Dana Lauenroth's scientific contributions

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Publications (3)


Assessing the probability and time of weed control failure due to herbicide resistance evolution
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April 2024

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14 Reads

Dana Lauenroth

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The recurrent exposure to herbicides in agricultural landscapes forces weeds to adapt in a race against extinction. What role newly arising mutations and pre-existing variation play in this evolution of herbicide resistance is critical for developing management strategies. Here, we present a model of rapid adaptation in response to strong selection, capturing complex life cycles of sexual and asexual reproduction and dormancy in a perennial weed. Using a multitype Galton-Watson process, we derive the probability of herbicide resistance evolution and the waiting time distribution until resistant plants appear in the field. We analyse the effect of seed bank dynamics and details of the reproductive system in defining the probability and timing of resistance adaptation in Sorghum halepense. Further, we investigate key factors determining the primary source of adaptive variation. We find that even small fitness costs associated with resistance reduce adaptation from standing genetic variation. For herbicide resistance inherited in a (incompletely) dominant fashion, self-pollination also diminishes standing variation for herbicide resistance by increasing the homozygosity. Our study highlights the importance of seed banks for weeds' adaptive potential, preserving genetic information of forgone selection and prolonging the period in which the population can adapt.

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Schematic illustration of the life cycle of Johnsongrass and its representation in our model
a, The life cycle of Johnsongrass. Johnsongrass reproduces sexually via seeds (inner ring) and asexually through rhizomes (outer ring). Seeds can stay dormant in the ground for several years, forming a seed bank (central circle). New seeds and seeds from the seed bank might germinate in spring or stay dormant as part of the seed bank (expressed by the dotted line). Rhizomes give rise to shoots in the first spring after their production. Herbicide application (red dotted line) can kill susceptible seedlings and shoots. The plants that survive, then compete for resources as they mature. The aboveground plant material dies in winter and Johnsongrass overwinters as seeds and rhizomes in the ground. b, Schematic representation of our model. The left side corresponds to the sexual reproduction of Johnsongrass and the right side represents the asexual propagation. Solid arrows depict within-season dynamics and dashed arrows show dynamics between seasons. Survival probabilities and fecundity are shown in grey next to the corresponding arrows. c, Intraspecific competition. Intraspecific resource competition leads to self-thinning and density-dependent fecundity reduction. The left graph displays the probability of intraspecific competition survival in young plants (P) as a function of their density. The density-dependent reduction in fecundity, that is the number of seeds (f) and rhizome buds (b) produced by mature plants, is illustrated on the right.
Variation of the approximated standing genetic variation for target-site resistance with the resistance cost
The genetic composition of untreated Johnsongrass populations is approximated on the basis of equation (22) and shown for different degrees of dominance (kc) of the resistance cost. Dashed lines correspond to a recessive resistance cost (kc = 0), solid lines indicate partial dominance (kc = 0.5) and dotted lines complete dominance (kc = 1). The grey line marks the spontaneous mutation rate of resistance alleles (μ = 10⁻⁸). a, Expected frequency of the resistance allele R in an untreated population depending on the resistance cost (c). b, Expected frequencies of the resistant genotypes in an untreated population as a function of the resistance cost (c). The frequency of resistant heterozygotes (RW) is shown in yellow and resistant homozygotes (RR) are represented in red.
Simulated target-site resistance evolution and resulting population regrowth in herbicide-treated Johnsongrass for low and high resistance cost
Shown are the results of 1,000 simulation runs obtained for a partially dominant resistance allele (kh = 0.5) and fitness cost (kc = 0.5). The initial genotype composition differs between the low (c = 0.001) and high (c = 0.3) fitness cost (compare Fig. 2b). a, Changes in genotype composition of plants (P̃\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\widetilde{P}$$\end{document}) over 30 years of herbicide application for low and high resistance cost. The frequency of sensitive plants (WW) is shown in blue, resistant heterozygotes (RW) in yellow and resistant homozygotes (RR) in red. The thick lines with closed circles correspond to the average of all simulation runs and the thin lines represent the individual realizations. b, Distribution of escapes from control over 30 years of herbicide application for low and high resistance cost. Weed populations can regrow under herbicide treatment if a resistant plant establishes on the field and reproduces. The year of escape from control is the year in which the first homozygous-resistant plant survives until reproduction. The pie charts display the proportion of simulation runs where the weed population escapes from control and regrows.
