Transposable elements (TEs) are parasites that are found in the DNA of almost all organisms. They are considered to be selfish genetic elements because they use host machinery to make copies of themselves and then manage to get these copies pasted around the host's genome. Because TEs are transmitted from parent to offspring, they play an important role in genome evolution. They dramatically expand the size of genomes, rearrange DNA within and among chromosomes, and modify the activity of individual genes. However, TE infection also harms the host by mutating, disrupting, and disorganizing DNA. As a consequence, TE movement can cause host sterility and is associated with the onset and progression of multiple cancers. Teasing apart the mechanisms of TE regulation, therefore, is of fundamental importance for human health. Additionally, the fertility costs of TE infection presents a potential strategy for biological control of disease vectors, agricultural pests, and invasive species. However, we know virtually nothing about how TEs adapt or evolve within a host or how a host evolves in response to TE invasion. This research project takes advantage of a new TE invasion into an experimental line of fruit flies and allows for an unprecendented exploration into the evolutionary interactions between a transposable element and a host.
Despite the manifold impact of TEs on their hosts, our understanding of how the host-genome responds to infection remains extremely limited. This research will use the well-characterized historical invasion of the Drosophila melanogaster genome by the P-element DNA transposon as a model to examine the evolution of host repression. The recent occurrence of this invasion, as well as the preservation of ancestral genetic variation in laboratory strains, provides an unparalleled opportunity to examine host repression at the three most critical time points: just before invasion, during invasion, and just after invasion. It also provides the opportunity to deconstruct this evolutionary process in the laboratory and to interpret outcomes in natural populations. Specifically, this project will: 1) Characterize standing genetic variation in permissiveness of P-element transposition in a genetic model of the ancestral D. melanogaster population (just before invasion); 2) Define the mutational and selective processes that lead to the evolution of repression during invasion of experimental populations by transpositionally active P-elements; 3) Uncover the contributions of standing genetic variation, de novo mutation, and selection to the evolution of host repression in extant natural populations (just after invasion).
