Abstract
The effect of genetic hitchhiking on neutral variation is analyzed in subdivided populations with differentiated demes. After fixation of a favorable mutation, the consequences on particular subpopulations can be radically different. In the subpopulation where the mutation first appeared by mutation, variation at linked neutral loci is expected to be reduced, as predicted by the classical theory. However, the effect in the other subpopulations, where the mutation is introduced by migration, can be the opposite. This effect depends on the level of genetic differentiation of the subpopulations, the selective advantage of the mutation, the recombination frequency, and the population size, as stated by analytical derivations and computer simulations. The characteristic outcomes of the effect are three. First, the genomic region of reduced variation around the selected locus is smaller than that predicted in a panmictic population. Second, for more distant neutral loci, the amount of variation increases over the level they had before the hitchhiking event. Third, for these loci, the spectrum of gene frequencies is dominated by an excess of alleles at intermediate frequencies when compared with the neutral theory. At these loci, hitchhiking works like a system that takes variation from the between-subpopulation component and introduces it into the subpopulations. The mechanism can also operate in other systems in which the genetic variation is distributed in clusters with limited exchange of variation, such as chromosome arrangements or genomic regions closely linked to targets of balancing selection.
MeSH Terms
Animals
Computer Simulation
Drosophila melanogaster/genetics
Genetic Variation
Genetics, Population
Genome
Polymorphism, Genetic
Recombination, Genetic
Sample Size
Selection, Genetic
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Santiago Enrique
Departamento de Biología Funcional, Facultad de Biología, Universidad de Oviedo, 33071 Oviedo, Spain.
[email protected]
Caballero Armando
References (23)
23 references, click to expand
-
Selective sweep at the Drosophila melanogaster Suppressor of Hairless locus and its association with the In(2L)t inversion polymorphism.
Genetics. 1999 Jul;152(3):1017-24
PMID: 10388820
-
Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus.
Am J Hum Genet. 2000 May;66(5):1669-79
PMID: 10762551
-
Contrasting evolutionary histories of two introns of the duchenne muscular dystrophy gene, Dmd, in humans.
Genetics. 2000 Aug;155(4):1855-64
PMID: 10924480
-
A selective sweep associated with a recent gene transposition in Drosophila miranda.
Genetics. 2000 Dec;156(4):1753-63
PMID: 11102371
-
Linkage disequilibria and the site frequency spectra in the su(s) and su(w(a)) regions of the Drosophila melanogaster X chromosome.
Genetics. 2000 Dec;156(4):1837-52
PMID: 11102378
-
Selective sweep near the In(2L)t inversion breakpoint in an African population of Drosophila melanogaster.
Genet Res. 2000 Oct;76(2):149-58
PMID: 11132408
-
Evidence for selection at the fused1 locus of Drosophila americana.
Genetics. 2001 May;158(1):279-90
PMID: 11333236
-
Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster.
Genetics. 2001 Jun;158(2):657-65
PMID: 11404330
-
Adaptive hitchhiking effects on genome variability.
Curr Opin Genet Dev. 2001 Dec;11(6):635-41
PMID: 11682306
-
Molecular evolution of the Est-6 gene in Drosophila melanogaster: contrasting patterns of DNA variability in adjacent functional regions.
Gene. 2002 Apr 17;288(1-2):167-77
PMID: 12034506
-
Natural selection at linked sites in humans.
Gene. 2002 Oct 30;300(1-2):31-42
PMID: 12468083
-
Estimation of the coancestry coefficient: basis for a short-term genetic distance.
Genetics. 1983 Nov;105(3):767-79
PMID: 17246175
-
Analyses of gene frequencies.
Genetics. 1973 Aug;74(4):679-700
PMID: 17248636
-
The genetical structure of populations.
Ann Eugen. 1951 Mar;15(4):323-54
PMID: 24540312
-
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
Genetics. 1989 Nov;123(3):585-95
PMID: 2513255
-
VARIANCE OF GENE FREQUENCIES.
Evolution. 1969 Mar;23(1):72-84
PMID: 28562963
-
ESTIMATING F-STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE.
Evolution. 1984 Nov;38(6):1358-1370
PMID: 28563791
-
The hitch-hiking effect of a favourable gene.
Genet Res. 1974 Feb;23(1):23-35
PMID: 4407212
-
Analysis of a genetic hitchhiking model, and its application to DNA polymorphism data from Drosophila melanogaster.
Mol Biol Evol. 1993 Jul;10(4):842-54
PMID: 8355603
-
The effect of deleterious mutations on neutral molecular variation.
Genetics. 1993 Aug;134(4):1289-303
PMID: 8375663
-
High nucleotide sequence variation in a region of low recombination in Drosophila simulans is consistent with the background selection model.
Mol Biol Evol. 1996 Oct;13(8):1133-40
PMID: 8865667
-
The evolution of recombination: removing the limits to natural selection.
Genetics. 1997 Oct;147(2):879-906
PMID: 9335621
-
Genetic hitch-hiking in a subdivided population.
Genet Res. 1998 Apr;71(2):155-60
PMID: 9717437