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

Singh ND, Macpherson JM, Jensen JD, Petrov DA - BMC Evol. Biol. (2007)

Bottom Line: We combine our experimental results with data from previous studies of molecular polymorphism in this species.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, Stanford University, Stanford, CA 94305 USA. nds25@cornell.edu

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.

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Mean diversities for X-linked and autosomal loci in African and non-African populations of D. melanogaster, comparing the Singh et al. dataset with the compiled dataset.
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Figure 2: Mean diversities for X-linked and autosomal loci in African and non-African populations of D. melanogaster, comparing the Singh et al. dataset with the compiled dataset.

Mentions: Nucleotide polymorphism can also be compared between X-linked and autosomal loci. Average levels of nucleotide polymorphism uncorrected for sequence divergence were 13.28 × 10-3 (95% confidence interval 11.73 × 10-3–14.82 × 10-3) and 13.10 × 10-3 (11.59 × 10-3–14.62 × 10-3) (Table 1) for autosomal and X-linked loci when all strains were grouped together. When African and non-African populations were considered separately, X-linked loci and autosomal loci also show similar levels of diversity per site (Figure 2, Table 1). There was no significant difference in estimated polymorphism between X-linked and autosomal loci, either when both populations were considered together or separately (P = 0.94, P = 0.83, and P = 0.46 for both populations, African strains only, and American strains only, respectively, Mann-Whitney U-test). Using these estimates of nucleotide diversity to infer the ratio of X-linked to autosomal variation yielded mean ratios greater than the expected 3/4 under a model of equal numbers of breeding males and females. These ratios were estimated as 0.99 (0.83–1.17), 0.99 (0.81–1.20), and 0.92 (0.68–1.21) for both populations together, African strains, and North American strains, respectively (Table 2). These confidence intervals indicate that we can reject the expected 3/4 ratio of X to autosomal levels of variation for the African population data and for the combined populations.


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

Singh ND, Macpherson JM, Jensen JD, Petrov DA - BMC Evol. Biol. (2007)

Mean diversities for X-linked and autosomal loci in African and non-African populations of D. melanogaster, comparing the Singh et al. dataset with the compiled dataset.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2164965&req=5

Figure 2: Mean diversities for X-linked and autosomal loci in African and non-African populations of D. melanogaster, comparing the Singh et al. dataset with the compiled dataset.
Mentions: Nucleotide polymorphism can also be compared between X-linked and autosomal loci. Average levels of nucleotide polymorphism uncorrected for sequence divergence were 13.28 × 10-3 (95% confidence interval 11.73 × 10-3–14.82 × 10-3) and 13.10 × 10-3 (11.59 × 10-3–14.62 × 10-3) (Table 1) for autosomal and X-linked loci when all strains were grouped together. When African and non-African populations were considered separately, X-linked loci and autosomal loci also show similar levels of diversity per site (Figure 2, Table 1). There was no significant difference in estimated polymorphism between X-linked and autosomal loci, either when both populations were considered together or separately (P = 0.94, P = 0.83, and P = 0.46 for both populations, African strains only, and American strains only, respectively, Mann-Whitney U-test). Using these estimates of nucleotide diversity to infer the ratio of X-linked to autosomal variation yielded mean ratios greater than the expected 3/4 under a model of equal numbers of breeding males and females. These ratios were estimated as 0.99 (0.83–1.17), 0.99 (0.81–1.20), and 0.92 (0.68–1.21) for both populations together, African strains, and North American strains, respectively (Table 2). These confidence intervals indicate that we can reject the expected 3/4 ratio of X to autosomal levels of variation for the African population data and for the combined populations.

Bottom Line: We combine our experimental results with data from previous studies of molecular polymorphism in this species.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, Stanford University, Stanford, CA 94305 USA. nds25@cornell.edu

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.

Show MeSH