Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution

Abstract

Drosophila mauritiana is an Indian Ocean island endemic species that diverged from its two sister species, Drosophila simulans and Drosophila sechellia, approximately 240,000 years ago. Multiple forms of incomplete reproductive isolation have evolved among these species, including sexual, gametic, ecological, and intrinsic postzygotic barriers, with crosses among all three species conforming to Haldane's rule: F(1) hybrid males are sterile and F(1) hybrid females are fertile. Extensive genetic resources and the fertility of hybrid females have made D. mauritiana, in particular, an important model for speciation genetics. Analyses between D. mauritiana and both of its siblings have shown that the X chromosome makes a disproportionate contribution to hybrid male sterility. But why the X plays a special role in the evolution of hybrid sterility in these, and other, species remains an unsolved problem. To complement functional genetic analyses, we have investigated the population genomics of D. mauritiana, giving special attention to differences between the X and the autosomes. We present a de novo genome assembly of D. mauritiana annotated with RNAseq data and a whole-genome analysis of polymorphism and divergence from ten individuals. Our analyses show that, relative to the autosomes, the X chromosome has reduced nucleotide diversity but elevated nucleotide divergence; an excess of recurrent adaptive evolution at its protein-coding genes; an excess of recent, strong selective sweeps; and a large excess of satellite DNA. Interestingly, one of two centimorgan-scale selective sweeps on the D. mauritiana X chromosome spans a region containing two sex-ratio meiotic drive elements and a high concentration of satellite DNA. Furthermore, genes with roles in reproduction and chromosome biology are enriched among genes that have histories of recurrent adaptive protein evolution. Together, these genome-wide analyses suggest that genetic conflict and frequent positive natural selection on the X chromosome have shaped the molecular evolutionary history of D. mauritiana, refining our understanding of the possible causes of the large X-effect in speciation.

Keywords: Drosophila; X chromosome; adaptation; genome; satellite DNA; selective sweep.

Fig. 1.—

Scans of population genetics statistics across the five major chromosomal arms of the D. mauritiana genome. The four statistics were calculated in nonoverlapping 10-kb windows. Each column of plots represents scans from a single chromosome arm. The top row of plots (blue points) shows scans of nucleotide diversity (π). The second row of plots (red points) shows the distribution of a likelihood ratio test statistic that measures the deviation of the local allele frequency spectrum (LR). The third row of plots (grey points) shows the measure of linkage disequilibrium (Z_nS) across all arms. Finally, the bottom row of plots (green points) shows the scan of average sequence divergence between the ten D. mauritiana samples and a single D. melanogaster genome sequence.

Fig. 2.—

Nucleotide diversity (π) across a large selective sweep on the X chromosome of D. mauritiana. The red rectangle in the inset above the graph delimits the region of reduced polymorphism on the X chromosome. Unfilled circles plot nucleotide diversity in 1-kb windows between positions X: 8,500,000–9,050,000. The red bars below the physical position of 1-kb windows represent the scaffolds constituting this region in the de novo assembly. Below the scaffolds are blue triangles that depict the gene models for a representative group of genes in the putative sweep regions (the names are from the homologous annotations in the D. melanogaster genome). The yellow squares mark the positions of 359-like satellite DNAs. Below the gene models are orange-filled triangles that show the positions of the markers used by True, Mercer, et al. (1996) and the observed intervening recombination distances. Finally, the green triangles give the locations of the two Winters sex-ratio meiotic drive genes in the D. simulans genome.

Fig. 3.—

A canonical selective sweep on the D. mauritiana X chromosome spans more than 140 kb. The red rectangle in the inset above the graph delimits the region of reduced polymorphism on the X chromosome. Unfilled circles plot nucleotide diversity (π) in 1-kb windows and the red line plots the expected π under a simple hard sweep model (see text). The red bars below the physical position of the 1-kb windows represent the scaffolds in the de novo assembly. Below the scaffolds are blue triangles showing the gene models. A 20-kb region of near-complete homozygosity contains four genes: wupA, CG32553, CG43133, and ari-1.

Fig. 4.—

Repeat content differs on the X and autosomes. In the top row, dot plots of the X chromosome and a representative autosomal arm (2R) show an enrichment of repetitive sequence on the X, which is organized into blocks of high repeat density. The bottom left panel shows the Percent repetitive sequence for the X chromosome compared with the average across the major autosomal arms. Finally, the bottom right panel shows the proportion of the different repeat classes in the highlighted repeat blocks on chromosomes X and 2R.