There are now many beautiful examples of phenotypic evolution on ecological timescales. Nevertheless, technological challenges and limited availability of temporal genomic data have left a large gap in knowledge of short-term evolutionary dynamics at the genomic level. Indeed, measuring evolution of natural populations in real-time remains challenging, and systems with sufficient data to study contemporary genetic evolution are rare. The proposed work combines evolutionary genomics with long-term demographic and pedigree data to investigate the evolution of natural populations on short timescales. Long-term, individual-based studies that have accumulated extensive phenotypic, environmental, and fitness data for thousands of individuals on a multigenerational pedigree provide a unique opportunity to study how short-term evolution occurs. In particular, knowledge of the population pedigree, the relationships among all individuals in a population over time, provides the ability to observe directly the actual processes underlying allele frequency change. The PI developed the Florida Scrub-Jay (Aphelocoma coerulescens) as a model for evolutionary genomics by adding substantial genomic data to a 50-year demographic study and formed collaborations with other groups with similar long-term datasets. This study will track the inheritance of the entire genome down the pedigree, as it is broken up by recombination over the generations, in two classic study systems: the Florida Scrub-Jay and the Soay sheep. Elucidating how an individual's genome is distributed across its descendants from generation to generation provides a powerful framework for determining how individual variation in lifetime reproductive success predicts variation in individual genetic contributions to future generations and allele frequency change and for identifying genomic regions associated with fitness. This project will also develop haplotype-dropping methods that simulate Mendelian transmission of haplotypes down the pedigree to test for short-term selection and improve selection component methods to test for selection at different life-history stages. Application of these methods to the Florida Scrub-Jays will increase understanding of the role of fluctuating selection and life- history trade-offs in maintaining adaptive genetic variation in natural populations. Furthermore, the proposed work will quantify the long-term contributions of immigrants to population genetic diversity and fitness by tracing the frequency and fitness impact of specific immigrant haplotypes across generations. Developing more advanced methods that effectively use pedigree information unlocks unprecedented opportunities to directly measure contemporary evolution and study many key questions in evolutionary biology. The proposed framework outlines a powerful approach for future evolutionary and human genomics research. A better understanding of evolution on ecological time scales offers valuable insights to studies of organismal response to rapid environmental change, as well as the evolution of drug and pesticide resistance.
A deeper understanding of the genetic basis of contemporary evolution in nature is critical to predict accurately how modern public health and medical interventions affect the long-term health and demography of human populations. Population pedigrees offer the ability to measure directly the evolutionary processes shaping patterns of genomic variation, but the few human populations with extensive pedigree information often have limited phenotypic and environmental data. Therefore, studies of contemporary evolution in long-term, individual-based systems provide unique opportunities to test directly long-standing questions in evolutionary biology, with significant implications for both understanding human evolution and efforts to breed crops and livestock to feed the rapidly growing human population.