DJ (2005). Patterns of polymorphism and divergence from noncoding sequences of Drosophila melanogaster and D. simulans: evidence for nonequilibrium processes. Mol Biol Evol 22: 51-62.
63. Kim Y, Stephan W (2003). Selective sweeps in the presence of interference among partially linked Loci. Genetics 164: 389-398.
64. Kliman RM (1999). Recent selection on synonymous codon usage in Drosophila. J Mol Evol 49: 343-351.
65. Kliman RM, Hey J (1993a). DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics 133: 375-387.
66. Kliman RM, Hey J (1993b). Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol 10: 1239-1258.
67. Kliman RM, Hey J (2003a). Hill-Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genet Res 81: 89-90.
68. Kliman RM, Irving N, Santiago M (2003). Selection conflicts, gene expression, and codon usage trends in yeast. J Mol Evol 57: 98-109.
69. Kondrashov AS (1994). Muller's ratchet under epistatic selection. Genetics 136: 1469-1473.
70. Kraft T, Sall T, Magnusson-Rading I, Nilsson NO, Hallden C (1998). Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics 150: 1239-1244.
71. Langley CH, MacDonald J, Miyashita N, Aguade M (1993). Lack of correlation between interspecific divergence and intraspecific polymorphism at the suppressor of forked region in Drosophila melanogaster and Drosophila simulans. Proc Natl Acad Sci USA 90: 1800-1803.
72. Li WH (1987). Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J Mol Evol 24: 337-345.
73. Loewe L, Charlesworth B (2007). Background selection in single genes may explain patterns of codon bias. Genetics 175: 1381-1393.
74. Lynch MBJ (1998). Deleterious mutation accumulation in organelle genomes. Genetica 102-103: 29-39.
75. Marais G, Mouchiroud D, Duret L (2001). Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA 98: 5688-5692.
76. Marais G, Mouchiroud D, Duret L (2003). Neutral effect of recombination on base composition in Drosophila. Genet Res 81: 79-87.
77. Marais G, Piganeau G (2002). Hill-Robertson interference is a minor determinant of variations in codon bias across Drosophila melanogaster and Caenorhabditis elegans genomes. Mol Biol Evol 19: 1399-1406.
78. Martin G, Otto SP, Lenormand T (2006). Selection for recombination in structured populations. Genetics 172: 593-609.
79. Martin-Campos JM, Comeron JM, Miyashita N, Aguade M (1992). Intraspecific and interspecific variation at the y-ac-sc region of Drosophila simulans and Drosophila melanogaster. Genetics 130: 805-816.
80. Maynard Smith J, Haigh J (1974). The hitch-hiking effect of a favorable gene. Genet Res 23: 23-35.
81. McPhee CP, Robertson A (1970). The effect of suppressing crossing-over on the response to selection in Drosophila melanogaster. Genet Res 16: 1-16.
82. McVean GA, Charlesworth B (1999). A population genetic model for the evolution of synonymous codon usage: patterns and predictions. Genet Res 74: 145-158.
83. McVean GA, Charlesworth B (2000). The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155: 929-944.
84. McVean GA, Vieira J (2001). Inferring parameters of mutation, selection and demography from patterns of synonymous site evolution in Drosophila. Genetics 157: 245-257.
85. Moriyama EN, Hartl DL (1993). Codon usage bias and base composition of nuclear genes in Drosophila. Genetics 134: 847-858.
86. Moriyama EN, Powell JR (1996). Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol 13: 261-277.
87. Moriyama EN, Powell JR (1998). Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Res 26: 3188-3193.
88. Muller HJ (1964). The relation of recombination to mutational advance. Mutat Res 1: 2-9.
89. Nachman MW (1997). Patterns of DNA variability at X-linked loci in Mus domesticus. Genetics 147: 1303-1316.
90. Nachman MW, Bauer VL, Crowell SL, Aquadro CF (1998). DNA variability and recombination rates at X-linked loci in humans. Genetics 150: 1133-1141.
91. Nagylaki T (1983). Evolution of a finite population under gene conversion. Proc Natl Acad Sci USA 80: 6278-6281.
92. Nordborg M, Charlesworth B, Charlesworth D (1996). The effect of recombination on background selection. Genet Res 67: 159-174.
