Multilocus patterns of nucleotide variability and the demographic and selection history of drosophila melanogaster populations

Penelope R Haddrill, Kevin R Thornton, Brian Charlesworth, Peter Andolfatto

Research output: Contribution to journalArticle

205 Citations (Scopus)

Abstract

Uncertainty about the demographic history of populations can hamper genome-wide scans for selection based on population genetic models. To obtain a portrait of the effects of demographic history on genome variability patterns in Drosophila melanogaster populations, we surveyed noncoding DNA polymorphism at 10 X-linked loci in large samples from three African and two non-African populations. All five populations show significant departures from expectations under the standard neutral model. We detect weak but significant differentiation between East (Kenya and Zimbabwe) and West/Central sub-Saharan (Gabon) African populations. A skew toward high-frequency-derived polymorphisms, elevated levels of linkage disequilibrium (LD) and significant heterogeneity in levels of polymorphism and divergence in the Gabon sample suggest that this population is further from mutation-drift equilibrium than the two Eastern African populations. Both non-African populations harbor significantly higher levels of LD, a large excess of high-frequency-derived mutations and extreme heterogeneity among loci in levels of polymorphism and divergence. Rejections of the neutral model in D. melanogaster populations using these and similar features have been interpreted as evidence for an important role for natural selection in shaping genome variability patterns. Based on simulations, we conclude that simple bottleneck models are sufficient to account for most, if not all, polymorphism features of both African and non-African populations. In contrast, we show that a steady-state recurrent hitchhiking model fails to account for several aspects of the data. Demographic departures from equilibrium expectations in both ancestral and derived populations thus represent a serious challenge to detecting positive selection in genome-wide scans using current methodologies.

LanguageEnglish
Pages790-799
Number of pages10
JournalGenome Research
Volume15
Issue number6
DOIs
Publication statusPublished - Jun 2005

Fingerprint

Drosophila melanogaster
Polymorphism
Nucleotides
Demography
Genes
Population
Gabon
Genome
Ports and harbors
Linkage Disequilibrium
Zimbabwe
DNA
Genetic Selection
Kenya
Genetic Models
Population Genetics
Mutation Rate
Uncertainty
History
Mutation

Keywords

  • animals
  • base sequence
  • drosophila melanogaster
  • genes, insect
  • genetics, population
  • linkage disequilibrium
  • molecular sequence data
  • polymorphism, genetic
  • quantitative trait loci
  • selection, genetic
  • X chromosome
  • drosophila melanogaster populations
  • multilocus patterns
  • nucleotide variability
  • demographic and selection
  • history

Cite this

Haddrill, Penelope R ; Thornton, Kevin R ; Charlesworth, Brian ; Andolfatto, Peter. / Multilocus patterns of nucleotide variability and the demographic and selection history of drosophila melanogaster populations. In: Genome Research. 2005 ; Vol. 15, No. 6. pp. 790-799.
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Multilocus patterns of nucleotide variability and the demographic and selection history of drosophila melanogaster populations. / Haddrill, Penelope R; Thornton, Kevin R; Charlesworth, Brian; Andolfatto, Peter.

In: Genome Research, Vol. 15, No. 6, 06.2005, p. 790-799.

Research output: Contribution to journalArticle

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AB - Uncertainty about the demographic history of populations can hamper genome-wide scans for selection based on population genetic models. To obtain a portrait of the effects of demographic history on genome variability patterns in Drosophila melanogaster populations, we surveyed noncoding DNA polymorphism at 10 X-linked loci in large samples from three African and two non-African populations. All five populations show significant departures from expectations under the standard neutral model. We detect weak but significant differentiation between East (Kenya and Zimbabwe) and West/Central sub-Saharan (Gabon) African populations. A skew toward high-frequency-derived polymorphisms, elevated levels of linkage disequilibrium (LD) and significant heterogeneity in levels of polymorphism and divergence in the Gabon sample suggest that this population is further from mutation-drift equilibrium than the two Eastern African populations. Both non-African populations harbor significantly higher levels of LD, a large excess of high-frequency-derived mutations and extreme heterogeneity among loci in levels of polymorphism and divergence. Rejections of the neutral model in D. melanogaster populations using these and similar features have been interpreted as evidence for an important role for natural selection in shaping genome variability patterns. Based on simulations, we conclude that simple bottleneck models are sufficient to account for most, if not all, polymorphism features of both African and non-African populations. In contrast, we show that a steady-state recurrent hitchhiking model fails to account for several aspects of the data. Demographic departures from equilibrium expectations in both ancestral and derived populations thus represent a serious challenge to detecting positive selection in genome-wide scans using current methodologies.

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KW - selection, genetic

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