Genetic hitchhiking versus background selection: The controversy and its implications

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1544, 2010, Pages 1245-1253

  Stephan, Wolfgang ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Adaptation; Background selection; Genetic hitchhiking; Reduction of nucleotide diversity in regions of restricted recombination; Selective sweeps

Indexed keywords

ADAPTATION; DOMESTICATION; GENE; MUTATION; NATURAL SELECTION; POPULATION GENETICS; RECOMBINATION;

EID: 77951615674     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0278     Document Type: Review

References (71)

1. Adams, M. D. et al. 2000 The genome sequence of Drosophila melanogaster. Science 287, 2185-2195. (doi:10.1126/science.287.5461.2185)
2. Aguadé, M., Miyashita, N. & Langley, C. H. 1989 Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics 122, 607-615.
3. Akey, J. M. et al. 2004 Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2, e286. (doi:10.1371/journal.pbio.0020286)
4. Andolfatto, P. & Przeworski, M. 2001 Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics 158, 657-665.
5. Aquadro, C. F., Begun, D. J. & Kindahl, E. C. 1994 Selection, recombination, and DNA polymorphism in Drosophila. In Non-neutral evolution: theories and molecular data (ed. B. Golding), pp. 46-56. New York, NY: Chapman & Hall.
6. Baines, J. F., Das, A., Mousset, S. & Stephan, W. 2004 The role of natural selection in genetic differentiation of worldwide populations of Drosophila ananassae. Genetics 168, 1987-1998. (doi: 10.1534/genetics. 104.027482)
7. Barton, N. H. 1998 The effect of hitch-hiking on neutral genealogies. Genet. Res. 72, 123-133. (doi:10.1017/S0016672398003462)
8. Bauer DuMont, V. & Aquadro, C. R 2005 Multiple signatures of positive selection downstream of Notch on the X chromosome in Drosophila melanogaster. Genetics 111, 639-653.
9. Beaumont, M. A. & Balding, D. J. 2004 Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13, 969-980. (doi:10.1111/j.1365-294X. 2004.02125.x)
10. Begun, D. J. & Aquadro, C. F. 1992 Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519-520. (doi:10.1038/356519a0)
11. Beisswanger, S. & Stephan, W. 2008 Evidence that strong positive selection drives neofunctionalization in the tandemly duplicated polyhomeotic genes in Drosophila. Proc. Natl Acad. Sci. USA 105, 5447-5452. (doi: 10.1073/pnas.0710892105)
12. Beisswanger, S., Stephan, W. & De Lorenzo, D. 2006 Evidence for a selective sweep in the wapl region of Drosophila melanogaster. Genetics 172, 265-274. (doi:10.1534/genetics.105.049346)
13. Braverman, J. M., Hudson, R. R., Kaplan, N. L., Langley, C. H. & Stephan, W. 1995 The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140, 783-796.
14. Charlesworth, B. 1996 Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet. Res. 68, 131-149. (doi:10.1017/S0016672300034029)
15. Charlesworth, B. 2009 Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10, 195-205. (doi:10.1038/nrg2526)
16. Charlesworth, B., Morgan, M. T. & Charlesworth, D. 1993 The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289-1303. (Pubitemid 23220050)
17. Chen, Y., Marsh, B. J. & Stephan, W. 2000 Joint effects of natural selection and recombination on gene flow between Drosophila ananassae populations. Genetics 155, 1185-1194.
18. David, J. R. & Capy, P. 1988 Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4, 106-111. (doi:10.1016/0168- 9525(88)90098-4)
19. Pay, J. C. & Wu, C. -I. 2000 Hitchhiking under positive Darwinian selection. Genetics 155, 1405-1413.
20. Fu, Y.-X. & Li, W. H. 1993 Statistical tests of neutrality of mutations. Genetics 133, 693-709.
21. Glinka, S., Ometto, L., Mousset, S., Stephan, W. & De Lorenzo, D. 2003 Demography and natural selection have shaped genetic variation in Drosophila melanogaster. a multi-locus approach. Genetics 165, 1269-1278. (Pubitemid 38020248)
22. Glinka, S., De Lorenzo, D. & Stephan, W 2006 Evidence of gene conversion associated with a selective sweep in Drosophila melanogaster. Mol. Biol. Evol. 23, 1869-1878. (doi: 10.1093/molbev/ms1069)
23. Harr, B., Kauer, M. & Schlötterer, C. 2002 Hitchhiking mapping: a population-based fine-mapping strategy for adaptive mutations in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 99, 12949-12954. (doi:10.1073/pnas. 202336899)
