Similar levels of X-linked and autosomal nucleotide variation in African and non-African populations of Drosophila melanogaster

Nadia D. Singh, J. Michael Macpherson, Jeffrey Jensen, Dmitri A. Petrov

Research output: Contribution to journalArticle

40 Citations (Scopus)

Abstract

Background. Levels of molecular diversity in Drosophila have repeatedly been shown to be higher in ancestral, African populations than in derived, non-African populations. This pattern holds for both coding and noncoding regions for a variety of molecular markers including single nucleotide polymorphisms and microsatellites. Comparisons of X-linked and autosomal diversity have yielded results largely dependent on population of origin. Results. In an attempt to further elucidate patterns of sequence diversity in Drosophila melanogaster, we studied nucleotide variation at putatively nonfunctional X-linked and autosomal loci in sub-Saharan African and North American strains of D. melanogaster. We combine our experimental results with data from previous studies of molecular polymorphism in this species. We confirm that levels of diversity are consistently higher in African versus North American strains. The relative reduction of diversity for X-linked and autosomal loci in the derived, North American strains depends heavily on the studied loci. While the compiled dataset, comprised primarily of regions within or in close proximity to genes, shows a much more severe reduction of diversity on the X chromosome compared to autosomes in derived strains, the dataset consisting of intergenic loci located far from genes shows very similar reductions of diversities for X-linked and autosomal loci in derived strains. In addition, levels of diversity at X-linked and autosomal loci in the presumably ancestral African population are more similar than expected under an assumption of neutrality and equal numbers of breeding males and females. Conclusion. We show that simple demographic scenarios under assumptions of neutral theory cannot explain all of the observed patterns of molecular diversity. We suggest that the simplest model is a population bottleneck that retains an ancestral female-biased sex ratio, coupled with higher rates of positive selection at X-linked loci in close proximity to genes specifically in derived, non-African populations.

Original languageEnglish (US)
Article number202
JournalBMC Evolutionary Biology
Volume7
DOIs
StatePublished - 2007
Externally publishedYes

Fingerprint

Drosophila melanogaster
Nucleotides
nucleotides
loci
gene
polymorphism
Population
population bottleneck
sex ratio
chromosome
breeding
Genes
Sex Ratio
X Chromosome
genes
autosomes
African Americans
Microsatellite Repeats
X chromosome
Drosophila

ASJC Scopus subject areas

  • Medicine(all)
  • Ecology, Evolution, Behavior and Systematics

Cite this

Similar levels of X-linked and autosomal nucleotide variation in African and non-African populations of Drosophila melanogaster. / Singh, Nadia D.; Macpherson, J. Michael; Jensen, Jeffrey; Petrov, Dmitri A.

In: BMC Evolutionary Biology, Vol. 7, 202, 2007.

Research output: Contribution to journalArticle

@article{1f5b012fc3b343b0ab43f541b0622e03,
title = "Similar levels of X-linked and autosomal nucleotide variation in African and non-African populations of Drosophila melanogaster",
abstract = "Background. Levels of molecular diversity in Drosophila have repeatedly been shown to be higher in ancestral, African populations than in derived, non-African populations. This pattern holds for both coding and noncoding regions for a variety of molecular markers including single nucleotide polymorphisms and microsatellites. Comparisons of X-linked and autosomal diversity have yielded results largely dependent on population of origin. Results. In an attempt to further elucidate patterns of sequence diversity in Drosophila melanogaster, we studied nucleotide variation at putatively nonfunctional X-linked and autosomal loci in sub-Saharan African and North American strains of D. melanogaster. We combine our experimental results with data from previous studies of molecular polymorphism in this species. We confirm that levels of diversity are consistently higher in African versus North American strains. The relative reduction of diversity for X-linked and autosomal loci in the derived, North American strains depends heavily on the studied loci. While the compiled dataset, comprised primarily of regions within or in close proximity to genes, shows a much more severe reduction of diversity on the X chromosome compared to autosomes in derived strains, the dataset consisting of intergenic loci located far from genes shows very similar reductions of diversities for X-linked and autosomal loci in derived strains. In addition, levels of diversity at X-linked and autosomal loci in the presumably ancestral African population are more similar than expected under an assumption of neutrality and equal numbers of breeding males and females. Conclusion. We show that simple demographic scenarios under assumptions of neutral theory cannot explain all of the observed patterns of molecular diversity. We suggest that the simplest model is a population bottleneck that retains an ancestral female-biased sex ratio, coupled with higher rates of positive selection at X-linked loci in close proximity to genes specifically in derived, non-African populations.",
author = "Singh, {Nadia D.} and Macpherson, {J. Michael} and Jeffrey Jensen and Petrov, {Dmitri A.}",
year = "2007",
doi = "10.1186/1471-2148-7-202",
language = "English (US)",
volume = "7",
journal = "BMC Evolutionary Biology",
issn = "1471-2148",
publisher = "BioMed Central",

