Chromosome evolution and rapid Y chromosome degeneration

PROJECT SUMMARY Chromosomes are a fundamental structure necessary for the faithful transmission of genetic information. At the center of chromosome formation and segregation are centromeres, whose underlying DNA sequence often make up a surprisingly large portion of a genome. Often composed of repetitive satellite sequences, they are found to evolve and change quickly across species, likely due to selfish behavior. Along with centromeric changes in sequence and position, one of the most dramatic genomic changes that can occur is when a chromosome becomes involved in sex determination. Over time, sex chromosomes typically diverge dramatically in gene content, gene expression, transposable element content, and levels of genetic variation. These types of chromosomal changes can be the root of a surprising amount of variation, and we still have a poor understanding of how and why these changes occur. The proposed research is a comprehensive examination of chromosome evolution and genome structure in Drosophila, one of the most powerful and heavily studied systems in genetics. Using chromosome-scale genome assemblies coupled with genomics and bioinformatics-based approaches, this research will identify rapidly evolving centromeric satellite sequences across the group to better understand the tempo of satellite turnover and potential role in karyotypic changes. Additionally, comparative analyses will for the first time systematically identify genus-wide chromosome evolution and constraints on gene order and organization. The unique features of Drosophila – numerous species, small genomes, few chromosomes, ease of karyotyping – make a large-scale comparative analysis tracking the fates of centromeric satellite sequence and chromosome arms possible. The proposed research will also investigate a system with very young sex chromosomes where multiple Y types that vary in their gene content are likely responsible for the evolution of reproductive incompatibilities between populations. The proposed research will use a combination of whole genome sequencing and assembly of multiple divergent Y chromosomes, functional characterization of the diverging X and Y, and population genomic analyses, to link Y degeneration with restricted gene flow in natural populations. Together, these projects will take advantage of the unique attributes of two systems to understand the processes that lead to major changes in karyotype, and variation in degeneration and gene regulation of young sex chromosomes. More broadly, this research will provide a deeper understanding of the maintenance of, and variation in, chromosome structure and function that we see across the tree of life.