Recurrent and recent selection in the Drosophila melanogaster genome

Mutation, recombination, selection, and genetic drift shape patterns of genetic variation. Population geneticists traditionally investigate the contributions of these forces to sequence evolution without respect to the chromosomal context of the gene of interest, i.e., without respect to structural proteins and their corresponding dynamics characteristic of a particular chromosomal location. The ontogeny of this dissertation work begins with such a traditional approach and ends with a reconsideration. Chapter one describes five genes that evolved de novo along the D. melanogaster lineage or in the ancestor of D. melanogaster/D. simulans. These five genes are largely X-linked and expressed in a testis-biased pattern. Moreover, all de novo genes with homologous sequence in D. simulans exhibit an excess of amino acid divergence. Two previously described novel genes that evolved along the D. melanogaster lineage via shuffling of both functional and noncoding elements ( Sdic, hydra) also exhibit a pattern of adaptive protein evolution, and more surprisingly, share both a testis-biased expression pattern and a chromosomal location with one of the de novo genes identified in our study. The unexpected co-occurrence of these three genes at the base of the X chromosome raises the possibility that particular features of a chromosomal region may facilitate the evolution of novel genes. The insight that physical location potentially contributes to the likelihood of novel gene evolution and consequently, adaptive protein evolution, challenged me to consider how chromosome structure may influence evolutionary forces such as selection. A rigorous investigation of this research question requires within- and between-species sequence data examined in a context of comprehensive information about chromosome dynamics. At the inception of my dissertation work, our understanding of chromatin biology was still in its infancy. Consequently, I took a "surrogate approach" by investigating the role of selection in shaping patterns of polymorphism and divergence at proteins that remodel chromatin. I began by investigating protein divergence between sister species D. melanogaster and D. simulans, and discovered a surprising amount of adaptive protein evolution at those loci encoding the Dosage Compensation Complex (DCC) proteins along the D. melanogaster lineage. Next, I investigated chromatin remodeling factors within D. melanogaster , and found evidence of spatially varying selection at several. My final chapter is a first step towards understanding the functional consequences of natural variation at these proteins. Specifically, I describe preliminary evidence of stress tolerance variation associated with coding variation at the histone acetyltransferase, chameau. Documenting signatures of selection both within and between species at chromatin remodeling factors strongly implicate chromatin dynamics as an underappreciated biological function targeted by selection and motivates deeper and more direct investigations of the functional and evolutionary mechanisms driving evolution of chromatin dynamics.