High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila

Abstract

Postzygotic reproductive isolation is characterized by two striking empirical patterns. The first is Haldane's rule—the preferential inviability or sterility of species hybrids of the heterogametic (XY) sex. The second is the so-called large X effect—substitution of one species's X chromosome for another's has a disproportionately large effect on hybrid fitness compared to similar substitution of an autosome. Although the first rule has been well-established, the second rule remains controversial. Here, we dissect the genetic causes of these two rules using a genome-wide introgression analysis of Drosophila mauritiana chromosome segments in an otherwise D. sechellia genetic background. We find that recessive hybrid incompatibilities outnumber dominant ones and that hybrid male steriles outnumber all other types of incompatibility, consistent with the dominance and faster-male theories of Haldane's rule, respectively. We also find that, although X-linked and autosomal introgressions are of similar size, most X-linked introgressions cause hybrid male sterility (60%) whereas few autosomal introgressions do (18%). Our results thus confirm the large X effect and identify its proximate cause: incompatibilities causing hybrid male sterility have a higher density on the X chromosome than on the autosomes. We evaluate several hypotheses for the evolutionary cause of this excess of X-linked hybrid male sterility.

Speciation through evolution of sex-linked genes

“…When two diverged populations hybridize, the drivers may escape the control of the suppressors and cause male sterility. Orr et al (2006) found that the same genes influence hybrid sex ratios and hybrid sterility in crosses between two Drosophila species, although Masly and Presgraves (2007) found no supporting evidence in another Drosophila study.…”

“…Studies of disproportionate X/Z effects that account for recessivity of hybrid dysfunction remain few and only for maleheterogametic taxa, but appear to support a large X effect for sterility (Table 1). True et al (1996), Tao et al (2003) and Masly and Presgraves (2007) have provided convincing evidence that male sterility factors in crosses between Drosophila simulans, D. mauritiana and D. sechellia occur at a higher density on the X chromosome than on autosomes and at a much higher density than female sterility factors, supporting faster male evolution. Their results also reveal an excess of recessive incompatibilities, supporting the dominance theory, but leave open the question of whether faster-X evolution is involved.…”

“…Their results also reveal an excess of recessive incompatibilities, supporting the dominance theory, but leave open the question of whether faster-X evolution is involved. Masly and Presgraves (2007) suggest that disruption of dosage compensation (transcription is normally increased on the X in male Drosophila to match that in females) or of X-inactivation during spermatogenesis are more likely mechanistic explanations for the large-X effect than faster-X evolution. However, despite previous studies providing no statistical support for faster-X evolution (Begun and Whitley, 2000;Betancourt et al, 2002;Thornton et al, 2006), Begun et al (2007) recently found strong evidence for faster-X in D. simulans, D. melanogaster and D. yakuba, which they suggest may be because of higher mutation rates on the X chromosome combined with more rapid adaptive divergence.…”

Higher levels of sex chromosome heteromorphism are associated with markedly stronger reproductive isolation

“…The second rule is named the large X-effect, and is based on observation that the X (or Z) chromosome has a disproportionately high impact on hybrid fitness compared to autosomes. This has been shown, in Drosophila, to be due to a higher density of male sterility factors in the X chromosome 6,7 .…”

“…The rate of this process is again dependent on the amount of degeneracy between sex chromosomes. Here I separate the large X-effect from the effects of dominance, where a large X-effect is caused by a higher density of incompatibilities accumulating on the X (Z) chromosome 6,7 , and not due to the fact that hemizygosity exposes incompatibilities in this chromosome (dominance theory). Of course, if the incompatibilities that stem from both faster X and/or faster-heterogametic-sex (which lead to the large X-effect) are on average partially recessive, we would observe an exaggerated pattern due to the combination of the large X-effect and the dominance theory 20 .…”