Why are sex and recombination so common?

Annals of the New York Academy of Sciences

Volumn 1133, Issue , 2008, Pages 26-43

  Hadany, Lilach ^a   Comeron, Josep M ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Epistasis; Evolution of sex; Linkage disequilibrium; Plasticity; Recombination; Red queen; Sexual reproduction

Indexed keywords

ENVIRONMENTAL FACTOR; EVOLUTIONARY ADAPTATION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE MUTATION; GENE SEGREGATION; GENETIC ASSOCIATION; GENETIC DIFFERENCE; GENETIC DRIFT; GENETIC EPISTASIS; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; GENOME; HUMAN; NONHUMAN; PLASTICITY; POPULATION SIZE; PROGENY; REPRODUCTION; REVIEW; SEX; SEX DIFFERENCE;

EID: 45249101153     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1196/annals.1438.011     Document Type: Review

References (186)

1. Abdullah, M.F.F. & R.H. Borts. 2001. Meiotic recombination frequencies are affected by nutritional states in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98 : 14524 14529.
2. Agrawal, A.F. & J.R. Chasnov. 2001. Recessive mutations and the maintenance of sex in structured populations. Genetics 158 : 913 917.
3. Agrawal, A.F., L. Hadany & S.P. Otto. 2005. The evolution of plastic recombination. Genetics 171 : 803 812.
4. Aguade, M. et al. 1994. Single-strand conformation polymorphism analysis coupled with stratified DNA-sequencing reveals reduced sequence variation in the Su(S) and Su(W(a)) regions of the Drosophila melanogaster X-chromosome. Proc. Natl. Acad. Sci. USA 91 : 4658 4662.
5. Altenberg, L. & M.W. Feldman. 1987. Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle. Genetics 117 : 559 572.
6. Andolfatto, P. 2005. Adaptive evolution of non-coding DNA in Drosophila. Nature 437 : 1149 1152.
7. Andolfatto, P. & M. Przeworski. 2001. Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics 158 : 657 665.
8. Aquadro, C.F., D.J. Begun & E.C. Kindahl. 1994. Selection, recombination and DNA polymorphism in Drosophila. In Non-Neutral Evolution: Theories and Molecular Data. B. Golding, Ed. Chapman & Hall. New York.
9. Awadalla, P. 2003. The frequency of sex and recombination in microbes and pathogens. Nat. Rev. Genet. 4 : 50 60.
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. 2004. Evidence that positive selection drives Y-chromosome degeneration in Drosophila miranda. Nat. Genet. 36 : 518 522.
12. Bachtrog, D. 2006. Expression profile of a degenerating neo-y chromosome in Drosophila. Curr. Biol. 16 : 1694 1699.
13. Bachtrog, D. & B. Charlesworth. 2000. Reduced levels of microsatellite variability on the neo-Y chromosome of Drosophila miranda. Curr. Biol. 10 : 1025 1031.
14. Bachtrog, D. & B. Charlesworth. 2002. Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416 : 323 326.
15. Barton, N.H. 1995a. Linkage and the limits to natural selection. Genetics 140 : 821 841.
16. Barton, N.H. 1995b. A general model for the evolution of recombination. Genet. Res. 65 : 123 144.
17. Barton, N.H. & S.P. Otto. 2005. Evolution of recombination due to random drift. Genetics 169 : 2353 2370.
18. Baudat, F. et al. 2000. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol. Cell 6 : 989 998.
19. Baudry, E. et al. 2001. Species and recombination effects on DNA variability in the tomato genus. Genetics 158 : 1725 1735.
20. Bell, G. 1982. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press. Berkeley.
21. Bell, G. & J.M. Smith. 1987. Short-term selection for recombination among mutually antagonistic species. Nature 328 : 66 68.
22. Belyaev, D.K. & P.M. Borodin. 1982. The influence of stress on variation and its role in evolution. Biol. Zentbl. 100 : 705 714.
23. Bergman, A. & M.L. Siegal. 2003. Evolutionary capacitance as a general feature of complex gene networks. Nature 424 : 549 552.
24. Berry, A.J. et al. 1991. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129 : 1111 1117.
25. Betancourt, A.J. & D.C. Presgraves. 2002. Linkage limits the power of natural selection in Drosophila. Proc. Natl. Acad. Sci. USA 99 : 13616 13620.
26. Birky, C.W. Jr. & J.B. Walsh. 1988. Effects of linkage on rates of molecular evolution. Proc. Natl. Acad. Sci. USA 85 : 6414 6418.
