Fig 1.
The D. persimilis Sex-Ratio (SR) chromosome is precisely collinear with D. pseudoobscura.
(A) The right arm of the X chromosome (XR) of D. persimilis is normally inverted as compared to its sister species, D. pseudoobscura, but the D. persimilis Sex-Ratio chromosome is collinear with its sister species. (B) Polytene chromosome squash of a D. persimilis SR/D. pseudoobscura hybrid female demonstrating perfect interspecies collinearity on XR. (C) Amplification and sequencing of the proximal breakpoint of the D. persimilis inversion reveals that the breakpoints are collinear at the base-pair level.
Fig 2.
The inversion breakpoints on XR show extensive phylogenetic discordance.
(A) Sliding window phylogeny classification on XR. Blue, grey, and orange vertical lines represent the tree topology supported by neighbor-joining trees. Grey trees represent no phylogenetic discordance. Blue trees represent regions where the two collinear chromosomes appear more similar. Large regions centered on the proximal and distal breakpoints (dashed lines) of the XR inversion show discordant clustering of D. persimilis SR with D. pseudoobscura rather than D. persimilis ST. (B) Large regions of phylogenetic discordance are not observed in the remainder of the genome.
Fig 3.
Discordance may be produced by introgression or incomplete lineage sorting of the XR arrangements.
Under model (A), the D. persimilis ST inversion segregates in the ancestral population of the species. Later divergence between D. persimilis SR and D. pseudoobscura chromosomes and recombination restriction between the two D. persimilis chromosomes leads to phylogenetic discordance at the inversion breakpoints. (B) An introgression model again predicts discordance if the D. persimilis SR chromosome introgressed from D. pseudoobscura after species divergence. Recombination between the introgressed chromosome and D. persimilis ST will gradually homogenize the two chromosomes excluding the inversion breakpoints.
Table 1.
Estimates of the relative ages of chromosomal inversions in D. persimilis and D. pseudoobscura relative to species divergence time.
The fixed inversions on the XL and 2nd chromosomes, as well as the polymorphic inversions on XR and the Pikes Peak (3PP) inversion arose before species divergence.
Fig 4.
The distribution of divergence estimated across genomic regions.
Divergence was estimated in 10 kb windows as the Relative Node Depth (RND; dxy normalized to the outgroup) across the genome. The boxplots show the distribution of RND for each comparison in all collinear regions, and across the XR, XL and 2nd chromosome inversions. The horizontal lines depicted in the three fixed inversions indicate the mean RND estimated in the regions flanking the inversion breakpoints (±250 kb) for D. pseudoobscura-D. persimilis ST (solid) and D. pseudoobscura-D. persimilis SR (dashed).
Fig 5.
Incomplete lineage sorting of the inversions of D. persimilis and D. pseudoobscura.
The fixed inversions on the XL and 2nd chromosomes, as well as the polymorphic inversions on XR and the Pikes Peak (3PP) inversion arose before species divergence. Incomplete lineage sorting produced the observed inversion patterns in the species present today.
Table 2.
Maximum likelihood support and likelihood ratio tests for gene flow under models of speciation.
The log-likelihoods are displayed for isolation (Iso), isolation-with-migration (IM), and isolation-with-initial-migration (IIM) models. The estimates in bold correspond to the maximum likelihoods for each genomic region. In each case, the IIM model has the best support. The columns labeled Iso and IM show the likelihood ratio test statistics for each model relative to the IIM model.
Fig 6.
Inversions accelerate the formation of hybrid incompatibilities.
(A) Polymorphic inversions arise in the ancestor of the two species. (B) Restricted recombination between the inversions leads to accumulating divergence (red, blue) distinct from collinear regions of the genome (grey). (C) Incomplete sorting of the inversions between two isolated populations generates immediate divergence between the two populations. (D) Preexisting divergence increases the chance of hybrid incompatibilities forming in the inverted regions as compared to the collinear regions.