The evolution and expression of Drosophila meiosis genes

Drosophila melanogaster is unique amongst model organisms in that males utilize achiasmatic meiosis, where formation of the synaptonemal complex (SC) and recombination are absent. Most organisms require the SC and chiasmata for the successful completion of meiosis and production of viable gametes, making D. melanogaster an ideal system for the study of meiotic variation. The goal of my research was to examine in detail the origin and evolution of male achiasmatic meiosis in Diptera. This was done in three parts: 1) assessing the presence and absence of meiosis genes across dipteran species, 2) analyzing the rate of evolution of Drosophila achiasmatic meiosis genes, and 3) evaluating differences in expression and splicing of meiosis genes between D. melanogaster males and females. I queried genome and transcriptome data from eleven dipteran species for both canonical and achiasmatic meiosis genes. Surprisingly, I found that a set of meiosis-specific genes was lost prior to the gain of Drosophila male achiasmy genes, suggesting that the latter were a later addition to an already non-canonical meiotic process. To assess the evolution of fourteen Drosophila achiasmatic meiosis genes, I performed phylogenetic, rate, selection and co-evolution analyses. My results show that, although these genes appear to be evolving under purifying selection, they are all evolving rapidly compared to their paralogs and paralogous genes throughout the Drosophila genome. Some groups of these genes are also co-evolving, supporting their potential for encoding members of protein complexes. These results suggest that male achiasmy is globally influencing the rapid evolution of these genes, even though their functions within meiosis vary greatly. Lastly, I investigated the expression and splicing of meiosis genes between male and female D. melanogaster. As expected, many meiosis genes with sex-limited roles showed biased expression for the sex that utilized them. However, some genes were expressed equally in both sexes or higher in the opposite sex. I also found evidence that sex-biased splicing may have a role in regulating protein production for some meiosis genes. These results indicate that the regulation of meiotic gene expression is more complex than originally thought and that multiple mechanisms, including alternative splicing, are utilized to control protein production. The combination of results from all parts of this work highlight some of the major events that occurred prior to and during the evolution of Drosophila male achiasmy and lay groundwork for future studies examining the details of this unusual evolutionary path.