Repeated origins, gene flow, and allelic interactions of herbicide resistance mutations in a widespread agricultural weed

Abstract

Causal mutations and their frequency in nature are well-characterized for herbicide resistance. However, we still lack understanding of the extent of parallelism in the mutational origin of target-site resistance (TSR), the role of standing variation and gene flow in the spread of TSR variants, and allelic interactions that mediate their selective advantage. We addressed these questions with genomic data from 18 agricultural populations of Amaranthus tuberculatus, which we show to have undergone a massive expansion over the past century, with a contemporary Ne estimate of 8x107. We found nine TSR variants, three of which were common—showing extreme parallelism in mutational origin and an important role of gene flow in their geographic spread. The number of repeated origins varied across TSR loci and generally showed stronger signals of selection on de novo mutations, but with considerable evidence for selection on standing variation. Allele ages at TSR loci varied from ~10-250 years old, greatly predating the advent of herbicides. The evolutionary history of TSR has also been shaped by both intra- and inter-locus allelic interactions. We found evidence of haplotype competition between two TSR mutations, their successes in part modulated by either adaptive introgression of, or epistasis with, genome-wide resistance alleles. Together, this work reveals a remarkable example of spatial parallel evolution—the ability of independent mutations to spread due to selection contingent on not only the time, place, and background on which they arise but the haplotypes they encounter.

Selective ancestral sorting and de novo evolution in the agricultural invasion of Amaranthus tuberculatus

“…It is extremely successful in agricultural systems, hypothesized to result in part from a combination of its obligately outcrossing dioecious wind-pollinated mating system (Costea et al 2005) and extremely high seed production (with females producing on average between 35,000 and 1,200,000 notably small [1 mm] seeds [Stevens 1932;Sellers et al 2003;Hartzler et al 2004]). Recent inference in the species highlights a massive recent expansion in effective population size over the last century-a key consequence of which is highly parallel target-site resistance evolution (Kreiner et al 2021). In A. tuberculatus, two major lineages and ecotypes exist, the classification of which has been debated and revised from two species (Riddell 1835;Sauer 1955) to one (Uline and Bray.…”

Interchromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance

“…Third, we anticipated that linkage disequilibrium, the nonrandom association of alleles at different loci, should be evident among regions of the genome harboring resistance loci. Although ILD has been identified in other systems for ecologically relevant traits such as mate choice and coloration (Petkov et al ., 2005; Long et al ., 2013; Hench et al ., 2019), and recently has even been implicated in TSR (Kreiner et al ., 2021a), it is unknown whether loci underlying NTSR that are found across chromosomes exhibit long‐distance or ILD, as would be expected if adaptation to herbicide is facilitated by multilocus genotypes favored by selection (Wallace, 1953; Dobzhansky, 1971; Schluter, 2000; Yeaman et al ., 2016).…”

Testing the role of allelochemicals in different wheat cultivars to sustainably manage weeds

“…In cropping systems, weeds are undesirable, competitive and, in many cases, difficult to eliminate, causing a loss of more than 34% of crop yields and becoming the most economically relevant pest in the agroecosystem 1 . In recent years, there has been massive use of synthetic herbicides, which are effective for weed control, but, conversely, cause problems in ecosystems resulting in damage to the environment and human health while inducing weeds' resistance 2 . For this reason, it is essential to work towards nonherbicide alternatives, such as organic farming methods that encourage healthy soil and weed management while avoiding agrochemicals.…”

“…1 In recent years, there has been massive use of synthetic herbicides, which are effective for weed control, but, conversely, cause problems in ecosystems resulting in damage to the environment and human health while inducing weeds' resistance. 2 For this reason, it is essential to work towards nonherbicide alternatives, such as organic farming methods that encourage healthy soil and weed management while avoiding agrochemicals. The coexistence of crops with spontaneous herbs promotes biodiversity and soil health as long as they do not become pests.…”