The homeodomain is a DNA binding motif that is usually conserved among diverse taxa. Rapidly evolving homeodomains are thus of interest because their divergence may be associated with speciation. The exact site of the Odysseus (Ods) locus of hybrid male sterility in Drosophila contains such a homeobox gene. In the past half million years, this homeodomain has experienced more amino acid substitutions than it did in the preceding 700 million years; during this period, it has also evolved faster than other parts of the protein or even the introns. Such rapid sequence divergence is driven by positive selection and may contribute to reproductive isolation.

It is generally believed that Drosophila melanogaster has no closely related species with which it can produce the viable and fertile hybrids that are essential for the genetic analysis of speciation. Following the recent report of molecular differentiation between a Zimbabwe, Africa, population and two United States populations, we provide evidence that strong sexual isolation exists between the D. melanogaster population in Zimbabwe and populations of other continents. In the presence of males of their own kind, females from most isofemale lines of Zimbabwe would not mate with males from elsewhere; the reciprocal mating is also significantly reduced, but to a lesser degree. The genes for sexual behaviors are apparently polymorphic in Zimbabwe and postmating reproductive isolation between this and other populations has not yet evolved. Whole chromosome substitutions indicate significant genetic contributions to male mating success by both major autosomes, whereas the X chromosome effect is too weak to measure. In addition, the relative mating success between hybrid and pure line males supports the interpretation of strong female choice. These observations suggest that we are seeing the early stages of speciation in this group and that it is driven by sexual selection. The genetic and molecular tractability of D. melanogaster offers great promise for the detailed analysis of this apparent case of incipient speciation.The difficulties in studying the genetics of speciation can arise from several sources. First, the species in question may have diverged beyond the incipient stage. Many genetic differences between them could have accumulated after speciation had been completed and the information on the population genetic dynamics of speciation may have been lost. Ideally, we would like to observe variation in genes of reproductive isolation that are still in the process of becoming fixed. Polymorphisms of such genes within species would suggest speciation inflagrante delicto (1). The second difficulty arises when the species of interest does not lend itself to extensive and detailed genetic analysis. The conspicuous absence of a species that could hybridize with Drosophila melanogaster to produce fertile progeny is the prime example of the second point. To some degree, all studies of the genetics of postmating reproductive isolation encounter the two problems (2). Genetic analysis of premating sexual isolation also confronts a third difficulty in that mating behaviors are often labile (3-8). Finding a system of sexual isolation associated with robust behavioral phenotypes is thus crucial for genetic studies of premating isolation.Recently, a collection of isofemale lines of D. melanogaster from Zimbabwe, Africa, was reported to show a surprisingly high level of DNA sequence divergence at several nuclear genes compared to flies from North American populations (9). In light of previous observations that flies of this species collected over a wide geographical range are very similar in their nuclear DNA polym...

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The collection of Drosophila melanogaster from Zimbabwe and nearby regions (the Z-type) yield females who would not mate with the cosmopolitan D. melanogaster males (the M-type). To dissect the genetic basis of this sexual isolation, we constructed 16 whole-chromosome substitution lines between two standard Z- and M-lines. The results were as follows: (1) All substitution lines appear normal in viability and fertility in both sexes, indicating no strong postmating isolation. (2) The genes for the behaviors are mapped to all three major chromosomes with the same ranking and comparable magnitude of effects for both sexes: III > II ⪢ X ≥ 0 (III, II and X designate the effects of the three chromosomes). The results suggest less evolution on the X than on autosomes at loci of sexual behavior. (3) The genes for “Z-maleness” are many and somewhat redundant. Whole-chromosome effects for Z-maleness appear nearly additive and show little dominance. (4) In contrast, “Z-femaleness” has less redundancy as partial genotypes never exhibit full phenotypic effects. Epistatic interactions and incomplete dominance can sometimes be detected. (5) The extensive genetic divergence underlying sexual isolation has evolved in the absence of detectable reduction in hybrid fitnesses. Sexual selection has apparently been a driving force of multiple facets of speciation at the nascent stage without reinforcement.

It is commonly assumed but not proven that microRNAs (miRNAs) and their targets coevolve. Under this assumption, miRNAs and targets from different species may interact adversely, resulting in reduced fitness. However, the strength of the adverse interactions may not be detectable because even outright deletions of miRNAs often manifest only subtle fitness effects. We tested and measured the strength of heterospecific interactions by carrying out transgenic experiments across Drosophila species by overexpressing the miR310s cluster of Drosophila melanogaster (Dm310s) and Drosophila pseudoobscura (Dp310s) in D. melanogaster. Flies overexpressing the heterospecific Dp310s are only one-third as viable as those overexpressing the conspecific Dm310s. The viability effect is easily detectable in comparison to the effect of the deletion of miR310s. The number of genes significantly misexpressed under the influence of Dp310s is 3-10 times greater than under Dm310s. Importantly, the numbers of predicted targets are similar between them. Expression analysis of the predicted target genes suggests that miRNAs may sometimes function to buffer fluctuations in the transcriptome output. After the buffering function has evolved, heterospecific combinations may cause adverse effects.oevolution is a central topic in evolutionary biology. Good examples of phenotypic coevolution abound, but coevolution at the molecular level has been observed only in limited contexts. Genic coevolution can be the molecular basis of the MullerDobzhansky (MD) model of hybrid incompatibility (1, 2). In the simplest two-locus MD model, the ancestral A0 and B0 alleles at loci A and B, respectively, evolved to A1B1 in species 1 and A2B2 in species 2. In each lineage, the two genes coevolve such that alleles at the two loci are always compatible. However, alleles A1 and B2 or B1 and A2 may not be compatible because they have never coexisted and coevolved in the same species. Interspecific hybridization brings them together, causing hybrid breakdown.