27. Bonhoeffer, S. et al. 2004. Evidence for positive epistasis in HIV-1. Science 306 : 1547 1550.
28. Broman, K. et al. 1998. Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am. J. Hum. Genet. 63 : 861 869.
29. Brooks, L. & W. Marks. 1986. The organization of genetic variation for recombination in Drosophila melanogaster. Genetics 114 : 525 547.
30. Bruvo, R. et al. 2007. Synergism between mutational meltdown and Red Queen in parthenogenetic biotypes of the freshwater planarian Schmidtea polychroa. Oikos 116 : 313 323.
31. Burch, C.L. & L. Chao. 2004. Epistasis and its relationship to canalization in the RNA virus phi 6. Genetics 167 : 559 567.
32. Burger, R. 1999. Evolution of genetic variability and the advantage of sex and recombination in changing environments. Genetics 153 : 1055 1069.
33. Burt, A. 2000. Perspective: sex, recombination, and the efficacy of selection - was Weismann right? Evolution 54 : 337 351.
34. Burt, A. & G. Bell. 1987. Mammalian chiasma frequencies as a test of two theories of recombination. Nature 326 : 803 805.
35. Bustamante, C.D. et al. 2002. The cost of inbreeding in Arabidopsis. Nature 416 : 531 534.
36. Caballero, A. & E. Santiago. 1995. Response to selection from new mutation and effective size of partially inbred populations. I. Theoretical results. Genet. Res. 66 : 213 225.
37. Carson, H.L. 1958. Response to selection under different conditions of recombination in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 23 : 291 306.
38. Caryl, A.P. et al. 2003. Dissecting plant meiosis using Arabidopsis thaliana mutants. J. Exp. Bot 54 : 25 38.
39. Charlesworth, B. 1976. Recombination modification in a fluctuating environment. Genetics 83 : 181 195.
40. Charlesworth, B. 1994. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63 : 213 227.
41. Charlesworth, B. & D. Charlesworth. 1975. Experiment on recombination load in Drosophila melanogaster. Genet. Res. 25 : 267 274.
42. Charlesworth, B. & D. Charlesworth. 1985. Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity 54 : 71 83.
43. Charlesworth, B. et al. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134 : 1289 1303.
44. Chasnov, J.R. 2000. Mutation-selection balance, dominance and the maintenance of sex. Genetics 156 : 1419 1425.
45. Chinnici, J.P. 1971. Modification of recombination frequency in Drosophila. I. Selection for increased and decreased crossing over. Genetics 69 : 71 83.
46. Colegrave, N. 2002. Sex releases the speed limit on evolution. Nature 420 : 664 666.
47. Colegrave, N. et al. 2002. The ecology and genetics of fitness in Chlamydomonas. VIII. The dynamics of adaptation to novel environments after a single episode of sex. Evolution 56 : 14 21.
48. Comeron, J.M. 2001. What controls the length of noncoding DNA? Curr. Opin. Genet. Dev. 11 : 652 659.
49. Comeron, J.M. 2005. Repetitive sequences and noncoding DNA in eukaryotes. Encyclopedia Mol. Cell. Biol. Mol. Med. R.A. Meyers 12 : 127 137.
50. Comeron, J.M. & T.B. Guthrie. 2005. Intragenic Hill-Robertson interference influences selection intensity on synonymous mutations in Drosophila. Mol. Biol. Evol. 22 : 2519 2530.
51. Comeron, J.M. & M. Kreitman. 2000. The correlation between intron length and recombination in Drosophila: dynamic equilibrium between mutational and selective forces. Genetics 156 : 1175 1190.
52. Comeron, J.M. & M. Kreitman. 2002. Population, evolutionary and genomic consequences of interference selection. Genetics 161 : 389 410.
53. Comeron, J.M. et al. 1999. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151 : 239 249.
54. Cooper, T.F. et al. 2005. Parasites and mutational load: an experimental test of a pluralistic theory for the evolution of sex. Proc. R. Soc. Lond. B Biol. Sci. 272 : 311 317.
55. Crow, J.F. & M. Kimura. 1965. Evolution in sexual and asexual populations. Am. Nat. 99 : 439 450.
56. Crow, J.F. & M. Kimura. 1970. An Introduction to Population Genetics Theory. Harper and Row. New York.
57. Cutter, A.D. & B.A. Payseur. 2003. Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol. Biol. Evol. 20 : 665 673.
58. Davis, L. & G.R. Smith. 2001. Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe. Proc. Nat. Acad. Sci. USA 98 : 8395 8402.