24. Hellmann, I., Ebersberger, I., Ptak, S. E., Pääbo, S. & Przeworski, M. 2003 A neutral explanation for the correlation of diversity with recombination rates in humans. Am. J. Hum. Genet. 11, 1527-1535. (doi:10.1086/375657)
25. Hill, W. G. & Robertson, A. 1966 The effect of linkage on limits to artificial selection. Genet. Res. 8, 269-294. (doi:10.1017/S0016672300010156)
26. Hudson, R. R. & Kaplan, N. L. 1995 Deleterious background selection with recombination. Genetics 141, 1605-1617.
27. Hutter, S., Li, H., Beisswanger, S., De Lorenzo, D. & Stephan, W. 2007 Distinctly different sex ratios in African and European populations of Drosophila melanogaster inferred from chromosome-wide single nucleotide polymorphism data. Genetics 177, 469-480. (doi: 10.1534/genetics. 107.074922)
28. Innan, H. & Stephan, W. 2000 The coalescent in an exponentially growing metapopulation and its application to Arabidopsis thaliana. Genetics 155, 2015-2019.
29. Innan, H. & Stephan, W. 2003 Distinguishing the hitchhiking and background selection models. Genetics 165, 2307-2312. (Pubitemid 38040311)
30. Jensen, J. D., Kim, Y., Bauer DuMont, V., Aquadro, C. F. & Bustamante, C. D. 2005 Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170, 1401-1410.(doi: 10.1534/genetics. 104. 038224)
31. Jensen, J. D., Bauer DuMont, V., Ashmore, A. B., Gutierrez, A. & Aquadro, C. F. 2007 Patterns of sequence variability and divergence at the diminuitive gene region of Drosophila melanogaster. complex patterns suggest an ancestral selective sweep. Genetics 177, 1071-1085. (doi:10.1534/genetics. 106.069468)
32. Jensen, J. D., Thornton, K. R. & Andolfatto, P. 2008 An approximate Bayesian estimator suggests strong, recurrent selective sweeps in Drosophila. PLoS Genet. 4, e1000198. (doi:10.1371/journal.pgen.1000198)
33. Kaiser, V. B. & Charlesworth, B. 2009 The effects of deleterious mutations on evolution in non-recombining chromosomes. Trends Genet. IS, 9-12. (doi: 10.1016/j.tig. 2008.10.009)
34. Kaplan, N. L., Hudson, R. R. & Langley, C. H. 1989 The 'hitchhiking effect' revisited. Genetics 123, 887-899.
35. Kim, Y. & Stephan, W. 2000 Joint effects of genetic hitchhiking and background selection on neutral variation. Genetics 155, 1415-1427.
36. Kim, Y. & Stephan, W. 2002 Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160, 765-777. (Pubitemid 34194545)
37. Kim, Y. & Stephan, W. 2003 Selective sweeps in the presence of interference among partially linked loci. Genetics 164, 389-398.
38. Lange, B. W., Langley, C. H. & Stephan, W. 1990 Molecular evolution of Drosophila metallothionein genes. Genetics 126, 921-932.
39. Langley, C. H., MacDonald, J., Miyashita, N. & Aguadé, M. 1993 Lack of correlation between interspecific divergence and intraspecific polymorphism in the suppressor of forked region in Drosophila melanogaster and D. simulons. Proc. Natl Acad. Sci. USA 90, 1800-1803. (doi:10.1073/pnas.90.5. 1800)
40. Li, H. & Stephan, W. 2006 Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet. 2,e166. (doi:10.1371/ journal.pgen.0020166)
41. Loewe, L. & Charlesworth, B. 2007 Background selection in single genes may explain patterns of codon bias. Genetics 175, 1381-1393. (doi: 10.1534/genetics. 106. 065557)
42. Martin-Campos, J. M., Comerón, J. M., Miyashita, N. & Aguadé, M. 1992 Intraspecific and interspecific variation at the y-ac-sc region of Drosophila simulons and D. melanogaster. Genetics 130, 805-816.
43. Maynard Smith, J. & Haigh, J. 1974 The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23-35.
44. Nachman, M. W., Bauer, V. L., Crowell, S. L. & Aquadro, C. F. 1998 DNA variability and recombination rates at X-linked loci in humans. Genetics 150, 1133-1141.
45. Nielsen, R. et al. 2005 Genomic scans for selective sweeps using SNP data. Genome Res. 15, 1566-1575. (doi:10.1101/gr.4252305)
46. Nordborg, M., Charlesworth, B. & Charlesworth, D. 1996 The effect of recombination on background selection. Genet. Res. 67, 159-174. (doi:10.1017/S0016672300033619)
47. Ometto, L., Glinka, S., De Lorenzo, D. & Stephan, W. 2005 Inferring the effects of demography and selection on Drosophila melanogaster populations from a chromosomewide scan of DNA variation. Mol. Biol. Evol. 22, 2119-2130. (doi:10.1093/molbev/msi207)
