Genomic analysis of inbreeding, DNA methylation and sexual trait expression in a lekking bird

• Applicant: Professor Dr. Joseph Hoffman
• Subject Area: Evolution, Anthropology ; Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
• Term: since 2020
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 454606304

Since Darwin first coined the term “sexual selection” to explain the evolution of exaggerated male traits, we have come to understand the complex interrelationships among these traits, the information they encode and the life histories of the animals they are embedded into. Sexual selection is built on the idea that individual quality is signaled by the expression of these traits, yet a clear mechanistic understanding of the genetic architectures of sexual traits and the mechanisms regulating sexual trait expression remains elusive.We know that inbreeding is an important component of individual quality, and several studies have documented inbreeding depression for sexually-selected traits. Moreover, trait expression can be influenced by dynamic factors such as age and environmental variation, so epigenetic control mediated by body condition has been proposed as a means of regulating genotype-dependent sexual trait expression. Resolving long-standing evolutionary questions about mate choice and sexual selection therefore requires a fundamental understanding of the genetic and epigenetic basis of sexual traits.We will combine the genomic inference of inbreeding with genome-wide methylation analysis to investigate the genetic and epigenetic mechanisms affecting sexual trait expression and reproductive success in a classical lek model system, the black grouse. First, we will use precise genomic estimates of inbreeding to quantify the magnitude of inbreeding depression for multiple sexual traits. From there, we will use structural equation modeling to integrate potential pathways linking inbreeding-dependent sexual trait expression to variation in reproductive success.To shed light on the genetic architectures of sexual traits, we will quantify the contribution of different genomic regions to inbreeding depression. We will evaluate support for the ‘genic capture’ hypothesis, which posits that sexual traits are influenced by the cumulative effects of large numbers of loci distributed across the genome. Alternatively, localized genomic regions could be disproportionately important, e.g. gene pathways linked to immunity or metabolism.Finally, we will build upon a recent pilot study linking heterozygosity to sexual trait expression via differential methylation by using a cost-effective genome-wide assay, epi-GBS, to identify genome-wide epigenetic signatures associated with inbreeding and male sexual trait expression. We expect inbreeding-dependent DNA methylation patterns to be strongest during periods of maximal trait expression, to be localized to specific genomic regions, and to be trait-specific.In summary, our project tackles an important knowledge gap by combining detailed data from multiple sexual traits over individual lifespans with genomic and epigenetic data in a classical lekking species. This project has the unrivalled potential to transform our understanding of sexual selection and underpin the next generation of detailed studies.

• DFG Programme: Research Grants