59. de Visser, J. & S.F. Elena. 2007. The evolution of sex: empirical insights into the roles of epistasis and drift. Nat. Rev. Genet. 8 : 139 149.
60. de Visser, J. et al. 2003. Perspective: evolution and detection of genetic robustness. Evolution 57 : 1959 1972.
61. de Visser, J. & R.F. Hoekstra. 1998. Synergistic epistasis between loci affecting fitness: evidence in plants and fungi. Genet. Res. 71 : 39 49.
62. Dolgin, E.S. & S.P. Otto. 2003. Segregation and the evolution of sex under overdominant selection. Genetics 164 : 1119 1128.
63. Elena, S.F. & R.E. Lenski. 1997. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390 : 395 398.
64. Ellegren, H. & A.K. Fridolfsson. 2003. Sex-specific mutation rates in salmonid fish. J. Mol. Evol. 56 : 458 463.
65. Eshel, I. & M.W. Feldman. 1970. On the evolutionary effect of recombination. Theor. Popul. Biol. 1 : 88 100.
66. Fay, J.C. et al. 2001. Positive and negative selection on the human genome. Genetics 158 : 1227 1234.
67. Feldman, M.W. et al. 1980. Evolution of recombination in a constant environment. Proc. Nat. Acad. Sci. USA 77 : 4838 4841.
68. Felsenstein, J. 1974. The evolutionary advantage of recombination. Genetics 78 : 737 756.
69. Felsenstein, J. 1988. Sex and the evolution of recombination. In The Evolution of Sex. R.E. Michod & B.R. Levin, Eds 74 86. Sinauer Associates. Sunderland, MA.
70. Flexon, P.B. & C.F. Rodell. 1982. Genetic recombination and directional selection for DDT resistance in Drosophila melanogaster. Nature 298 : 672 674.
71. Fridolfsson, A.-K. & H. Ellegren. 2000. Molecular evolution of the avian CHD1 genes on the Z and W sex chromosomes. Genetics 155 : 1903 1912.
72. Gemmill, A.W. et al. 1997. Host immune status determines sexuality in a parasitic nematode. Evolution 51 : 393 401.
73. Gerrard, D.T. & D.A. Filatov. 2005. Positive and negative selection on mammalian Y chromosomes. Mol. Biol. Evol. 22 : 1423 1432.
74. Gessler, D.D.G. & S.Z. Xu. 2000. Meiosis and the evolution of recombination at low mutation rates. Genetics 156 : 449 456.
75. Gillespie, J.H. 2000. Genetic drift in an infinite population: the pseudohitchhiking model. Genetics 155 : 909 919.
76. Goddard, M.R. et al. 2005. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434 : 636 640.
77. Gorodetskii, V.P. et al. 1990. Efficiency of feedback selection for recombination in Drosophila. Genetika 26 : 1942 1952.
78. Green, M.M. 1959. Effect of different wild-type isoalleles on crossing-over in Drosophila melanogaster. Nature 184 (Suppl 5 294.
79. Greig, D. et al. 1998. The effect of sex on adaptation to high temperature in heterozygous and homozygous yeast. Proc. R. Soc. Lond. B Biol. Sci. 265 : 1017 1023.
80. Grell, R.F. 1978. A comparison of heat and interchromosomal effects on recombination and interference in Drosophila melanogaster. Genetics 89 : 65 77.
81. Grishkan, I. et al. 2003. Ecological stress and sex evolution in soil microfungi. Proc. R. Soc. Lond. B Biol. Sci. 270 : 13 18.
82. Hadany, L. & T. Beker. 2003. On the evolutionary advantage of fitness-associated recombination. Genetics 165 : 2167 2179.
83. Hadany, L. & T. Beker. 2007. Sexual selection and the evolution of obligatory sex. BMC Evol. Biol. 7 : 245.
84. Hadany, L. & M.W. Feldman. 2005. Evolutionary traction: the cost of adaptation and the evolution of sex. J. Evol. Biol. 18 : 309 314.
85. Hadany, L. & S.P. Otto. 2007. The evolution of condition-dependent sex in the face of high costs. Genetics 176 : 1713 1727.
86. Haddrill, P.R. et al. 2007. Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol. 8 : R18.
87. Haldane, J.B.S. 1935. The rate of spontaneous mutation of a human gene. J. Genet. 31 : 317 326.
88. Hamilton, W.D. et al. 1990. Sexual reproduction as an adaptation to resist parasites. Proc. Nat. Acad. Sci. USA 87 : 3566 3573.
