Chromosomal inversions and the reproductive isolation of species

Abstract

Recent genetic studies have suggested that many genes contribute to differences between closely related species that prevent gene exchange, particularly hybrid male sterility and female species preferences. We have examined the genetic basis of hybrid sterility and female species preferences in Drosophila pseudoobscura and Drosophila persimilis, two occasionally hybridizing North American species. Contrary to findings in other species groups, very few regions of the genome were associated with these characters, and these regions are associated also with fixed arrangement differences (inversions) between these species. From our results, we propose a preliminary genic model whereby inversions may contribute to the speciation process, thereby explaining the abundance of arrangement differences between closely related species that co-occur geographically. We suggest that inversions create linkage groups that cause sterility to persist between hybridizing taxa. The maintenance of this sterility allows the species to persist in the face of gene flow longer than without such inversions, and natural selection will have a greater opportunity to decrease the frequency of interspecies matings.

Figure 1

Recombinational distances (in Kosambi centimorgans) between genetic markers in hybrids of D. pseudoobscura and D. persimilis. The circles indicate positions of large inversions that differentiate the strains used. Also indicated are positions of genomic segments introgressed from D. persimilis into D. pseudoobscura (bars right of the chromosomes) and the positions of loci associated with species discrimination by backcross females (asterisks right of the chromosomes).

Figure 2

Model for the long term effect of inversions on introgression and species persistence with hybridization. Two species are designated by diploid chromosomes of a single color (black or white) at the top of the figure. Horizontal lines indicate the locations of alleles that confer hybrid sterility in a heterospecific genetic background. The oval indicates an inverted gene arrangement relative to the other species. (A) No inversion difference between species. (B) One inversion differentiates the species.