Evolution of Drosophila buzzatii wings: Modular genetic organization, sex-biased integrative selection and intralocus sexual conflict

The Drosophila wing is a structure shared by males and females with the main function of flight. However, in males, wings are also used to produce songs, or visual displays during courtship. Thus, observed changes in wing phenotype depend on the interaction between sex-specific selective pressures and the genetic and ontogenetic restrictions imposed by a common genetic architecture. Here, we investigate these issues by studying how the wing has evolved in twelve populations of Drosophila buzzatii raised in common-garden conditions and using an isofemale line design. The between-population divergence shows that sexual dimorphism is greater when sex evolves in different directions. Multivariate Qst-Fst analyses confirm that male wing shape is the target for multiple selective pressures, leading males' wings to diverge more than females' wings. While the wing blade and the wing base appear to be valid modules at the genetic (G matrix) and among-population (D matrix) levels, the reconstruction of between-population adaptive landscapes (Ω matrix) shows selection as an integrative force. Also, cross-sex covariances reduced the predicted response to selection in the direction of the extant sexual dimorphism, suggesting that selection had to be intensified in order to circumvent the limitations imposed by G. However, such intensity of selection was not able to break the modularity pattern of the wing. The results obtained here show that the evolution of D. buzzatii wing shape is the product of a complex interplay between ontogenetic constraints and conflicting sexual and natural selections.

Drosophila Interspecific Hybridization Causes a Deregulation of the piRNA Pathway Genes

Almost all eukaryotes have transposable elements (TEs) against which they have developed defense mechanisms. In the Drosophila germline, the main transposable element (TE) regulation pathway is mediated by specific Piwi-interacting small RNAs (piRNAs). Nonetheless, for unknown reasons, TEs sometimes escape cellular control during interspecific hybridization processes. Because the piRNA pathway genes are involved in piRNA biogenesis and TE control, we sequenced and characterized nine key genes from this pathway in Drosophila buzzatii and Drosophila koepferae species and studied their expression pattern in ovaries of both species and their F1 hybrids. We found that gene structure is, in general, maintained between both species and that two genes—armitage and aubergine—are under positive selection. Three genes—krimper, methyltransferase 2, and zucchini—displayed higher expression values in hybrids than both parental species, while others had RNA levels similar to the parental species with the highest expression. This suggests that the overexpression of some piRNA pathway genes can be a primary response to hybrid stress. Therefore, these results reinforce the hypothesis that TE deregulation may be due to the protein incompatibility caused by the rapid evolution of these genes, leading to a TE silencing failure, rather than to an underexpression of piRNA pathway genes.

What does mitogenomics tell us about the evolutionary history of the Drosophila buzzatii cluster (repleta group)

The Drosophila repleta group is an array of more than 100 cactophilic species endemic to the “New World”. The acquisition of the ability to utilize decaying cactus tissues as breeding and feeding sites is a key aspect that allowed the successful diversification of the repleta group in the American deserts. Within this group, the Drosophila buzzatii cluster is a South American clade of seven cactophilic closely related species in different stages of divergence, a feature that makes it a valuable model system for evolutionary research. However, even though substantial effort has been devoted to elucidating the phylogenetic relationships among members of the D. buzzatii cluster, the issue is still controversial. In effect, molecular phylogenetic studies performed to date generated ambiguous results since tree topologies depend on the kind of molecular marker employed. Curiously, even though mitochondrial DNA has become a popular marker in evolutionary biology and population genetics, none of the more than twenty Drosophila mitogenomes assembled so far belongs to this cluster. In this work we report the assembly of six complete mitogenomes of five species: D. antonietae, D. borborema, D. buzzatii, D. seriema and two strains of D. koepferae, with the aim to revisit the phylogenetic relationships and divergence times by means of a mitogenomic approach. The recovered topology using complete mitogenomes gives support to the hypothesis of the monophyly of that the D. buzzatii cluster and shows two main clades, one including D. buzzatii and D. koepferae (both strains) and the other the remaining species. These results are in agreement with previous reports based on a few mitochondrial and/or nuclear genes but in conflict with the results of a recent large-scale nuclear phylogeny, suggesting that nuclear and mitochondrial genomes depict different evolutionary histories.