Can Very Rapid Adaptation Arise Without Ancestral Variation? Insight from the Molecular Evolution of Herbicide Resistance in Genus Amaranthus

In this dissertation I investigate the source and spread of adaptive resistance to the herbicide glyphosate by the weedy species Amaranthus palmeri. This is an ideal system for furthering scientific understanding of the dynamics of evolution because the adaptation is in response to a well understood selection pressure and is happening on an extremely short time scale. The plant genus Amaranthus contains several agriculturally important weeds, but is not closely related to any current model systems—the closest model system is Beta vulgaris(sugar beet). In the first part of this work I seek to determine the relationship between extant species of Amaranthus, particularly the relationship between weedy and non-weedy species, using Bayesian phylogenetic analysis of independent genomic loci. This phylogeny will provide context for investigating the dynamics of adaptation to glyphosate stress. The second chapter is an investigation of the sequence constraints and selection pressures acting on the gene that codes for 5-enolpyruvalshikimate-3-phosphate synthase (EPSPS) in the genus Amaranthus. The first population of A. palmeri verified as resistant to glyphosate was identified in Macon, Georgia in 2004. The mechanism of resistance was found to be proliferation in copy number of the gene encoding the enzyme target of glyphosate toxicity, EPSPS. The proliferation of genomic copies of the gene encoding a target enzyme is unique among mechanisms documented for herbicide resistance—though it has been observed as a resistance mechanism in other systems, including human cancer resistance to chemotherapy. Understanding EPSPS DNA sequence constraint will allow a better understanding of the evolutionary processes that led to a unique mechanism of herbicide resistance. In the final chapter I seek to determine if the same EPSPS copy number proliferation mechanism is responsible for glyphosate resistance in North Carolina A. palmeri and address the question of the source of the EPSPS copy number proliferation genotype. I investigate the potential of parallel evolution from ancestral variation as an explanation for observed spread of resistance by looking for genus-wide variation in EPSPS copy number and analyze population structure to determine the most probable number of adaptive events. Understanding the constraints on the EPSPS gene and protein that may have led to the observed resistance mechanism, how many times the mechanism evolved independently, and how it spread through the population(s) improves our understanding of how genomes are changed by adaptation to environmental stress. It also has the potential to provide important insights about the dynamics of herbicide resistance adaptation that can help growers make the best possible choices in weed management for protecting our food supply and our environment