Antifungal alternation can be beneficial for durability but at the cost of generalist resistance

Abstract

The evolution of resistance to pesticides is a major burden in agriculture. Resistance management involves maximizing selection pressure heterogeneity, particularly by combining active ingredients with different modes of action. We tested the hypothesis that alternation may delay the build-up of resistance not only by spreading selection pressure over longer periods, but also by decreasing the rate of evolution of resistance to alternated fungicides, by applying an experimental evolution approach to the economically important crop pathogen Zymoseptoria tritici. Our results show that alternation is either neutral or slows the evolution of resistance, relative to continuous fungicide use, but results in higher levels of generalism in evolved lines. We demonstrate that the relative risk of resistance intrinsic to fungicide alternation probably underlies a trade-off between the number of fungicides and the frequency of alternation. This trade-off is also dynamic over the course of resistance evolution. These findings open up new possibilities for tailoring resistance management effectively while optimizing interplay between alternation components.

Why do fungicide mixtures delay the evolution of resistance? An experimental evolutionary approach

“…The design of this experiment was similar to that used in a previous study [22] using the same AIs but addressing the issue of the sustainability of alternation strategies. Here, the ranking of times to resistance emergence did not reflect the assumed hierarchy of the intrinsic risks of resistance associated with benzimidazoles (high; C), SDHIs (moderate to high; B) and DMIs (moderate; P) [26].…”

“…We ensured that population sizes were equivalent at the start of each cycle by mimicking immigration from external populations through the addition of spores from the untreated line to reach a total of 10 7 spores for each line. OD 405 was measured at the end of each cycle and used to calculate population size (see [22] for details). Malthusian growth was calculated for each line as previously described [23]: Spore concentration and Malthusian growth were normalized against the concentration and Malthusian growth, respectively, of the control line.…”

“…Using an approach previously developed for the study of resistance selection in alternation strategies [22], we observed the evolution of resistance in a haploid yeast-like easily cultured form of a fully susceptible strain of Z. tritici . We first compared the rates of resistance evolution under single or mixed fungicide treatments, for three AIs with different modes of action applied in amounts resulting in similar efficacy ( i.e .…”

Are Efficient-Dose Mixtures a Solution to Reduce Fungicide Load and Delay Evolution of Resistance? An Experimental Evolutionary Approach

“…We ensured that population sizes were equivalent at the start of each cycle by mimicking immigration from external populations through the addition of spores from the untreated line to reach a total of 10 7 spores for each line. OD 405 was measured at the end of each cycle and used to calculate population size (see [22] for details). Malthusian growth was calculated for each line as previously described [23]: m = ln( cell density at the end of the cycle, day 7 cell density at the beginning of the cycle, day 0 )…”

“…Using an approach previously developed for the study of resistance selection in alternation strategies [22], we observed the evolution of resistance in a haploid yeast-like easily cultured form of a fully susceptible strain of Z. tritici. We first compared the rates of resistance evolution under single or mixed fungicide treatments for three AIs with different modes of action applied in amounts resulting in similar efficacy (i.e., EC 90 ).…”