Recent selection on the Y-to-dot translocation in Drosophila pseudoobscura

Abstract

The Drosophila pseudoobscura dot chromosome acquired genes from the ancestral Drosophila Y chromosome in a Y-to-dot translocation event that occurred between 12.7 and 20.8 Ma. The formerly Y-linked genes mostly retained their testis-specific expression but shrank drastically in size, mostly through intron reduction, since becoming part of the dot chromosome in this species. We investigated the impact of this translocation on the evolution of the both the Y-to-dot translocated region and the original segments of the dot chromosome in D. pseudoobscura. Our survey of polymorphism and divergence across the chromosome reveals a reduction in variation, a deletion polymorphism segregating at high frequency, and a shift in the frequency spectra, all consistent with a history of recent selective sweeps in the Y-to-dot translocated region but not on the rest of the dot chromosome. We do find evidence for recombination primarily as gene conversion on the dot chromosome; however, predicted recombination events are restricted to the part of the dot chromosome outside the translocation. It therefore appears that recombination has resulted in a degree of decoupling between the ancestral Y region and the conserved region of the dot chromosome.

Keywords: Y chromosome; dot chromosome; positive selection.

Fig. 1.

Reduced silent site diversity on the Drosophila pseudoobscura dot chromosome. Shown are the medians and interquartile ranges of π, θ_w, and divergence between D. pseudoobscura and D. miranda for the autosomes, the X chromosome, and the dot chromosome (outliers represented by open circles). The dot is further partitioned into the Y-to-dot translocated region and the conserved region of the dot, not involved in the translocation.

Fig. 2.

The relationship between LD (measured as r²) and distance between SNPs. The distance between SNPs and r² for the entire dot chromosome (open black circles, solid black line), just the conserved region of the dot chromosome (filled black circles, dotted black line), and just the Y-to-dot translocation (filled gray circles, dotted gray line). The negative Pearson’s product moment coefficient (r² = −0.119) is statistically significant for the entire dot chromosome (P = 0.0009), indicating that this chromosome has experienced recombination. This pattern appears to be driven by the conserved region of the dot chromosome (r² = −0.266, P = 0.0018).

Fig. 3.

Fit of the exponential growth model to Y-to-dot, dot (non-Y), and autosomal data. Barplot showing the fraction of loci (with S > 0) that reject the growth model (at FDR < 5%, or Q < 0.05) for π and D_Taj.

Fig. 4.

The marginal posterior distribution for the time since the last selective sweep (t_sweep) in 4N_e generations. We infer the time to the most recent selective sweep in an expanding population (see Materials and Methods) for the Y-to-dot region as 0.0578 (95% CI t_sweep 0.0118–1.881) 4N_e generations ago.