Competition between genotypes within a plant population can result in the displacement of the least competitive by more competitive genotypes. Although evolutionary processes in plants may occur over thousands and millions of years, it has been suggested that changes in key fitness traits could occur in as little as decades being herbicide resistance a common example. However, the rapid evolution of complex traits has not been proven in weeds. We hypothesized that changes in weed growth and competitive ability can occur in just a few years because of selection in agroecosystems. Seed of multiple generations of a single natural population of the grassy weed giant foxtail (Setaria faberi Herrm.) were collected during 34 years (i.e., 1983 to 2017). Using a “resurrection” approach, we characterized life-history traits of the different year-lines under non-competitive and competitive conditions. Replacement-series experiments comparing the growth of the oldest year-line (1983) vs. newer year-lines (1991, 1996, 1998, 2009, and 2017) showed that plant competitive ability decreased and then increased progressively in accordance with oscillating selection. The adaptations in competitive ability were reflected in dynamic changes in leaf area and biomass when plants were in competition. The onset of increased competitive ability coincided with the introduction of herbicide-resistant crops in the landscape in 1996. We also conducted a genome-wide association study (GWAS) and identified four loci that were associated with increased competitive ability over time, confirming that this trait changed in response to directional selection. Putative transcription factors and cell wall-associated enzymes were linked to those loci. This is the first study providing direct in situ evidence of rapid directional evolution of competitive ability in a plant species. The results suggest that agricultural systems can exert enough pressure to cause evolutionary adaptations of complex life-history traits potentially increasing weediness and invasiveness.

BACKGROUNDThe potential of weed species to respond to selection forces affecting the evolution of weedy traits such as competitive ability is poorly understood. This research characterized evolutionary growth changes in a single Abutilon theophrasti Medik. population comparing multiple generations collected from 1988 to 2016. A competition study was performed to understand changes in competitive ability, and a herbicide dose–response study was carried out to assess changes in sensitivity to acetolactate synthase‐inhibiting herbicides and glyphosate over time.RESULTSWhen grown in monoculture, A. theophrasti biomass production per plant increased steadily across year‐lines while leaf number decreased. In replacement experiments, A. theophrasti plants from newer year‐lines were more competitive and produced more biomass and leaf area than the oldest year‐line. No clear differences in sensitivity to imazamox were observed among year‐lines. However, starting in 1995, this A. theophrasti population exhibited a progressive increase in growth in response to a sublethal dose of glyphosate (52 g a.e. ha−1), with the 2009 and 2016 year‐lines having more than 50% higher biomass than the nontreated control.CONCLUSIONThis study demonstrates that weeds can rapidly evolve increased competitive ability. Furthermore, the results indicate the possibility of changes in glyphosate hormesis over time. These results highlight the importance of the role that rapid (i.e., subdecadal) evolution of growth traits might have on the sustainability of weed management strategies. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.