93. Ohta T, Kimura M (1971). On the constancy of the evolutionary rate of cistrons. J Mol Evol 1: 18-25.
94. Ohta T, Kimura M (1975). The effect of selected linked locus on heterozygosity of neutral alleles (the hitch-hiking effect). Genet Res 25: 313-326.
95. Otto SP, Barton NH (1997). The evolution of recombination: removing the limits to natural selection. Genetics 147: 879-906.
96. Otto SP, Barton NH (2001). Selection for recombination in small populations. Evolution 55: 1921-1931.
97. Otto SP, Lenormand T (2002). Resolving the paradox of sex and recombination. Nat Rev Genet 3: 252-261.
98. Piganeau G, Westrelin R, Tourancheau B, Gautier C (2001). Multiplicative versus additive selection in relation to genome evolution: a simulation study. Genet Res 78: 171-175.
99. Powell JR, Moriyama EN (1997). Evolution of codon usage bias in Drosophila. Proc Natl Acad Sci USA 94: 7784-7790.
100. Przeworski M, Hudson RR, Di Rienzo A (2000). Adjusting the focus on human variation. Trends Genet 16: 296-302.
101. Qin H, Wu WB, Comeron JM, Kreitman M, Li WH (2004). Intragenic spatial patterns of codon usage bias in prokaryotic and eukaryotic genomes. Genetics 168: 2245-2260.
102. Rice WR (1994). Degeneration of a nonrecombining chromosome. Science 263: 230-232.
103. Rice WR, Chippindale AK (2001). Sexual recombination and the power of natural selection. Science 294: 555-559.
104. Robertson A (1960). A theory of limits in artificial selection. Proc R Soc Lond B Biol Sci 153: 234-249.
105. Robertson A (1961). Inbreeding in artificial selection programmes. Genet Res 2: 189-194.
106. Roze D, Barton NH (2006). The Hill-Robertson effect and the evolution of recombination. Genetics 173: 1793-1811.
107. Schaeffer SW (2002). Molecular population genetics of sequence length diversity in the Adh region of Drosophila pseudoobscura. Genet Res 80: 163-175.
108. Singh ND, Arndt PF, Petrov DA (2005). Genomic heterogeneity of background substitutional patterns in Drosophila melanogaster. Genetics 169: 709-722.
109. Stephan W (1994). Effects of genetic recombination and population subdivision on nucleotide sequence variation in Drosophila ananassae. In: Golding B (ed). Non-Neutral Evolution: Theories and Molecular Data. Chapman and Hall: New York. pp 57-66.
110. Stephan W, Langley CH (1989). Molecular genetic variation in the centromeric region of the X chromosome in three Drosophila ananassae populations. I. Contrasts between the vermilion and forked loci. Genetics 121: 89-99.
111. Stephan W, Langley CH (1998). DNA polymorphism in lycopersicon and crossing-over per physical length. Genetics 150: 1585-1593.
112. Stephan W, Wiehe THE, Lenz MW (1992). The effect of strongly selected substitutions on neutral polymorphism-analytical results based on diffusion theory. Theor Popul Biol 41: 237-254.
113. Tachida H (2000). Molecular evolution in a multisite nearly neutral mutation model. J Mol Evol 50: 69-81.
114. Tajima F (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
115. Takano TS (1998). Rate variation of DNA sequence evolution in the Drosophila lineages. Genetics 149: 959-970.
116. Wang J, Hill WG, Charlesworth D, Charlesworth B (1999). Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet Res 74: 165-178.
117. Wang W, Thornton K, Berry A, Long M (2002). Nucleotide variation along the Drosophila melanogaster fourth chromosome. Science 295: 134-137.
118. Weinreich DM, Rand DM (2000). Contrasting patterns of nonneutral evolution in proteins encoded in nuclear and mitochondrial genomes. Genetics 156: 385-399.
119. Wright S (1931). Evolution in Mendelian populations. Genetics 16: 97-159.
120. Wright S (1938). Size of population and breeding structure in relation to evolution. Science 87: 430-431.
121. Zhang Z, Parsch J (2005). Positive correlation between evolutionary rate and recombination rate in Drosophila genes with male-biased expression. Mol Biol Evol 22: 1945-1947.
122. Zurovcova M, Eanes WF (1999). Lack of nucleotide polymorphism in the Y-linked sperm flagellar dynein gene Dhc-Yh3 of Drosophila melanogaster and D. simulans. Genetics 153: 1709-1715.