Repeated origins, widespread gene flow, and allelic interactions of target-site herbicide resistance mutations

Abstract

Causal mutations and their frequency in agricultural fields are well-characterized for herbicide resistance. However, we still lack understanding of their evolutionary history: the extent of parallelism in the origins of target-site resistance (TSR), how long these mutations persist, how quickly they spread, and allelic interactions that mediate their selective advantage. We addressed these questions with genomic data from 18 agricultural populations of common waterhemp (Amaranthus tuberculatus), which we show to have undergone a massive expansion over the past century, with a contemporary effective population size (Ne) estimate of 8x107. We found variation at seven characterized TSR loci, two of which had multiple amino acid substitutions, and three of which were common. These three common resistance variants show parallelism in their mutational origins, with gene flow having shaped their distribution across the landscape. Allele age estimates supported a strong role of adaptation from de novo mutations, with a median allele age of 30 suggesting that most resistance alleles arose soon after the onset of herbicide use. However, resistant lineages varied in both their age and evidence for selection over two different timescales, implying considerable heterogeneity in the forces that govern their persistence. The evolutionary history of TSR has also been shaped by both intra- and inter-locus allelic interactions. We report a signal of extended haplotype competition between two common TSR alleles, and extreme linkage with genome-wide alleles with known functions in resistance adaptation. Together, this work reveals a remarkable example of spatial parallel evolution in a metapopulation, with important implications for the management of herbicide resistance.

Rapid weed adaptation and range expansion in response to agriculture over the last two centuries

“…tuberculatus ancestry into the most eastwards part of the range in Kansas ( Fig 4B) . A. tuberculatus demography thus appears to have been drastically influenced by human-mediated landscape change over the last two centuries, consistent with the massive recent expansion of effective population size we have previously inferred over this same timeframe (26) . That this shift has been most notable over the last 40 years is further consistent with the timescale of rampant herbicide resistance evolution within the species (10, 26, 28) , suggesting selection on resistance may facilitate the colonization of var.…”

“…The historical trajectory of known herbicide resistance alleles epitomizes extreme selection over the last 50 years ( Fig 3D) . Five out of seven known herbicide resistance loci present in our contemporary collection are absent from our historical samples, consistent with the suggested importance of resistance adaptation from de novo mutation (25, 26) . Only three out of 108 historical samples show variation for herbicide resistance, two samples homozygous for resistance at ALS574 and one heterozygous for resistance at ALS122—all of which were sampled after the onset of herbicide applications in the 1960s ( Fig 3D) .…”

“…Average LD across SNPs was 0.043, with only four pairs of SNPs showing high pairwise LD (r 2 > 0.4) with another SNP. All of these four SNP pairs are found on separate chromosomes from the SNP with which it has high LD, suggesting the correlation is not driven by linked selection (alternatively, genome-assembly or polygenic adaptation [such as in ( 43, 64 )] may drive such a signal). Specifically, we used plink --clump, to find the most significant hit genome-wide, scan 1 Mb around it, and exclude any SNP from the resulting output that is in r 2 > 0.25 with the focal SNP.…”

Diversity of Herbicide-Resistance Mechanisms of Avena fatua L. to Acetyl-CoA Carboxylase-Inhibiting Herbicides in the Bajio, Mexico

“…The probability that two different mutations evolved to resistance in the same farm is low. This random distribution of biotypes and the lack of genetic structure in the populations are frequent in other agricultural regions [22]; the dispersion increases the complexity of the problem. For this reason, the distribution of herbicide-resistant populations is considered similar to epidemiological cases [23].…”

Weak population differentiation and high diversity in Salsola tragus in the inland Pacific Northwest, USA

“…Weed managers should expect that future herbicide-resistance traits will likely spread across the region with similar rapidity, and be prepared to adjust herbicide programs and other relevant management inputs with equal speed, regardless of their proximity to the point of initial origin. Low acrossrange differentiation, usually in combination with high levels of genetic diversity, has also been suggested as a shared trait among problematic and adaptable weeds, 79 with examples in a range of arable 67,69,[80][81][82][83][84][85][86][87] and invasive 88,89 weeds. This pattern appears to be emerging with particular regularity in outcrossing dicot weeds with widespread herbicide resistance, including Bassia scoparia, 67,85,86 Amaranthus palmeri S. Watson, 83,85 Amaranthus tuberculatus (Moq.)…”