Rapid evolution of competitive ability in Giant Foxtail (Setaria faberi) over 34 years.

Authors: ETHRIDGE, SANDRA - North Carolina State University; CHANDRA, SAKET - North Carolina State University; EVERMAN, WESLEY - North Carolina State University; JORDAN, DAVID - North Carolina State University; Locke, Anna; OWEN, MICHEAL - Iowa State University; LEON, RAMON - North Carolina State University

Submitted to: Weed Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/25/2023
Publication Date: 1/25/2023
Citation: Ethridge, S., Chandra, S., Everman, W., Jordan, D., Locke, A.M., Owen, M., Leon, R. 2023. Rapid evolution of competitive ability in giant foxtail (setaria faberi) over 34 years. Weed Science. 71(1):59-68. https://doi.org/10.1017/wsc.2023.1.
DOI: https://doi.org/10.1017/wsc.2023.1

Interpretive Summary: Plant traits, such as the abilities to outcompete neighbors for water, light, and nutrients, evolve over extremely long periods of time. The ability to outcompete neighbors is fundamental for weedy species in agricultural fields. Agricultural systems place unusual selection pressure on weeds due to intense field management. We hypothesized that this intense selection pressure could enable weed species to evolve better competitive abilities within a few decades. Using seed of the grassy weed Setaria faberi that had been collected annually from an agricultural field in Iowa from 1983 through 2017, we grew seeds from different years alongside each other to evaluate the plants’ competitive ability. Competitive ability was evaluated as the plants’ potential to outgrow their neighbors. Plant growth data showed the weed’s competitive abilitiy actually declined from 1983 to the early 1990s, but the weed’s competitive ability increased again after 1996. An analysis of genetic variation among seeds from different years identified several genetic markers associated with these complex changes in competitive ability. Overall, this study demonstrated that selection pressures in agricultural systems could push weeds to evolve rapidly, which could increase weed problems in food production.

Technical Abstract: Competition between genotypes within a plant population can result in the displacement of the least competitive by the more competitive genotypes. This is the tenet of Charles Darwin’s natural selection and speciation theory (Darwin, 1859). Although evolutionary processes in plants may occur over thousands and millions of years, in more recent times changes of key traits for fitness have occurred more rapidly in as little as hundreds and even tens of years (Otto, 2018; Pelletier & Coltman, 2018; Wu & Bradshaw, 1972). Agroecosystems are more likely than natural ecosystems to be conducive to evolutionary adaptations over shorter periods of time, due to intense and frequent disturbance thus causing strong selection pressure (Gould, 1988; Simon & Peccoud, 2018). However, our understanding of how species, especially those identified as weed species, can maintain their presence in agroecosystems and quickly adapt to diverse selection pressures is limited (Kuester et al., 2016), and this knowledge is of grave importance to ensure sustainability of food production for future generations. We hypothesised that changes in weed growth and competitive ability can occur in just a few years because of selection. Here, by tracking a single natural (non-experimental) population of the grassy weed Setaria faberi R.A.W. Herrm. over several generations using a “resurrection” experiment, we show that in just 34 years (i.e., 1983 to 2017) 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. These oscillatory temporal adaptations explain the contradictory results of studies testing the evolution of increased competitive ability (EICA) hypothesis. The onset of increased competitive ability coincided with the introduction of herbicide resistant crops in the landscape in 1996 (Duke, 2018; Owen, 2008). 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. The results suggest that agricultural systems can exert enough pressure to cause evolutionary adaptations of complex traits, such as competitive ability, potentially increasing weediness and invasiveness and adding to the challenges already threatening food production.