Rapid evolution of competitive ability in giant foxtail (Setaria faberi) over 34 years

Abstract

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.

Changes in the herbicide sensitivity and competitive ability of Abutilon theophrasti over 28 years: Implications for hormesis and weed evolution

“…However, unlike the case of Setaria faberi R.A.W. Herrm., where clear directional selection of competitive ability was documented, 13 the trends observed here do not allow the process by which evolution of competitive ability occurred in velvetleaf to be identified. Nevertheless, the time scale covered in the present study supports the observation that weeds can exhibit rapid evolution (i.e., tens of years) of competitive ability and not only of herbicide resistance.…”

“…Under such a scenario, if glyphosate hormesis has a strong genetic component, this trait could be selected in glyphosate‐based weed‐control crop systems. Additionally, this selection might result in the evolution of higher competitive ability by favoring more vigorous growth in a competitive environment (i.e., crop canopy) 13 …”

“…Additionally, this selection might result in the evolution of higher competitive ability by favoring more vigorous growth in a competitive environment (i.e., crop canopy). 13…”

“…This has caused not only selection pressure for glyphosate resistance (GR), but also dramatic changes in crop management (e.g., fewer and less diverse rotations, uniformity in planting time, and increased reduced‐tillage and no‐till practices), weed control tools (e.g., less mechanical control), weed community composition, and interspecific competition 10,11 . It is therefore possible that evolutionary adaptations other than GR, such as changes in seed dormancy, plant height, nutrient use efficiency, and competitive ability, have been occurring during that time 12–15 …”

“…10,11 It is therefore possible that evolutionary adaptations other than GR, such as changes in seed dormancy, plant height, nutrient use efficiency, and competitive ability, have been occurring during that time. [12][13][14][15] Abutilon theophrasti Medik. (velvetleaf) is an annual weed of economic importance in major agronomic crops such as maize (Zea mays L.), cotton (Gossypium hirsutum L.), and soybean (Glycine max [L.] Merr.).…”