The Evolution of Recombination Landscapes and Mechanisms in Drosophila in Light of Intragenomic Conflict

Abstract

Sex and recombination are ubiquitous across the vast majority of life on earth. In eukaryotes, recombination during meiosis yields new variation that selection acts upon and, thus, facilitates evolution. However, meiosis provides an arena for manipulation and exploitation by selfish genetic elements. Selfish elements can increase in abundance independently of their host organism and frequently at a cost to host fitness. Several types of selfish elements act during meiosis and therefore it is possible for recombination rates and mechanisms to evolve to counteract and ameliorate their negative effects. However, few studies have investigated the interaction between recombination and selfish genetic elements. I conducted three studies on the evolution of recombination mechanisms in light of the impact of selfish elements. I begin my thesis with an introduction on selfish elements, recombination, and their possible interactions in Chapter 1. In Chapter 2, I found evidence that the synaptonemal complex (SC), a protein complex necessary for proper meiotic recombination, is evolving rapidly in Drosophila due to positive selection. I proposed several hypotheses to explain the rapid evolution of the SC including the interaction between the SC and centromere-mediated meiotic drive. In the next two experiments, I utilized advances in DNA sequencing to genotype hundreds of Drosophila progeny to quantify recombination events. In Chapter 3, I demonstrate that recombination frequency and distribution is robust to transposable element activity in D. virilis. The only effect of increased transposable element activity that I discovered was found in rare cases of aberrant recombination events that occur prior to meiosis. In Chapter 4, I constructed the first complete genetic map for D. yakuba, a close relative of D. melanogaster. The genetic map and previous studies of recombination in species within the melanogaster subgroup suggest rapid evolution of recombination, especially in regards to the suppression of recombination near the centromere. My findings support theoretical work that suggests that centromere-mediated meiotic drive can result in the rapid evolution of recombination rates near centromeres. Further studies are needed to definitively prove the link between selfish genetic element behavior and meiotic recombination and how their interaction impacts the evolution of genes, genomes, and species.