Evaluation of the genomic extent of effects of fixed inversion differences on intraspecific variation and interspecific gene flow in Drosophila pseudoobscura and D. persimilis

Abstract

There is increasing evidence that chromosomal inversions may facilitate the formation or persistence of new species by allowing genetic factors conferring species-specific adaptations or reproductive isolation to be inherited together and by reducing or eliminating introgression. However, the genomic domain of influence of the inverted regions on introgression has not been carefully studied. Here, we present a detailed study on the consequences that distance from inversion breakpoints has had on the inferred level of gene flow and divergence between Drosophila pseudoobscura and D. persimilis. We identified the locations of the inversion breakpoints distinguishing D. pseudoobscura and D. persimilis in chromosomes 2, XR, and XL. Population genetic data were collected at specific distances from the inversion breakpoints of the second chromosome and at two loci inside the XR and XL inverted regions. For loci outside the inverted regions, we found that distance from the nearest inversion breakpoint had a significant effect on several measures of divergence and gene flow between D. pseudoobscura and D. persimilis. The data fitted a logarithmic relationship, showing that the suppression of crossovers in inversion heterozygotes also extends to loci located outside the inversion but close to it (within 1-2 Mb). Further, we detected a significant reduction in nucleotide variation inside the inverted second chromosome region of D. persimilis and near one breakpoint, consistent with a scenario in which this inversion arose and was fixed in this species by natural selection.

Figure 1.—

Plot of nucleotide variation (θ) vs. chromosome location for the 18 second chromosome loci of the three species included in this study. The location of the inverted region is indicated.

Figure 2.—

Plot of percentage of fixed differences vs. distance to inversion for the group of second chromosome markers outside the inversion (A) or inside the inversion (B).

Figure 3.—

Plot of migration rate (Nm) vs. distance to inversion for the group of second chromosome markers outside the inversion (A) or inside the inversion (B). In this plot, marker 2M06 is not included (see text).

Figure 4.—

Plot of relative node depth (RND) vs. distance to inversion for the group of second chromosome markers outside the inversion (A) or inside the inversion (B).

Figure 5.—

NJ tree of X_2102 (chromosome XR) showing the genealogy of the regular and sex-ratio D. persimilis sequences. Individuals with the prefix “ps” are D. pseudoobscura, and those with prefix “bog” are D. p. bogotana. Numbers associated with branches represent bootstrap values >65% based on 500 pseudoreplications. Midpoint rooting was used to place the outgroup.

Figure 6.—

NJ trees of 3 second chromosome loci (A–C) and one XL locus (D) showing three different patterns of phylogenetic association. Individuals with the prefix “ps” are D. pseudoobscura, those with prefix “per” are D. persimilis, those with prefix “bog” are D. p. bogotana, and those with prefix “mir” are D. miranda. Numbers associated with branches represent bootstrap values >65% based on 500 pseudoreplications. (A) 2M12; (B) 2M06; (C) 2M17.3; (D) X_2105. Midpoint rooting was used to place the outgroup in all trees.