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Cited by 601Evolution and Genetic DynamicsGenetic diversity and population structureForensic and Genetic Research

The hitchhiking effect on the site frequency spectrum of DNA polymorphisms

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Braverman, J M, Hudson, R R, Kaplan, N L, Langley, C H, Stephan, W·1995·Genetics
DOI 10.1093/genetics/140.2.783
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Abstract

The level of DNA sequence variation is reduced in regions of the Drosophila melanogaster genome where the rate of crossing over per physical distance is also reduced. This observation has been interpreted as support for the simple model of genetic hitchhiking, in which directional selection on rare variants, e.g., newly arising advantageous mutants, sweeps linked neutral alleles to fixation, thus eliminating polymorphisms near the selected site. However, the frequency spectra of segregating sites of several loci from some populations exhibiting reduced levels of nucleotide diversity and reduced numbers of segregating sites did not appear different from what would be expected under a neutral equilibrium model. Specifically, a skew toward an excess of rare sites was not observed in these samples, as measured by Tajima's D. Because this skew was predicted by a simple hitchhiking model, yet it had never been expressed quantitatively and compared directly to DNA polymorphism data, this paper investigates the hitchhiking effect on the site frequency spectrum, as measured by Tajima's D and several other statistics, using a computer simulation model based on the coalescent process and recurrent hitchhiking events. The results presented here demonstrate that under the simple hitchhiking model (1) the expected value of Tajima's D is large and negative (indicating a skew toward rare variants), (2) that Tajima's test has reasonable power to detect a skew in the frequency spectrum for parameters comparable to those from actual data sets, and (3) that the Tajima's Ds observed in several data sets are very unlikely to have been the result of simple hitchhiking. Consequently, the simple hitchhiking model is not a sufficient explanation for the DNA polymorphism at those loci exhibiting a decreased number of segregating sites yet not exhibiting a skew in the frequency spectrum.

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  • The SFS of polymorphisms in genomic regions containing hybrid incompatibilities is expected to depart from the genome-wide SFS.

    “Therefore, we might expect the site frequency spectrum (SFS) of polymorphisms in genomic regions containing hybrid incompatibilities to depart from the genome-wide SFS (Braverman et al. 1995; Simonsen et al. 1995).”

    From Finding Hybrid Incompatibilities Using Genome Sequences from Hybrid Populations (2021) · cites this paper as Braverman et al. 1995

    The introductory passage (page unavailable) predicts that simple genetic hitchhiking skews the site frequency spectrum of linked polymorphisms toward rare variants. It does not examine genomic regions containing hybrid incompatibilities or compare their spectra with a genome-wide SFS, so the claim extends the paper’s prediction to a different setting. (LLM, conf=0.86)

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Research works printed but not linked: 5

  1. AGUADE, M., W. MEYERS, A. D. LONG and C. H. LANGLEY, 1994 Reduced DNA sequence polymorphism in the s u ( s ) and su( w") regions of Drosophila melanogaster as revealed by SSCP and stratified DNA sequencing. Proc. Natl. Acad. Sci. USA 91: 4658-4662.
  2. HUDSON, R. R., 1993 The how and why of generating gene genealo- gies, pp. 23-36 in Mechanisms of Molecular Evolution: Introduction to Molecular Paleopopulation Biology, edited by N. TAKAHATA and A. G. CLARK. Sinauer Associates, Sunderland, MA.
  3. KIMURA, M., 1983 The Neutral T h e q of Molecular Evolution. Cam- bridge University Press, Cambridge.
  4. KREITMAN, M., 1991 Detecting selection at the level of DNA, pp. 204-221 in Evolution at the Molecular Level, edited by R. K SE- LANDER, A. G. CLARK and T. S. WHITTAM. Sinauer Associates, Sunderland, MA.
  5. STEPHAN, W., and C. H. LANGLw, 1989 Molecular genetic variation in the centromeric region of the Xchromosome in three Drosoph- 806-809. 90: 1800-1803. Downloaded from https://academic.oup.com/genetics/article/140/2/783/6016583 by guest on 17 August 2023 ila ananassue populations. I. Contrasts between the vermilion and forked loci. Genetics 121: 89-99.

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Authors
Braverman, J. M., Hudson, R. R., Kaplan, N. L., Langley, C. H., & Stephan, W.
Affiliations
  • University of California, Davis (US)
  • University of Maryland, College Park (US)
  • National Institute of Environmental Health Sciences (US)
  • University of California System (US)
ORCID
Venue
Genetics
Publisher
Oxford University Press (OUP)
Published
1995-06-01
Volume
140
Issue
2
Pages
783-796
ISSN
  • 0016-6731 (ISSN-L)
  • 1943-2631
DOI
10.1093/genetics/140.2.783
OpenAlex
W1947714123
Cited by
601
References
35
Citations by year
2026: 10 · 2025: 16 · 2024: 19 · 2023: 9 · 2022: 10 · 2021: 15 · 2020: 10 · 2019: 11 · 2018: 19 · 2017: 14 · 2016: 15 · 2015: 17 · 2014: 32 · 2013: 17 · 2012: 20
FWCI
9.57
Type
journal article
Language
en
Open access
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations
  • Genetics (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
Keywords
genetic hitchhiking, site frequency spectrum, Tajima's D, DNA polymorphism, Drosophila melanogaster, recombination rate, coalescent simulation, nucleotide diversity, segregating sites, population genetics
MeSH terms
Animals, DNA, Drosophila melanogaster, Models, Genetic, Polymorphism, Genetic, Genetic Variation

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