89. Hill, W.G. & A. Robertson. 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8 : 269 294.
90. Hilton, H. et al. 1994. Using hitchhiking genes to study adaptation and divergence during speciation within the Drosophila melanogaster species complex. Evolution 48 : 1900 1913.
91. Hoffman, A.A. & P.A. Parsons. 1991. Evolutionary Genetics and Environmental Stress. Oxford University Press. New York.
92. Howard, R.S. & C.M. Lively. 1994. Parasitism, mutation accumulation and the maintenance of sex. Nature 367 : 554 557.
93. Howard, R.S. & C.M. Lively. 1998. The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution 52 : 604 610.
94. Hudson, R.R. & N.L. Kaplan. 1995. Deleterious background selection with recombination. Genetics 141 : 1605 1617.
95. Hurst, L.D. 1993. The incidences, mechanisms and evolution of cytoplasmic sex-ratio distorters in animals. Biol. Rev. Camb. Philos. Soc. 68 : 121 194.
96. Hutson, V. & R. Law. 1981. Evolution of recombination in populations experiencing frequency-dependent selection with time-delay. Proc. R. Soc. Lond. B Biol. Sci. 213 : 345 359.
97. Jeffreys, A.J. et al. 2001. Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nat. Genet. 29 : 217 222.
98. Kaplan, N.L. et al. 1989. The hitchhiking effect revisited. Genetics 123 : 887 899.
99. Kassir, Y. et al. 1988. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell 52 : 853 862.
100. Keightley, P.D. & S.P. Otto. 2006. Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443 : 89 92.
101. Kelly, J.K. 2005. Epistasis in monkeyflowers. Genetics 171 : 1917 1931.
102. Kidwell, M. 1972. Genetic change of recombination value in Drosophila melanogaster. I. Artificial selection for high and low recombination and some properties of recombination-modifying genes. Genetics 70 : 419 432.
103. Kim, Y. & W. Stephan. 2003. Selective sweeps in the presence of interference among partially linked Loci. Genetics 164 : 389 398.
104. Kimura, M. 1962. On the probability of fixation of mutant genes in a population. Genetics 47 : 713 719.
105. Kliman, R.M. & J. Hey. 1993a. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics 133 : 375 387.
106. Kliman, R.M. & J. Hey. 1993b. Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol. Biol. Evol. 10 : 1239 1258.
107. Kliman, R.M. & J. Hey. 2003. Hill-Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genet. Res. 81 : 89 90.
108. Kondrashov, A.S. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336 : 435 440.
109. Kondrashov, A.S. 1994. Mullers ratchet under epistatic selection. Genetics 136 : 1469 1473.
110. Kondrashov, A.S. & L.Y. Yampolsky. 1996. Evolution of amphimixis and recombination under fluctuating selection in one and many traits. Genet. Res. 68 : 165 173.
111. Korol, A.B. & K.G. Iliadi. 1994. Increased recombination frequencies resulting from directional selection for geotaxis in Drosophila. Heredity 72 : 64 68.
112. Korol, A.B. et al. 1994. Recombination Variability and Evolution. Chapman & Hall. London.
113. Kraft, T. et al. 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.
114. Ladle, R.J. et al. 1993. Coevolutionary dynamics of sex in a metapopulation - escaping the red queen. Proc. R. Soc. Lond. B Biol. Sci. 253 : 155 160.
115. Lawrence, M. 1958. Genotypic control of crossing-over on the first chromosome of Drosophila melanogaster. Nature 182 : 889 890.
116. Lenormand, T. & S.P. Otto. 2000. The evolution of recombination in a heterogeneous environment. Genetics 156 : 423 438.
117. Lewontin, R.C. 1971. The effect of genetic linkage on the mean fitness of a population. Proc. Natl. Acad. Sci. USA 68 : 984 986.
118. Liberman, U. & M.W. Feldman. 1986. A general reduction principle for genetic modifiers of recombination. Theor. Popul. Biol. 30 : 341 371.
119. Lichten, M. & A.S. Goldman. 1995. Meiotic recombination hotspots. Annu. Rev. Genet. 29 : 423 444.
120. Lynch M.B.J. 1998. Deleterious mutation accumulation in organelle genomes. Genetica 102-103 : 29 39.
121. Lyttle, T.W. 1991. Segregation distorters. Annu. Rev. Genet. 25 : 511 557.
122. Machado, C.A. et al. 2002. Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol. Biol. Evol. 19 : 472 488.
123. Makova, K.D. & W.H. Li. 2002. Strong male-driven evolution of DNA sequences in humans and apes. Nature 416 : 624 626.
