PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of transbThe Royal Society PublishingPhilosophical Transactions BAboutBrowse By SubjectAlertsFree Trial
 
Philos Trans R Soc Lond B Biol Sci. 2000 November 29; 355(1403): 1553–1562.
PMCID: PMC1692896

Genetic hitchhiking.

Abstract

Selection on one or more genes inevitably perturbs other genes, even when those genes have no direct effect on fitness. This article reviews the theory of such genetic hitchhiking, concentrating on effects on neutral loci. Maynard Smith and Haigh introduced the classical case where the perturbation is due to a single favourable mutation. This is contrasted with the apparently distinct effects of inherited variation in fitness due to loosely linked loci. A model of fluctuating selection is analysed which bridges these alternative treatments. When alleles sweep between extreme frequencies at a rate lambda, the rate of drift is increased by a factor (1 + E[1/pq]lambda/(2(2lambda + r))), where the recombination rate r is much smaller than the strength of selection. In spatially structured populations, the effects of any one substitution are weaker, and only cause a local increase in the frequency of a neutral allele. This increase depends primarily on the rate of recombination relative to selection (r/s), and more weakly, on the neighbourhood size, Nb = 4(pi rho sigma)2. Spatial subdivision may allow local selective sweeps to occur more frequently than is indicated by the overall rate of molecular evolution. However, it seems unlikely that such sweeps can be sufficiently frequent to increase significantly the drift of neutral alleles.

