Resistance evolution, from genetic mechanism to ecological contextRegina S. Baucom1, Veronica Iriart2, Julia Kreiner3, and Sarah Yakimowski41Ecology and Evolutionary Biology Department, University of Michigan, Ann Arbor, Michigan, USA2Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA3Biodiversity Research Centre & Department of Botany, The University of British Columbia, Vancouver, BC V6T 1Z44Department of Biology, Queen’s University, Kingston, ON K7L 3N6CorrespondenceRegina S. Baucom, Ecology and Evolutionary Biology Department, University of Michigan, Ann Arbor, Michigan, 48109.Email: [email protected]*Authors contributed equallyPesticide use by humans has induced strong selective pressures, reshaping evolutionary trajectories, ecological networks, and even influencing ecosystem dynamics. The evolution of pesticide resistance across weeds, insects, and fungi often leads to negative impacts on both human health and the economy while concomitantly providing excellent systems for studying the process of evolution. In fact, the study of pesticide resistance has been a feature of evolutionary biology since the Evolutionary Synthesis, with Dobzhansky noting in his book The Genetics and Origins of Species (1937) that cyanide resistance in the California red scale constituted the “best proof of the effectiveness of natural selection yet obtained”. Following the pioneering work of James Crow and others in the 1950’s—which greatly expanded our knowledge of the genetics underlying adaptation—the study of pesticide resistance has shed light on a variety of topics, such as the repeatability of phenotypic evolution across the landscape, ‘hotspots’ of evolution across the genome, and information on the number and type of genetic solutions that populations may employ to strong selection pressures.Landscape level approaches have come to the forefront over the last 20 years of resistance evolution research, often taking advantage of the fact that replicated populations of the same species are exposed to the same pesticide. Further, the resistance evolution field is turning more attention to the ecological context within which resistance evolution occurs, likely stemming, at least in part, from an historical focus on fitness costs (Cousens & Fournier-Level 2018; Baucom 2019). This special feature, ‘Resistance evolution, from genetic mechanism to ecological context’ in Molecular Ecology captures the current state of resistance evolution with contributions broadly addressing the question ‘What has the rapid evolution of pesticide resistance taught us about genome dynamics and adaptation as well as the ecological context within which resistance evolution occurs?’ Below, we contextualize the manuscripts in this special issue that provide insight into the state of the art investigations of resistance evolution across various species of insects, weeds and fungi.

Although much of what we know about the genetic basis of herbicide resistance has come from detailed investigations of monogenic adaptation at known target-sites, the importance of polygenic resistance has been increasingly recognized. Despite this, little work has been done to characterize the genomic basis of herbicide resistance, including the number and distribution of involved genes, their effect sizes, allele frequencies, and signatures of selection. Here we implement genome-wide association (GWA) and population genomic approaches to examine the genetic architecture of glyphosate resistance in the problematic agricultural weed, Amaranthus tuberculatus. GWA correctly identifies the gene targeted by glyphosate, and additionally finds more than 100 genes across all 16 chromosomes associated with resistance. The encoded proteins have relevant non-target-site resistance and stress-related functions, with potential for pleiotropic roles in resistance to other herbicides and diverse life history traits. Resistance-related alleles are enriched for large effects and intermediate frequencies, implying that strong selection has shaped the genetic architecture of resistance despite potential pleiotropic costs. The range of common and rare allele involvement implies a partially shared genetic basis of non-target-site resistance across populations, complemented by population-specific alleles. Resistance-related alleles show evidence of balancing selection, and suggest a long-term maintenance of standing variation at stress-response loci that have implications for plant performance under herbicide pressure. By our estimates, genome-wide SNPs explain a near comparable amount of the total variation in glyphosate resistance to monogenic mechanisms, indicating the potential for an underappreciated polygenic contribution to the evolution of herbicide resistance in weed populations.