UC Davis

Gene expression evolution leads to much of the diversity observed among species. Expressiondivergence may be driven by regulatory evolution in cis loci and trans factors. Additionally, regulatory evolution may lead to hybrid incompatibilities in the form of misexpression linked to sterility. Many studies have shown that expression divergence varies widely among tissues, and male gonadal tissues tend to evolve particularly rapidly. There has been less work on somatic male reproductive tissues, and little work on the evolutionary properties of different cell types. Additionally, our understanding of how gene regulatory evolution and hybrid misexpression vary among tissues is especially limited. In this study I use the Drosophila male accessory gland and ejaculatory duct—organs that produce seminal fluid—as a for evolution of expression and regulation in cells and tissues. In Chapter I, I used single-nucleus RNA-Seq of the accessory gland and ejaculatory duct three Drosophila species to comprehensively describe the cell diversity of these tissues for the first time. I found that rates of transcriptome divergence were heterogenous among cell types and lineages, with ejaculatory duct cells evolving faster than the cells of the accessory gland. I also found that proteins characteristic of each cell type have variable rates of adaptive substitutions. In Chapter II, I used allele-specific expression in accessory glands and ejaculatory ducts of hybrids between D. melanogaster and D. simulans to estimate regulatory changes in cis and trans and quantify hybrid misexpression. I found an unexpected excess of trans-regulatory divergence in contrast to the prevailing expectation in the literature. I also found that the accessory gland has limited misexpression, potentially indicative of less hybrid dysgenesis in comparison to gonads. I integrated ATAC-Seq and RNA-Seq data to show that differences in chromatin accessibility correlate with divergence in both cis and trans. Taken together, these studies contribute to our knowledge of the unique evolution of the accessory gland and ejaculatory duct and underline the importance of tissue- and cell-type specific differences in expression and regulatory divergence.