Predicted target-site resistance evolution in herbicide-treated Johnsongrass depending on seed bank formation and self-pollination
The results are obtained for a partially dominant resistance allele (kh = 0.5) and fitness cost (kc = 0.5). a, Simulated changes in Johnsongrass density (P̃/A\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\widetilde{P}/A$$\end{document}) and genotype composition of seeds (in the seed bank (B) if formed, otherwise produced seeds (S) that survived the winter) over 30 years of herbicide application and tillage depending on the formation of a seed bank. Shown are the results of 1,000 simulation runs. The thick lines with closed circles correspond to the average of all simulation runs and the thin lines represent the individual realizations. The frequency of sensitive seeds (WW) is shown in blue, resistant heterozygotes (RW) in yellow and resistant homozygotes (RR) in red. The pie charts display the proportion of simulation runs in which the weed population escapes from control and regrows due to herbicide resistance evolution. b, Predicted changes in the frequency of the resistance allele R in Johnsongrass plants (P̃\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\widetilde{P}$$\end{document}) under herbicide application for pure cross-pollination and 95% self-pollination. Shown are predictions of our deterministic model.
Predicted population dynamics and target-site resistance evolution in Johnsongrass under different control regimes
The results are obtained for a partially dominant resistance allele (kh = 0.5) and fitness cost (kc = 0.5). a, Simulated changes in Johnsongrass density (P̃/A\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\widetilde{P}/A$$\end{document}) and proportion of populations escaping from control over 30 years of different control regimes. Shown are the results of 1,000 simulation runs. The thick lines with closed circles correspond to the average of all simulation runs and the thin lines represent the individual realizations. The pie charts display the proportion of simulation runs in which the weed population escapes from control and regrows due to herbicide resistance evolution. The distinct control strategies are from left to right, top to bottom: ACCase-inhibitor application, ACCase-inhibitor application combined with tillage, application of ACCase-inhibitor and ALS-inhibitor with low efficacy, application of ACCase-inhibitor and ALS-inhibitor with low efficacy combined with tillage. b, Predicted changes in the frequency of the ACCase resistance allele R in Johnsongrass plants (P̃\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\widetilde{P}$$\end{document}) under different control regimes. Shown are predictions of our deterministic model. The distinct control strategies are: ACCase-inhibitor (light grey line with closed circles) or ACCase-inhibitor and ALS-inhibitor with low (dark grey line with closed squares) or high (black line with closed triangles) efficacy applied solely (solid line) or combined with tillage (dashed line).

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Theoretical assessment of persistence and adaptation in weeds with complex life cycles

August 2023

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81 Reads

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3 Citations

Nature Plants

Herbicide-resistant weeds pose a substantial threat to global food security. Perennial weed species are particularly troublesome. Such perennials as Sorghum halepense spread quickly and are difficult to manage due to their ability to reproduce sexually via seeds and asexually through rhizomes. Our theoretical study of S. halepense incorporates this complex life cycle with control measures of herbicide application and tillage. Rooted in the biology and experimental data of S. halepense, our population-based model predicts population dynamics and target-site resistance evolution in this perennial weed. We found that the resistance cost determines the standing genetic variation for herbicide resistance. The sexual phase of the life cycle, including self-pollination and seed bank dynamics, contributes substantially to the persistence and rapid adaptation of S. halepense. While self-pollination accelerates target-site resistance evolution, seed banks considerably increase the probability of escape from control strategies and maintain genetic variation. Combining tillage and herbicide application effectively reduces weed densities and the risk of control failure without delaying resistance adaptation. We also show how mixtures of different herbicide classes are superior to rotations and mono-treatment in controlling perennial weeds and resistance evolution. Thus, by integrating experimental data and agronomic views, our theoretical study synergistically contributes to understanding and tackling the global threat to food security from resistant weeds.


