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.

Figure 1

Frequency distribution of observed nucleotide diversity across loci in a) Singh et al. 16 X-linked and autosomal loci from African strains, b) Singh et al. 16 X-linked and autosomal loci from North American strains c) compiled data from X-linked and autosomal loci for African strains and d) compiled data from X-linked and autosomal loci for African strains.

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.