Ancestral polymorphisms explain the role of chromosomal inversions in speciation

Abstract

Understanding the role of chromosomal inversions in speciation is a fundamental problem in evolutionary genetics. Here, we perform a comprehensive reconstruction of the evolutionary histories of the chromosomal inversions in Drosophila persimilis and D. pseudoobscura. We provide a solution to the puzzling origins of the selfish Sex-Ratio arrangement in D. persimilis and uncover surprising patterns of phylogenetic discordance on this chromosome. These patterns show that, contrary to widely held views, all fixed chromosomal inversions between D. persimilis and D. pseudoobscura were already present in their ancestral population long before the species split. Our results suggest that patterns of higher genomic divergence and an association of reproductive isolation genes with chromosomal inversions may be a direct consequence of incomplete lineage sorting of ancestral polymorphisms. These findings force a reconsideration of the role of chromosomal inversions in speciation, not as protectors of existing hybrid incompatibilities, but as fertile grounds for their formation.

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.

Fig 4. The distribution of divergence estimated across genomic regions.

Divergence was estimated in 10 kb windows as the Relative Node Depth (RND; d_xy 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 2^nd 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 (3^PP) inversion arose before species divergence. Incomplete lineage sorting produced the observed inversion patterns in the species present today.

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.