Collaborative Research: Genetic redundancy and the tempo of polygenic adaptation in small natural populations

Evolution can occur more quickly than the many people think. Some of the fastest examples occur in small or newly established populations, even though these populations usually have less genetic variation. This presents a fundamental puzzle: how can populations with so little genetic variation adapt so quickly to new challenges? One possible explanation is that many different genes each make small contributions to important traits, such as the ability to survive disease. Because so many genes influence these traits, losing some genetic variation may not prevent adaptation. Different populations may reach the same solution using different combinations of genes. This genetic redundancy is a central prediction of evolutionary theory but has rarely been demonstrated in nature. By combining long-term field data with modern genome sequencing and computational analyses, this project will determine whether wild guppy populations adapt through the same genetic changes or through different genetic solutions leading to the same abilities. Understanding how populations adapt to environmental change is increasingly important as wildlife faces emerging diseases, invasive species, and habitat alteration. Beyond advancing fundamental knowledge of evolution, this project will provide research opportunities for high school, undergraduate, graduate, and early-career scientists through training programs at the University of Notre Dame, Auburn University, and long-running field programs in Trinidad. The resulting data, analytical tools, and educational activities will help prepare the next generation of scientists while increasing public understanding of how evolution shapes the natural world. This project will test fundamental predictions of polygenic adaptation theory using four replicated populations of Trinidadian guppies that independently evolved following invasion by the same parasitic nematode. The investigators will combine genomic prediction, whole-genome sequencing of archived samples collected before, during, and after parasite invasion, and temporal analyses of allele-frequency change to reconstruct the evolutionary process through time. Genomic prediction will first be used to estimate the genetic architecture of parasite tolerance by quantifying the contributions of thousands of genes to this complex trait. These estimates will then be integrated with temporal genomic data to evaluate whether adaptive evolution occurred through shared or alternative genetic solutions and whether selection acted as a brief evolutionary pulse or persisted across multiple generations. Simulation models incorporating known pedigrees will distinguish natural selection from genetic drift and evaluate alternative evolutionary scenarios. By integrating quantitative genetics, temporal genomics, and replicated natural populations, this project will provide a rigorous test of how genetic redundancy shapes rapid adaptation in the wild and establish a general framework for studying evolutionary responses to environmental change. 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.