The Role of Oogenesis in Speciation

Project Summary All biodiversity on earth is generated through the process of speciation. While speciation research is focused on the origins of reproductive barriers between species, the results of this work will inform the study of infertility, an important reproductive health concern. Though gametogenesis is a logical developmental process

to study in regard to reproductive isolation, nearly all research focuses on male gametogenesis, with little to no work on oogenesis. The proposed research hypothesizes that environmental stress hastens the accumulation of genetic divergence through its impact on oogenesis, drawing connections between reproductive and

environmental health. For example, environmental stress has been shown to cause recurrent spontaneous abortion, making this work relevant to public health. There are four key outcomes of environmental stress on oogenesis – transposable elements, structural variants, meiotic recombination rates, and gene regulation –

that have been shown to be important to the study of speciation. By increasing genetic differences, oogenesis facilitates speciation between species that are differentially exposed. This proposal focuses primarily on recombination, while taking an important step towards integrating other outcomes. Previous research has

shown that recombination rates evolve more rapidly than nucleotide divergence. This coupled with evidence that recombination rates are environmentally sensitive, suggests that the environment could be a major driver of local adaptation through recombination. This proposal leverages the ease of experimental manipulation in

fruit flies to study the link between environmental sensitivity of oogenesis, the accumulation of novel genetic variation, and subsequent species divergence. First, within species oogenesis will be compared to hybrids under control and stress conditions investigating gene expression, chromatin conformation, organismal

measures of stress response, and recombination. By targeting molecular pathways associated with transposable element silencing and DNA repair, this work can indirectly inform the accumulation of these novel genetic variants, answering a key question in evolutionary biology regarding sources of intra- and inter-

species variation. Second, because differences in hybrid oogenesis could be attributed to reproductive incompatibilities impacting fitness, this work will investigate the relationship between fitness and recombination plasticity directly with three unique experimental stress treatments. Mutant markers will be used to compare

recombination, with the aid of a novel high-throughput phenotyping robot. Wild type stocks known to be either sensitive or tolerant to selected stressors will be targeted. A major innovation of this work will be to investigate organismal stress response directly to compare fitness across treatments. The data collected from these two

questions will be critical in the broader investigation of mechanisms of recombination rate plasticity, which remains a mystery even after a century of research in this area. In five years, the proposed work will answer crucial questions in speciation, while also filling a major gap of the importance of oogenesis in speciation.