Abstract
Recurrent directional selection on a partially recombining chromosome may cause a substantial reduction of standing genetic variation in natural populations. Previous studies of this effect, commonly called selective sweeps, assumed that at most one beneficial allele is on the way to fixation at a given time. However, for a high rate of selected substitutions and a low recombination rate, this assumption can easily be violated. We investigated this problem using full-forward simulations and analytical approximations. We found that interference between linked beneficial alleles causes a reduction of their fixation probabilities. The hitchhiking effect on linked neutral variation for a given substitution also slightly decreases due to interference. As a result, the strength of recurrent selective sweeps is weakened. However, this effect is significant only in chromosomal regions of relatively low recombination rates where the level of variation is greatly reduced. Therefore, previous results on recurrent selective sweeps although derived for a restricted parameter range are still valid. Analytical approximations are obtained for the case of complete linkage for which interference between competing beneficial alleles is maximal.
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- Andolfatto P. Adaptive hitchhiking effects on genome variability. Curr Opin Genet Dev. 2001 Dec;11(6):635–641. doi: 10.1016/s0959-437x(00)00246-x. [DOI] [PubMed] [Google Scholar]
- Barton N. H. Genetic hitchhiking. Philos Trans R Soc Lond B Biol Sci. 2000 Nov 29;355(1403):1553–1562. doi: 10.1098/rstb.2000.0716. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barton N. H. Linkage and the limits to natural selection. Genetics. 1995 Jun;140(2):821–841. doi: 10.1093/genetics/140.2.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
- Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Charlesworth B. Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet Res. 1996 Oct;68(2):131–149. doi: 10.1017/s0016672300034029. [DOI] [PubMed] [Google Scholar]
- Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fay J. C., Wu C. I. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. doi: 10.1093/genetics/155.3.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gerrish P. J., Lenski R. E. The fate of competing beneficial mutations in an asexual population. Genetica. 1998;102-103(1-6):127–144. [PubMed] [Google Scholar]
- Gillespie J. H. Genetic drift in an infinite population. The pseudohitchhiking model. Genetics. 2000 Jun;155(2):909–919. doi: 10.1093/genetics/155.2.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gillespie J. H. The neutral theory in an infinite population. Gene. 2000 Dec 30;261(1):11–18. doi: 10.1016/s0378-1119(00)00485-6. [DOI] [PubMed] [Google Scholar]
- Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kim Y., Stephan W. Joint effects of genetic hitchhiking and background selection on neutral variation. Genetics. 2000 Jul;155(3):1415–1427. doi: 10.1093/genetics/155.3.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kim Yuseob, Stephan Wolfgang. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics. 2002 Feb;160(2):765–777. doi: 10.1093/genetics/160.2.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Przeworski Molly. The signature of positive selection at randomly chosen loci. Genetics. 2002 Mar;160(3):1179–1189. doi: 10.1093/genetics/160.3.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sawyer S. A., Hartl D. L. Population genetics of polymorphism and divergence. Genetics. 1992 Dec;132(4):1161–1176. doi: 10.1093/genetics/132.4.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slatkin M. Inbreeding coefficients and coalescence times. Genet Res. 1991 Oct;58(2):167–175. doi: 10.1017/s0016672300029827. [DOI] [PubMed] [Google Scholar]
- Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
- Stephan W. An improved method for estimating the rate of fixation of favorable mutations based on DNA polymorphism data. Mol Biol Evol. 1995 Sep;12(5):959–962. doi: 10.1093/oxfordjournals.molbev.a040274. [DOI] [PubMed] [Google Scholar]
- Wiehe T. H., Stephan W. Analysis of a genetic hitchhiking model, and its application to DNA polymorphism data from Drosophila melanogaster. Mol Biol Evol. 1993 Jul;10(4):842–854. doi: 10.1093/oxfordjournals.molbev.a040046. [DOI] [PubMed] [Google Scholar]