Figure 7: Simulated change in Johnsongrass density per m 2 and number of escapes from control for different control strategies over 30 years (k c = 0.5, k h = 0.5). Thick lines correspond to averages over 1000 simulation runs and thin lines depict individual runs (section 2.2). The distinct control strategies are from left to right, top to bottom: ACCase-inhibitor application, ACCase-inhibitor application combined with tillage, application of ACCase-inhibitor and ALS-inhibitor with low efficiency, application of ACCase-inhibitor and ALS-inhibitor with low efficiency combined with tillage.
Figure 8: Deterministic change in the ACCase resistance allele fraction in plants (Eq. (7)) for different control strategies over 30 years (k c = 0.5, k h = 0.5). The distinct control strategies are: ACCase-inhibitor or ACCase-inhibitor and ALS-inhibitor with low or high efficiency applied solely or combined with tillage.
Figure 9: Average proportion of escapes from control, average year of escape and year of fixation of the resistance allele over 30 years depending on the cycle length in rotations of ACCase-inhibitor and ALS-inhibitor with equal efficiency (k c = 0.5, k h = 0.5). The cycle length corresponds to the number of years one herbicide is recurrently applied before the treatment switches to the other herbicide. (A) Presented values are the average over 10 5 stochastic simulation runs (section 2.2). (B) The year of resistance allele fixation is equivalent to the year in which the resistance allele frequency in plants (Eq. (7)), obtained from the deterministic model, reaches 99.5 %.
Model parameters, values and references.
(continued)
Theoretical assessment of persistence and adaptation in weeds with complex life cycles

August 2022

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64 Reads

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1 Citation

Perennial weed species like Sorghum halepense are a bane of agriculture and lead to significant economic losses. Such weeds can spread quickly and are particularly hard to control due to their ability to reproduce sexually via seeds and asexually through rhizomes. The growing problem of herbicide resistance imposes an additional major challenge on the weed management. Our theoretical study of Sorghum halepense incorporates the complete complex life cycle along with control measures of herbicide application and tillage. We evaluate the extent of control that the different strategies provide and the evolution of herbicide resistance. Our analysis indicates that the natural frequency of target-site resistance mainly depends on the resistance cost and less on its dominance. The sexual phase of the life cycle, including self-pollination and seed bank dynamics, contributes substantially to the persistence and rapid adaptation of the weed. For example, the seed bank significantly increases the probability of escape from control while maintaining genetic variation. We also extend our analysis to study herbicide mixtures, rotations and treatment combinations and how they contribute to reducing control failure. Our model is rooted in observational and experimental data on Sorghum halepense. Still, the general methodology developed herein is extendable to other perennial weeds comprising a complex life cycle. This approach shows how an integrated interdisciplinary view can synergistically contribute to understanding and tackling the global threat to food production presented by resistant weeds.

Citations (2)


... The mathematical representation of the model is shown in Figure 1 b. In Lauenroth and Gokhale (2023), we presented a deterministic model of Johnsongrass' life cycle capturing all life-history stages and intraspecific competition between the plants, allowing the prediction of long-term population dynamics ( Figure 1 a). In the present study, we are interested in the probability and timing of herbicide resistance evolution. ...

Reference:

Assessing the probability and time of weed control failure due to herbicide resistance evolution
Theoretical assessment of persistence and adaptation in weeds with complex life cycles

Nature Plants

... The general result can be tailored to the specific properties of the crops, such as the threshold soil quality required to grow the cash crop and how fast the cover crop can replenish the soil quality. The probabilities of profit making are often complex combinations of social, economic and evolutionary parameters such as the presence and intensity of crop pests like pathogens and weeds [8,28]. For crop systems, these probabiltities can then be estimated to develop a system-specific model. ...

Theoretical assessment of persistence and adaptation in weeds with complex life cycles