Full Text

The Full Text of this article is available as a PDF (333K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aguade M, Miyashita N, Langley CH. Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics. 1989 Jul;122(3):607–615. [PubMed]
  • Barton NH. The effects of linkage and density-dependent regulation on gene flow. Heredity (Edinb) 1986 Dec;57(Pt 3):415–426. [PubMed]
  • Begun DJ, Aquadro CF. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature. 1993 Oct 7;365(6446):548–550. [PubMed]
  • Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. [PubMed]
  • Charlesworth B. Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol. 1998 May;15(5):538–543. [PubMed]
  • Charlesworth B. The evolution of chromosomal sex determination and dosage compensation. Curr Biol. 1996 Feb 1;6(2):149–162. [PubMed]
  • Charlesworth B, Nordborg M, Charlesworth D. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res. 1997 Oct;70(2):155–174. [PubMed]
  • Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. [PubMed]
  • Clegg MT, Kidwell JF, Kidwell MG, Daniel NJ. Dynamics of correlated genetic systems. I. Selection in the region of the Glued locus of Drosophila melanogaster. Genetics. 1976 Aug;83(4):793–810. [PubMed]
  • Eyre-Walker A, Keightley PD. High genomic deleterious mutation rates in hominids. Nature. 1999 Jan 28;397(6717):344–347. [PubMed]
  • Fay JC, Wu CI. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. [PubMed]
  • Filatov DA, Monéger F, Negrutiu I, Charlesworth D. Low variability in a Y-linked plant gene and its implications for Y-chromosome evolution. Nature. 2000 Mar 23;404(6776):388–390. [PubMed]
  • Gillespie JH. Junk ain't what junk does: neutral alleles in a selected context. Gene. 1997 Dec 31;205(1-2):291–299. [PubMed]
  • Galtier N, Depaulis F, Barton NH. Detecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics. 2000 Jun;155(2):981–987. [PubMed]
  • Gillespie JH. Genetic drift in an infinite population. The pseudohitchhiking model. Genetics. 2000 Jun;155(2):909–919. [PubMed]
  • Hey J. A multi-dimensional coalescent process applied to multi-allelic selection models and migration models. Theor Popul Biol. 1991 Feb;39(1):30–48. [PubMed]
  • Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966 Dec;8(3):269–294. [PubMed]
  • Hudson RR, Kaplan NL. The coalescent process in models with selection and recombination. Genetics. 1988 Nov;120(3):831–840. [PubMed]
  • Hudson RR, Kaplan NL. Deleterious background selection with recombination. Genetics. 1995 Dec;141(4):1605–1617. [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PubMed]
  • Kaplan N, Hudson RR, Iizuka M. The coalescent process in models with selection, recombination and geographic subdivision. Genet Res. 1991 Feb;57(1):83–91. [PubMed]
  • Ingvarsson PK, Whitlock MC. Heterosis increases the effective migration rate. Proc Biol Sci. 2000 Jul 7;267(1450):1321–1326. [PMC free article] [PubMed]
  • Kaplan NL, Hudson RR, Langley CH. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. [PubMed]
  • Keightley PD, Caballero A. Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3823–3827. [PubMed]
  • Keightley PD. Inference of genome-wide mutation rates and distributions of mutation effects for fitness traits: a simulation study. Genetics. 1998 Nov;150(3):1283–1293. [PubMed]
  • Keightley PD, Eyre-Walker A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics. 1999 Oct;153(2):515–523. [PubMed]
  • Kondrashov AS. Contamination of the genome by very slightly deleterious mutations: why have we not died 100 times over? J Theor Biol. 1995 Aug 21;175(4):583–594. [PubMed]
  • Kelly JK, Wade MJ. Molecular evolution near a two-locus balanced polymorphism. J Theor Biol. 2000 May 7;204(1):83–101. [PubMed]
  • Kruuk LE, Baird SJ, Gale KS, Barton NH. A comparison of multilocus clines maintained by environmental adaptation or by selection against hybrids. Genetics. 1999 Dec;153(4):1959–1971. [PubMed]
  • Liu F, Zhang L, Charlesworth D. Genetic diversity in Leavenworthia populations with different inbreeding levels. Proc Biol Sci. 1998 Feb 22;265(1393):293–301. [PMC free article] [PubMed]
  • Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed]
  • Medina JR, Petit C. L'effet hitch-hiking comme processus dispersif. J Theor Biol. 1979 Nov 21;81(2):235–246. [PubMed]
  • Nachman MW. Patterns of DNA variability at X-linked loci in Mus domesticus. Genetics. 1997 Nov;147(3):1303–1316. [PubMed]
  • Nachman MW, Bauer VL, Crowell SL, Aquadro CF. DNA variability and recombination rates at X-linked loci in humans. Genetics. 1998 Nov;150(3):1133–1141. [PubMed]
  • Nei M, Li WH. Linkage disequilibrium in subdivided populations. Genetics. 1973 Sep;75(1):213–219. [PubMed]
  • Nei M, Murata M. Effective population size when fertility is inherited. Genet Res. 1966 Oct;8(2):257–260. [PubMed]
  • Nordborg M. Structured coalescent processes on different time scales. Genetics. 1997 Aug;146(4):1501–1514. [PubMed]
  • Nordborg M, Charlesworth B, Charlesworth D. The effect of recombination on background selection. Genet Res. 1996 Apr;67(2):159–174. [PubMed]
  • Petry D. The effect on neutral gene flow of selection at a linked locus. Theor Popul Biol. 1983 Jun;23(3):300–313. [PubMed]
  • Notohara M. The coalescent and the genealogical process in geographically structured population. J Math Biol. 1990;29(1):59–75. [PubMed]
  • Piálek J, Barton NH. The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics. 1997 Feb;145(2):493–504. [PubMed]
  • Slatkin M, Maruyama T. Genetic drift in a cline. Genetics. 1975 Sep;81(1):209–222. [PubMed]
  • Santiago E, Caballero A. Effective size and polymorphism of linked neutral loci in populations under directional selection. Genetics. 1998 Aug;149(4):2105–2117. [PubMed]
  • Slatkin M, Wiehe T. Genetic hitch-hiking in a subdivided population. Genet Res. 1998 Apr;71(2):155–160. [PubMed]
  • Stephan W, Langley CH. 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. 1989 Jan;121(1):89–99. [PubMed]
  • Stephan W, Langley CH. DNA polymorphism in lycopersicon and crossing-over per physical length. Genetics. 1998 Dec;150(4):1585–1593. [PubMed]
  • Sved JA. Does natural selection increase or decrease variability at linked Loci. Genetics. 1983 Sep;105(1):239–240. [PubMed]
  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. [PubMed]
  • Whitlock MC, Barton NH. The effective size of a subdivided population. Genetics. 1997 May;146(1):427–441. [PubMed]
  • Woolliams JA, Bijma P, Villanueva B. Expected genetic contributions and their impact on gene flow and genetic gain. Genetics. 1999 Oct;153(2):1009–1020. [PubMed]
  • Wray NR, Thompson R. Prediction of rates of inbreeding in selected populations. Genet Res. 1990 Feb;55(1):41–54. [PubMed]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society