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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 Hybridisation is a common feature of evolutionary radiations, but its genomic consequences vary depending on when it occurs. Since reproductive isolation takes time to accumulate, hybridisation can occur at multiple points during divergence. Previous studies suggested that the taxonomic diversity in evolutionary radiations can help infer the timing of past gene flow events. Here, we assess the power of these approaches for revealing when gene flow occurred between two monkeyflower taxa (Mimulus aurantiacus) endemic to the Channel Islands of California. Coalescent simulations reveal that conventional four‐taxon tests may not be capable of fully distinguishing between recent and ancient introgression, but genome‐wide patterns of phylogenetic discordance vary predictably with different histories of hybridisation. Using whole‐genome sequencing and phylogenetic tests for introgression across theM. aurantiacusradiation, we identify signals of both ancient and recent hybridisation that occurred between the island taxa and their ancestors. In addition, we find widespread selection against introgressed ancestry, consistent with polygenic barriers to gene flow. However, we also identify localised signals across the genome that may indicate adaptive introgression. This study highlights the power and challenges of trying to disentangle complex histories of hybridisation. More broadly, our results illustrate the multiple roles that gene flow can play in evolutionary radiations: hybridisation can expose genetic incompatibilities that contribute to reproductive isolation while also likely facilitating adaptation by transferring beneficial alleles between taxa. These findings underscore the dynamic interplay between the timing of hybridisation and natural selection in shaping evolutionary trajectories within radiations. 

Abstract Plants have the ability to transmit mutations to progeny that arise through both meiotic and mitotic (somatic) cell divisions. This is because the same meristem cells responsible for vegetative growth will also generate gametes for sexual reproduction. Despite the potential for somatic mutations to contribute to genetic variation and adaptation, their role in plant evolution remains largely unexplored. We conducted experiments with the bush monkeyflower (Mimulus aurantiacus) to assess the phenotypic effects of somatic mutations inherited across generations. By generating self-pollinations within a flower (autogamy) or between flowers on different stems of the same plant (geitonogamy), we tracked the effects of somatic mutations transmitted to progeny. Autogamy and geitonogamy lead to different segregation patterns of somatic mutations among stems, with only autogamy resulting in offspring that are homozygous for somatic mutations specific to that stem. This allowed us to compare average phenotypic differences between pollination treatments that could be attributed to the inheritance of somatic variants. While most experimental units showed no impacts on fitness, in some cases, we detected increased seed production, as well as significant increases in drought tolerance, even though M. aurantiacus is already well adapted to drought conditions. We also found increased variance in drought tolerance following autogamy, consistent with the hypothesis that somatic mutations transmitted between generations can impact fitness. These results highlight the potential role of inherited somatic mutations as a relevant source of genetic variation in plant evolution. 

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. 

The unique life form of plants promotes the accumulation of somatic mutations that can be passed to offspring in the next generation, because the same meristem cells responsible for vegetative growth also generate gametes for sexual reproduction. However, little is known about the consequences of somatic mutation accumulation for offspring fitness. We evaluate the fitness effects of somatic mutations in Mimulus guttatus by comparing progeny from self-pollinations made within the same flower (autogamy) to progeny from self-pollinations made between stems on the same plant (geitonogamy). The effects of somatic mutations are evident from this comparison, as autogamy leads to homozygosity of a proportion of somatic mutations, but progeny from geitonogamy remain heterozygous for mutations unique to each stem. In two different experiments, we find consistent fitness effects of somatic mutations from individual stems. Surprisingly, several progeny groups from autogamous crosses displayed increases in fitness compared to progeny from geitonogamy crosses, likely indicating that beneficial somatic mutations occurred in some stems. These results support the hypothesis that somatic mutations accumulate during vegetative growth, but they are filtered by different forms of selection that occur throughout development, resulting in the culling of expressed deleterious mutations and the retention of beneficial mutations.