The evolution of Oskar function in insects

Abstract

The emergence of genetic novelty underlies major shifts in the evolution of development. In this thesis, I investigate evolution in primordial germ cell specification in insects, with a particular focus on the gene oskar. As a lineage-restricted, rapidly evolving gene with essential roles not only in the germ line, but also in the developing nervous system of some species, oskar presents a compelling case study of how genetic innovation drives phenotypic evolution. First, I synthesize observational and experimental data on the origin of primordial germ cells to describe how germ cell specification has evolved in insects, and more broadly across panarthropods. I also speculate on how evolution in germ line gene expression and function may drive shifts in the mechanisms of germ cell formation. Next, I specifically investigate evolution in oskar, which has undergone functionally significant sequence divergence over a short evolutionary timescale. I determine how protein-coding sequence differences between oskar orthologs from Drosophila melanogaster and D. virilis prevent the D. virilis ortholog from rescuing D. melanogaster oskar loss-of-function. I identify domains of the D. virilis Oskar protein that differentially impact localization of germ line and patterning determinants and dramatically influence downstream cell fate decisions. By leveraging this natural sequence variation as an evolution-guided mutagenesis strategy, I uncover new insights into the in vivo mechanisms of Oskar function. These experiments also reveal how oskar gene dosage affects germ plasm assembly and germ cell specification, shedding light on how embryos respond to changes not only in gene sequence but also quantity. Finally, I explore the potential co-option of oskar to different tissue contexts. I present preliminary data testing the hypothesis that oskar is expressed in the central nervous system of D. melanogaster, and I describe ongoing efforts to characterize oskar expression and function in other insect species. This broader comparative approach will eventually allow us to reconstruct the trajectory of oskar’s functional evolution across insects. I conclude by outlining promising directions for future research into the evolution of development, particularly through the lens of the genes that both influence and are influenced by these processes.