THE GENOMIC ARCHITECTURE OF REPRODUCTIVE SYSTEMS IN DROSOPHILA

Abstract

Reproduction is among the most dynamic and rapidly evolving genetic systems across sexual taxa. However, the evolutionary mechanisms that drive reproductive traits during the early stages of species divergence are relatively unknown. Using a systems-level, comparative functional genomics approach, I investigate the role of selection, drift, and genomic architecture in promoting the rapid divergence of reproductive systems in Drosophila. I develop a new comparative genomics database, flyDIVaS (Divergence and Selection in Drosophila), an updateable database for identifying patterns and processes involved in species conservation and divergence. I show that tissue-specific genes play a disproportionate role in driving species level divergence and, in particular, that genes specific to male reproductive tissue are among the most rapidly evolving. Using two deeply sequenced populations of Drosophila melanogaster, I reveal that adaptation is widespread among male-specific genes and identify local signatures of selection that have evolved in less than 500 years on sperm motility. In Drosophila mercatorum, a fruit fly capable of facultative parthenogenesis, I find recent signatures of protein changes involved with centrosomal and meiotic functions, and identify early genomic signatures of male degeneration. Among laboratory strains of Drosophila melanogaster, I identify adaptive signatures on neurogenic genes that have recently been domesticated during the last century . Finally, I explore the role of genomic architecture in shaping such reproductive functional systems by developing a novel hypothesis that rapid changes in behavior, such as those found in diverse mating preferences, is a function of the size of the neurogenome. The results presented in this dissertation point toward the importance of selection, drift, and genomic architecture in driving rapid functional change which, together, promote the generation of species diversity via the formation of reproductive barriers in early species divergence.