48. Orengo, D. J. & Aguadé, M. 2004 Detecting the footprint of positive selection in a European population of Drosophila melanogaster: multilocus patterns of variation and distance to coding regions. Genetics 167, 1759-1766. (doi:10.1534/genetics.104.028969)
49. Orengo, D. J. & Aguadé, M. 2007 Genome scans of variation and adaptive change: extended analysis of a candidate locus close to the phantom gene region in Drosophila melanogaster. Mol. Biol. Evol. 24, 1122-1129. (doi:10.1093/molbev/msm032)
50. Pavlidis, P., Hutter, S. & Stephan, W. 2008 A population genomic approach to map recent positive selection in model species. Mol. Ecol. 17, 3585-3598.
51. Perlitz, M. & Stephan, W. 1997 The mean and variance of the number of segregating sites since the last hitchhiking event. J. Math. Biol. 36, 1-23. (doi: 10.1007/S002850050087)
52. Pool, J. E., Bauer DuMont, V., Mueller, J. L. & Aquadro, C. F. 2006 A scan of molecular variation leads to a narrow localization of a selective sweep affecting both Afrotropical and cosmopolitan populations of Drosophila melanogaster. Genetics 172, 1093-1105. (doi:10.1534/genetics.105.049973)
53. Riebler, A., Held, L. & Stephan, W. 2008 Bayesian variable selection for detecting adaptive genomic differences among populations. Genetics 178, 1817-1829. (doi:10.1534/genetics.107.081281)
54. Roselius, K., Stephan, W. & Stadler, T. 2005 The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171, 753-763. (doi:10.1534/genetics.105.043877)
55. Ross-Ibarra, J. et al. 2008 Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoS One 3, e2411. (doi:10.1371/joumal.pone. 0002411)
56. Schwartz, Y. B. Pirrotta, V. 2007 Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9-22. (doi: 10.1038/nrg1981) (Pubitemid 46006046)
57. Stephan, W. 1995 An improved method for estimating the rate of fixation of favorable mutations based on DNA polymorphism data. Mol. Biol. Evol. 12, 959-962.
58. Stephan, W. & Langley, C. H. 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 111, 89-99.
59. Stephan, W. & Langley, C. H. 1998 DNA polymorphism in Lycopersicon and crossing-over per physical length. Genetics 150, 1585-1593.
60. Stephan, W. & Mitchell, S. J. 1992 Reduced levels of DNA polymorphism and fixed between-population differences in the centromeric region of Drosophila ananassae. Genetics 132, 1039-1045.
61. Stephan, W., Wiehe, T. H. E. & Lenz, M. W. 1992 The effect of strongly selected substitutions on neutral polymorphism: analytical results based on diffusion theory. Theor. Popul. Biol. 41, 237-254. (doi: 10.1016/00405809(92)90045-11)
62. Stephan, W., Xing, L., Kirby, D. A. & Braverman, J. M. 1998 A test of the background selection hypothesis based on nucleotide data from Drosophila ananassae. Proc. Natl Acad. Sci. USA 95, 5649-5654. (doi: 10.1073/pnas.95.10. 5649)
63. Stephan, W., Charlesworth, B. & McVean, G. 1999 The effect of background selection at a single locus on weakly selected, partially linked variants. Genet. Res. 73, 133-146. (doi:10.1017/S0016672399003705)
64. Svetec, N., Pavlidis, P. & Stephan, W. 2009 Recent strong positive selection on Drosophila melanogaster HDAC6, a gene encoding a stress surveillance factor, as revealed by population genomic analysis. Mol. Biol. Evol. 26, 1549-1556. (doi:10.1093/molbev/msp065)
65. Tajima, F. 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595. (Pubitemid 19274682)
66. Vigoroux, Y. et al. 2002 Rate and pattern of mutation at microsatellite loci in maize. Mol. Biol. Evol. 19, 1251-1260.
67. Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. 2006 A map of recent positive selection in the human genome. PLoS Biol. 4, e72. (doi:10.1371/joumal.pbio. 0040072)
68. Wiehe, T. H. E. & Stephan, W. 1993 Analysis of a genetic hitchhiking model, and its application to DNA polymorphism data from Drosophila melanogaster. Mol. Biol. Evol. 10, 842-855.
69. Wright, S. I. & Gaut, B. S. 2005 Molecular population genetics and the search for adaptive evolution in plants. Mol. Biol. Evol. 11, 506-519. (doi:10.1093/molbev/msi035)
70. Wright, S. I. et al. 2005 The effects of artificial selection on the maize genome. Science 308, 1310-1314. (doi:10.1126/science.1107891)
71. Zivkovic, D. & Wiehe, T. 2008 Second order moments of segregating sites under variable population size. Genetics 180, 341-357. (doi:10.1534/genetics.108.091231)