}

TY - JOUR

T1 - Similar levels of X-linked and autosomal nucleotide variation in African and non-African populations of Drosophila melanogaster

AU - Singh, Nadia D.

AU - Macpherson, J. Michael

AU - Jensen, Jeffrey

AU - Petrov, Dmitri A.

PY - 2007

Y1 - 2007

N2 - Background. Levels of molecular diversity in Drosophila have repeatedly been shown to be higher in ancestral, African populations than in derived, non-African populations. This pattern holds for both coding and noncoding regions for a variety of molecular markers including single nucleotide polymorphisms and microsatellites. Comparisons of X-linked and autosomal diversity have yielded results largely dependent on population of origin. Results. In an attempt to further elucidate patterns of sequence diversity in Drosophila melanogaster, we studied nucleotide variation at putatively nonfunctional X-linked and autosomal loci in sub-Saharan African and North American strains of D. melanogaster. We combine our experimental results with data from previous studies of molecular polymorphism in this species. We confirm that levels of diversity are consistently higher in African versus North American strains. The relative reduction of diversity for X-linked and autosomal loci in the derived, North American strains depends heavily on the studied loci. While the compiled dataset, comprised primarily of regions within or in close proximity to genes, shows a much more severe reduction of diversity on the X chromosome compared to autosomes in derived strains, the dataset consisting of intergenic loci located far from genes shows very similar reductions of diversities for X-linked and autosomal loci in derived strains. In addition, levels of diversity at X-linked and autosomal loci in the presumably ancestral African population are more similar than expected under an assumption of neutrality and equal numbers of breeding males and females. Conclusion. We show that simple demographic scenarios under assumptions of neutral theory cannot explain all of the observed patterns of molecular diversity. We suggest that the simplest model is a population bottleneck that retains an ancestral female-biased sex ratio, coupled with higher rates of positive selection at X-linked loci in close proximity to genes specifically in derived, non-African populations.

AB - Background. Levels of molecular diversity in Drosophila have repeatedly been shown to be higher in ancestral, African populations than in derived, non-African populations. This pattern holds for both coding and noncoding regions for a variety of molecular markers including single nucleotide polymorphisms and microsatellites. Comparisons of X-linked and autosomal diversity have yielded results largely dependent on population of origin. Results. In an attempt to further elucidate patterns of sequence diversity in Drosophila melanogaster, we studied nucleotide variation at putatively nonfunctional X-linked and autosomal loci in sub-Saharan African and North American strains of D. melanogaster. We combine our experimental results with data from previous studies of molecular polymorphism in this species. We confirm that levels of diversity are consistently higher in African versus North American strains. The relative reduction of diversity for X-linked and autosomal loci in the derived, North American strains depends heavily on the studied loci. While the compiled dataset, comprised primarily of regions within or in close proximity to genes, shows a much more severe reduction of diversity on the X chromosome compared to autosomes in derived strains, the dataset consisting of intergenic loci located far from genes shows very similar reductions of diversities for X-linked and autosomal loci in derived strains. In addition, levels of diversity at X-linked and autosomal loci in the presumably ancestral African population are more similar than expected under an assumption of neutrality and equal numbers of breeding males and females. Conclusion. We show that simple demographic scenarios under assumptions of neutral theory cannot explain all of the observed patterns of molecular diversity. We suggest that the simplest model is a population bottleneck that retains an ancestral female-biased sex ratio, coupled with higher rates of positive selection at X-linked loci in close proximity to genes specifically in derived, non-African populations.

UR - http://www.scopus.com/inward/record.url?scp=37549020695&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=37549020695&partnerID=8YFLogxK

U2 - 10.1186/1471-2148-7-202

DO - 10.1186/1471-2148-7-202

M3 - Article

C2 - 17961244

AN - SCOPUS:37549020695

VL - 7

JO - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

SN - 1471-2148

M1 - 202

ER -