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Abstract Numerous studies have revealed a signature of strong adaptive evolution in the piwi-interacting RNA (piRNA) machinery of Drosophila melanogaster, but the cause of this pattern is not understood. Several hypotheses have been proposed. One hypothesis is that transposable element (TE) families and the piRNA machinery are co-evolving under an evolutionary arms race, perhaps due to antagonism by TEs against the piRNA machinery. A related, though not co-evolutionary, hypothesis is that recurrent TE invasion drives the piRNA machinery to adapt to novel TE strategies. A third hypothesis is that ongoing fluctuation in TE abundance leads to adaptation in the piRNA machinery that must constantly adjust between sensitivity for detecting new elements and specificity to avoid the cost of off-target gene silencing. Rapid evolution of the piRNA machinery may also be driven independently of TEs, and instead from other functions such as the role of piRNAs in suppressing sex-chromosome meiotic drive. We sought to evaluate the impact of TE abundance on adaptive evolution of the piRNA machinery in D. melanogaster and 2 species with higher repeat content—Drosophila ananassae and Drosophila willistoni. This comparison was achieved by employing a likelihood-based hypothesis testing framework based on the McDonald–Kreitman test. We show that we can reject a faster rate of adaptive evolution in the piRNA machinery of these 2 species. We propose that the high rate of adaptation in D. melanogaster is either driven by a recent influx of TEs that have occurred during range expansion or selection on other functions of the piRNA machinery. 

Abstract Wolbachia are a genus of widespread bacterial endosymbionts in which some strains can hijack or manipulate arthropod host reproduction. Male killing is one such manipulation in which these maternally transmitted bacteria benefit surviving daughters in part by removing competition with the sons for scarce resources. Despite previous findings of interesting genome features of microbial sex ratio distorters, the population genomics of male-killers remain largely uncharacterized. Here, we uncover several unique features of the genome and population genomics of four Arizonan populations of a male-killing Wolbachia strain, wInn, that infects mushroom-feeding Drosophila innubila. We first compared the wInn genome with other closely related Wolbachia genomes of Drosophila hosts in terms of genome content and confirm that the wInn genome is largely similar in overall gene content to the wMel strain infecting D. melanogaster. However, it also contains many unique genes and repetitive genetic elements that indicate lateral gene transfers between wInn and non-Drosophila eukaryotes. We also find that, in line with literature precedent, genes in the Wolbachia prophage and Octomom regions are under positive selection. Of all the genes under positive selection, many also show evidence of recent horizontal transfer among Wolbachia symbiont genomes. These dynamics of selection and horizontal gene transfer across the genomes of several Wolbachia strains and diverse host species may be important underlying factors in Wolbachia’s success as a male-killer of divergent host species.