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.

Sex ratio distortion (sex-ratio for short) has been reported in numerous species such as Drosophila, where distortion can readily be detected in experimental crosses, but the molecular mechanisms remain elusive. Here we characterize an autosomal sex-ratio suppressor from D. simulans that we designate as not much yang (nmy, polytene chromosome position 87F3). Nmy suppresses an X-linked sex-ratio distorter, contains a pair of near-perfect inverted repeats of 345 bp, and evidently originated through retrotransposition from the distorter itself. The suppression is likely mediated by sequence homology between the suppressor and distorter. The strength of sex-ratio is greatly enhanced by lower temperature. This temperature sensitivity was used to assign the sex-ratio etiology to the maturation process of the Y-bearing sperm, a hypothesis corroborated by both light microscope observations and ultrastructural studies. It has long been suggested that an X-linked sex-ratio distorter can evolve by exploiting loopholes in the meiotic machinery for its own transmission advantage, which may be offset by other changes in the genome that control the selfish distorter. Data obtained in this study help to understand this evolutionary mechanism in molecular detail and provide insight regarding its evolutionary impact on genomic architecture and speciation.

Many evolutionary studies use comparisons across species to detect evidence of natural selection and to examine the rate of character evolution. Statistical analyses in these studies are usually performed by means of a species phylogeny to accommodate the effects of shared evolutionary history. The phylogeny is usually treated as known without error; this assumption is problematic because inferred phylogenies are subject to both stochastic and systematic errors. We describe methods for accommodating phylogenetic uncertainty in evolutionary studies by means of Bayesian inference. The methods are computationally intensive but general enough to be applied in most comparative evolutionary studies.

The divergent genital morphology observed among closely related animal species has long been posited as a mechanism of reproductive isolation. Despite the intuitive appeal that rapidly evolving genitalia might cause speciation, evidence for its importance—or even its potential—in reproductive isolation is mixed. Most tests of genital structural isolation between species often fail to find convincing evidence that differences in morphology prevent copulation or insemination between species. However, recent work suggests that differences in genital morphology might contribute to reproductive isolation in less obvious ways through interactions with sensory mechanisms that result in lowered reproductive fitness in heterospecific matings. In this paper, I present a brief history of the “lock-and-key” hypothesis, summarize the evidence for the involvement of genital morphology in different mechanisms of reproductive isolation, discuss progress in identifying the molecular and genetic bases of species differences in genital morphology, and discuss prospects for future work on the role of genitalia in speciation. L'armure copulatrice est un organe ou mieux un instrument ingénieusement compliqué, destiné à s'adapter aux parties sexuelles externes de la femelle pour l'accomplissement de l'acte copulatif; elle est la garantie de la conservation des types, la sauvegarde de la légitimité de l'espèce. [The copulation armor is an organ or better an instrument ingeniously complicated, destined to adapt to sexual parts external to the female for the completion of copulation; it is the guarantee of the preservation of the standards, the safeguard of the legitimacy of the species.] L. Dufour, 1844

We describe reproductive isolation caused by a gene transposition. In certain Drosophila melanogaster-D. simulans hybrids, hybrid male sterility is caused by the lack of a single-copy gene essential for male fertility, JYAlpha. This gene is located on the fourth chromosome of D. melanogaster but on the third chromosome of D. simulans. Genomic and molecular analyses show that JYAlpha transposed to the third chromosome during the evolutionary history of the D. simulans lineage. Because of this transposition, a fraction of hybrids completely lack JYAlpha and are sterile, representing reproductive isolation without sequence evolution.