124. Manning, J.T. & D.J. Thompson. 1984. Muller's ratchet and the accumulation of favorable mutations. Acta Biotheor. 33 : 219 225.
125. Marais, G. et al. 2004. Correlated evolution of synonymous and nonsynonymous sites in Drosophila. J. Mol. Evol. 59 : 771 779.
126. Marais, G. et al. 2003. Neutral effect of recombination on base composition in Drosophila. Genet. Res. 81 : 79 87.
127. Marais, G. & G. Piganeau. 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.
128. Maynard Smith, J. 1971. The origin and maintenance of sex. In Group Selection. G.C. Williams, Ed 163 175. Aldine-Atherton. Chicago.
129. Maynard Smith, J. 1978. The Evolution of Sex. Cambridge University Press. Cambridge, UK.
130. Maynard Smith, J. & J. Haigh. 1974. The hitch-hiking effect of a favorable gene. Genet. Res. 23 : 23 35.
131. McKim, K. et al. 2002. Meiotic recombination and chromosome segregation in Drosophila females. Annu. Rev. Genet. 36 : 205 232.
132. McPhee, C.P. & A. Robertson. 1970. Effect of suppressing crossing-over on response to selection in Drosophila melanogaster. Genet. Res. 16 : 1 16.
133. Miller, L.H. et al. 1975. Erythrocyte receptors for Plasmodium knowlesi malaria: Duffy blood group determinants. Science 189 : 561 563.
134. Moran, P.A.P. 1961. The survival of a mutant under general conditions. Proc. Cambridge Philos. Soc. 57 : 304 314.
135. Moriyama, E.N. & J.R. Powell. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol. Biol. Evol. 13 : 261 277.
136. Mukai, T. 1969. Genetic structure of natural populations of Drosophila melanogaster. 7. Synergistic interaction of spontaneous mutant polygenes controlling viability. Genetics 61 : 749 761.
137. Muller, H.J. 1964. The relation of recombination to mutational advance. Mutat. Res. 106 : 2 9.
138. Nachman, M.W. 1997. Patterns of DNA variability at X-linked loci in Mus domesticus. Genetics 147 : 1303 1316.
139. Nachman, M.W. 1998. Deleterious mutations in animal mitochondrial DNA. Genetica 102-103 : 61 69.
140. Nei, M. 1967. Modification of linkage intensity by natural selection. Genetics 57 : 625 641.
141. Nunney, L. 1989. The maintenance of sex by group selection. Evolution 43 : 245 257.
142. Orr, H.A. 2000. The rate of adaptation in asexuals. Genetics 155 : 961 968.
143. Otto, S.P. 2003. The advantages of segregation and the evolution of sex. Genetics 164 : 1099 1118.
144. Otto, S.P. & N.H. Barton. 1997. The evolution of recombination: Removing the limits to natural selection. Genetics 147 : 879 906.
145. Otto, S.P. & N.H. Barton. 2001. Selection for recombination in small populations. Evolution 55 : 1921 1931.
146. Otto, S.P. & T. Lenormand. 2002. Resolving the paradox of sex and recombination. Nat. Rev. Genet. 3 : 252 261.
147. Otto, S.P. & Y. Michalakis. 1998. The evolution of recombination in changing environments. Trends Ecol. Evol. 13 : 145 151.
148. Otto, S.P. & S.L. Nuismer. 2004. Species interactions and the evolution of sex. Science 304 : 1018 1020.
149. Partridge, L. & L.D. Hurst. 1998. Sex and conflict. Science 281 : 2003 2008.
150. Peck, J.R. 1994. A ruby in the rubbish: beneficial mutations, deleterious mutations and the evolution of sex. Genetics 137 : 597 606.
151. Peck, J.R. & D. Waxman. 2000. Mutation and sex in a competitive world. Nature 406 : 399 404.
152. Peters, A.D. & C.M. Lively. 1999. The red queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. Am. Nat. 154 : 393 405.
153. Przeworski, M. et al. 2000. Adjusting the focus on human variation. Trends Genet. 16 : 296 302.
154. Ptak, S.E. et al. 2005. Fine-scale recombination patterns differ between chimpanzees and humans. Nat. Genet. 37 : 429 434.
