Sex chromosomes and speciation in Drosophila

Abstract

Two empirical rules suggest that sex chromosomes play a special role in speciation. The first is Haldane's rule - the preferential sterility and inviability of species hybrids of the heterogametic (XY) sex. The second is the disproportionately large effect of the X chromosome in genetic analyses of hybrid sterility. Whereas the causes of Haldane's rule are well established, the causes of the 'large X-effect' have remained controversial. New genetic analyses in Drosophila confirm that the X is a hotspot for hybrid male sterility factors, providing a proximate explanation for the large X-effect. Several other new findings -- on faster X evolution, X chromosome meiotic drive and the regulation of the X chromosome in the male-germline -- provide plausible evolutionary explanations for the large X-effect.

Figure 1. The large X-effect in Drosophila hybrids

The X chromosome has a conspicuously large effect on the sterility of backcross hybrid males between D. pseudoobscura (white) and D. persimilis (purple; modified from [79]). The x axis shows the percentage of fertile male flies obtained in the different chromosomal backcrosses that are depicted on the y axis. Similar results have been obtained in backcross analyses of hybrid sterility between many other species pairs, including Drosophila, mammals, Lepidoptera and birds (reviewed in [6]).

Figure 2. Introgression analyses of hybrid incompatibilities

Introgression studies move small chromosomal regions from one species (purple bars) into the genomic background of a closely related sister species (white bars) by repeated backcrossing through fertile hybrid females. Introgressed chromosomal segments typically bear a selectable dominant genetic marker (e.g., a P-element bearing the w⁺ eye color marker) and become progressively smaller with each generation of backcrossing. After several generations of backcrossing, the foreign introgression is made homozygous and tested for its effects on hybrid fitness.

Figure 3. The X chromosome is a hotspot for hybrid male sterility factors

The density of introgressions from D. mauritiana that cause hybrid male sterility (red triangles) in an otherwise D. sechellia genomic background is four times higher on the X chromosome than on chromosomes 2 and 3. A chromosomal inversion is bracketed by parentheses on chromosome arm 3R. Gray and black triangles mark fertile and hybrid lethal introgressions, respectively. Introgression sizes are depicted beneath the chromosomes (modified from [16]).