The evolutionary origins of pesticide resistance

Abstract

Durable crop protection is an essential component of current and future food security. However, the effectiveness of pesticides is threatened by the evolution of resistant pathogens, weeds and insect pests. Pesticides are mostly novel synthetic compounds, and yet target species are often able to evolve resistance soon after a new compound is introduced. Therefore, pesticide resistance provides an interesting case of rapid evolution under strong selective pressures, which can be used to address fundamental questions concerning the evolutionary origins of adaptations to novel conditions. We ask: (i) whether this adaptive potential originates mainly from de novo mutations or from standing variation; (ii) which pre-existing traits could form the basis of resistance adaptations; and (iii) whether recurrence of resistance mechanisms among species results from interbreeding and horizontal gene transfer or from independent parallel evolution. We compare and contrast the three major pesticide groups: insecticides, herbicides and fungicides. Whilst resistance to these three agrochemical classes is to some extent united by the common evolutionary forces at play, there are also important differences. Fungicide resistance appears to evolve, in most cases, by de novo point mutations in the target-site encoding genes; herbicide resistance often evolves through selection of polygenic metabolic resistance from standing variation; and insecticide resistance evolves through a combination of standing variation and de novo mutations in the target site or major metabolic resistance genes. This has practical implications for resistance risk assessment and management, and lessons learnt from pesticide resistance should be applied in the deployment of novel, non-chemical pest-control methods.

Induced expression of CYP51 associated with difenoconazole resistance in the pathogenic Alternaria sect. on potato in China

“…Fungicide resistance in pathogens occurs when the changes in these chemical and physiological processes enable pathogen populations to evade biological and biochemical interruption from a fungicide. Pathogens can adapt to fungicide pressure qualitatively or quantitatively depending on the underlying resistance mechanisms and modes of action …”

Independently evolved and gene flow‐accelerated pesticide resistance in two‐spotted spider mites

“…A fundamental question in the evolution of pesticide resistance is the origin of resistance mutations in natural populations (Ffrench-Constant, 2007), whether they emerge within a population from standing genetic variation or as new mutations, versus being introduced into it through migration. Answers to this question can contribute to insecticide resistance management (IRM) programs and theories of adaptive evolution more generally (Daborn & Le Goff, 2004;Hawkins et al, 2018;MacLean, Hall, Perron, & Buckling, 2010;Neve, Busi, Renton, & Vila-Aiub, 2014).…”

Transcription factor FTZ‐F1 and cis‐acting elements mediate expression of CYP6BG1 conferring resistance to chlorantraniliprole in Plutella xylostella

“…The evolution of insecticide resistance causes huge loses through its impact on crop production. Insecticide resistance is most often acquired through enhancement of metabolic detoxification and alterations in the target site of insecticides . An increase in the activities of detoxification enzymes is often related to metabolic degradation .…”