155. Rice, W.R. 1994. Degeneration of a nonrecombining chromosome. Science 263 : 230 232.
156. Rice, W.R. & A.K. Chippindale. 2001a. Intersexual ontogenetic conflict. J. Evol. Biol. 14 : 685 693.
157. Rice, W.R. & A.K. Chippindale. 2001b. Sexual recombination and the power of natural selection. Science 294 : 555 559.
158. Rodell, C.F. et al. 2004. Modes of selection and recombination response in Drosophila melanogaster. J. Hered. 95 : 70 75.
159. Romanienko, P.J. & R.D. Camerini-Otero. 1999. Cloning, characterization, and localization of mouse and human SPO11. Genomics 61 : 156 169.
160. Sandstedt, S.A. & P.K. Tucker. 2005. Male-driven evolution in closely related species of the mouse genus Mus. J. Mol. Evol. 61 : 138 144.
161. Sasaki, A. & Y. Iwasa. 1987. Optimal recombination rate in fluctuating environments. Genetics 115 : 377 388.
162. Sawyer, S.A. et al. 2003. Bayesian analysis suggests that most amino acid replacements in Drosophila are driven by positive selection. J. Mol. Evol. 57 : S154 S164.
163. Simchen, G. & J. Stamberg. 1969. Fine and coarse controls of genetic recombination. Nature 222 : 329 332.
164. Sismanidis, A. 1942. Selection for an almost invariable character in Drosophila. J. Genet. 44 : 204 215.
165. Smith, N.G.C. & A. Eyre-Walker. 2002. Adaptive protein evolution in Drosophila. Nature 415 : 1022 1024.
166. Steinemann, M. & S. Steinemann. 1997. The enigma of Y chromosome degeneration: TRAM, a novel retrotransposon is preferentially located on the Neo-Y chromosome of Drosophila miranda. Genetics 145 : 261 266.
167. Steinemann, S. & M. Steinemann. 2001. Biased distribution of repetitive elements: a landmark for neo-Y chromosome evolution in Drosophila miranda. Cytogenet. Cell. Genet. 93 : 228 233.
168. Stephan, W. 1994. Effects of genetic recombination and population subdivision on nucleotide sequence variation in Drosophila ananassae. In Non-Neutral Evolution: Theories and Molecular Data. B. Golding, Ed 57 66. Chapman and Hall. New York.
169. Stephan, W. & C.H. Langley. 1998. DNA polymorphism in Lycopersicon and crossing-over per physical length. Genetics 150 : 1585 1593.
170. Takano, T.S. 1998. Rate variation of DNA sequence evolution in the Drosophila lineages. Genetics 149 : 959 970.
171. True, J.R. et al. 1996. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142 : 507 523.
172. Van Kleunen, M. & M. Fischer. 2003. Effects of four generations of density-dependent selection on life history traits and their plasticity in a clonally propagated plant. J. Evol. Biol. 16 : 474 484.
173. Van Valen, L. 1973. A new evolutionary law. Evol. Theor. 1 : 1 30.
174. Wagner, A. 2005. Robustness, evolvability, and neutrality. FEBS Lett. 579 : 1772 1778.
175. Wang, J. et al. 1999. Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet. Res. 74 : 165 178.
176. Waxman, D. & J.R. Peck. 1999. Sex and adaptation in a changing environment. Genetics 153 : 1041 1053.
177. West, S.A. et al. 2001. Immune stress and facultative sex in a parasitic nematode. J. Evol. Biol. 14 : 333 337.
178. West, S.A. et al. 1999. A pluralist approach to sex and recombination. J. Evol. Biol. 12 : 1003 1012.
179. Whitlock, M.C. & D. Bourguet. 2000. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54 : 1654 1660.
180. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16 : 97 159.
181. Yu, A. et al. 2001. Comparison of human genetic and sequence-based physical maps. Nature 409 : 951 953.
182. Zeyl, C. 2005. The number of mutations selected during adaptation in a laboratory population of Saccharomyces cerevisiae. Genetics 169 : 1825 1831.
183. Zeyl, C. & G. Bell. 1997. The advantage of sex in evolving yeast populations. Nature 388 : 465 468.
184. Zhuchenko, A.A. et al. 1985. Change in the crossing-over frequency in Drosophila during selection for resistance to temperature fluctuations. Genetica 67 : 73 78.
185. Zhuchenko, A.A. et al. 1986. The correlation between the stability of the genotype and the change in its recombination characteristics under temperature influences. Genetika 22 : 966 974.
186. Zurovcova, M. & W.F. Eanes. 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.