CAREER: Drivers and impacts of repeated neo-sex chromosome evolution

In many animals and plants, the development of distinct sexes is driven by a set of specialized chromosomes called sex chromosomes. Sex chromosomes begin as a pair of identical autosomes but often evolve to become unrecognizable from each other and from the rest of the genome. Understanding how sex chromosomes evolve and the evolutionary forces that drive their evolution has been challenging because many model systems have sex chromosomes that are ancient. However, transitions can occur from old, degenerated sex chromosomes to neo-sex chromosomes that reset their trajectory and provide an opportunity to study the critical active stages of sex chromosome evolution. This project will leverage comparisons among multiple species with neo-sex chromosomes to investigate the evolutionary and molecular processes responsible for neo-sex chromosome evolution, and their consequences on genome function. This project will use advanced DNA and RNA sequencing technologies, cytogenetics, and bioinformatic methods to advance foundational knowledge in evolutionary genomics. This work will also integrate research and education by engaging undergraduate students and public audiences in learning and discovery at the interface of genetics/genomics, evolution, ecology, and data science, contributing to the development of the STEM workforce and to science literacy. Sex chromosomes originate from a pair of homologous autosomes but often evolve to become unrecognizable from each other and from the rest of the genome, as they follow distinct trajectories shaped by sex differences in selection and inheritance. Understanding the factors that shape sex chromosome evolution has been a major goal in evolutionary genetics, but a significant challenge in studying the key, initial stages of sex chromosome evolution has been the advanced age of sex chromosomes in many model systems. However, transitions can occur from old, degenerated sex chromosome systems to neo-sex chromosomes that reset this trajectory and provide an opportunity to study the critical active stages of sex chromosome evolution. Within treehoppers (hemipteran insects in the family Membracidae), multiple independent origins of neo-sex chromosomes have recently been discovered that span different stages from early to later sex chromosome evolution, creating an ideal comparative system. The proposed work leverages this interspecific variation through comparative studies of five neo-sex chromosome systems to (1) test the role of sexually antagonistic selection and genetic drift in the formation of neo-sex chromosomes, (2) investigate the timing and molecular basis of neo-Y chromosome degeneration and (3) assess if and how dosage compensation evolves on neo-sex chromosomes. These aims are designed to test unanswered questions arising from classic sex chromosome theory using the unique natural variation found in treehoppers. Pairing classic theory with current genomic and cytogenetic methods will generate new knowledge that elucidates the patterns and processes of sex chromosome and genome evolution. This work will also be used to develop hands-on learning experiences for undergraduates that integrate sex chromosome biology, evolution, genomics, and bioinformatics, training them in data-driven inquiry in biology. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.