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ABSTRACT Herbicide resistance in agricultural weeds has become one of the greatest challenges for sustainable crop production. The repeated evolution of herbicide resistance provides an excellent opportunity to study the genetic and physiological basis of the resistance phenotype and the evolutionary responses to human‐mediated selection pressures.Lolium multiflorumis a ubiquitous weed that has evolved herbicide resistance repeatedly around the world in various cropping systems. We assembled and annotated a chromosome‐scale genome forL. multiflorumand elucidated the genetic architecture of paraquat resistance by performing quantitative trait locus analysis, genome‐wide association studies, genetic divergence analysis and transcriptome analyses from paraquat‐resistant and ‐susceptibleL. multiflorumplants. We identified two regions on chromosome 5 that were associated with paraquat resistance. These regions both showed evidence for positive selection among the resistant populations we sampled, but the effects of this selection on the genome differed, implying a complex evolutionary history. In addition, these regions contained candidate genes that encoded cellular transport functions, including a novel multidrug and toxin extrusion (MATE) protein and a cation transporter previously shown to interact with polyamines. Given thatL. multiflorumis a weed and a cultivated crop species, the genomic resources generated will prove valuable to a wide spectrum of the plant science community. Our work contributes to a growing body of knowledge on the underlying evolutionary and ecological dynamics of rapid adaptation to strong anthropogenic selection pressure that could help initiate efforts to improve weed management practices in the long term for a more sustainable agriculture. 

Abstract The reuse of old genetic variation can promote rapid diversification in evolutionary radiations, but in most cases, the historical events underlying this divergence are not known. For example, ancient hybridization can generate new combinations of alleles that sort into descendant lineages, potentially providing the raw material to initiate divergence. In the Mimulus aurantiacus species complex, there is evidence for widespread gene flow among members of this radiation. In addition, allelic variation in the MaMyb2 gene is responsible for differences in flower color between the closely related ecotypes of subspecies puniceus, contributing to reproductive isolation by pollinators. Previous work suggested that MaMyb2 was introgressed into the red-flowered ecotype of puniceus. However, additional taxa within the radiation have independently evolved red flowers from their yellow-flowered ancestors, raising the possibility that this introgression had a more ancient origin. In this study, we used repeated tests of admixture from whole-genome sequence data across this diverse radiation to demonstrate that there has been both ancient and recurrent hybridization in this group. However, most of the signal of this ancient introgression has been removed due to selection, suggesting that widespread barriers to gene flow are in place between taxa. Yet, a roughly 30 kb region that contains the MaMyb2 gene is currently shared only among the red-flowered taxa. Patterns of admixture, sequence divergence, and extended haplotype homozygosity across this region confirm a history of ancient hybridization, where functional variants have been preserved due to positive selection in red-flowered taxa but lost in their yellow-flowered counterparts. The results of this study reveal that selection against gene flow can reduce genomic signatures of ancient hybridization, but that historical introgression can provide essential genetic variation that facilitates the repeated evolution of phenotypic traits between lineages.