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.

Keywords: adaptive introgression; de novo mutation; evolution; fungicide; herbicide; insecticide; pesticide resistance; pleiotropic co-option; selective sweeps; standing variation.

Figure 1

Evolution of pesticide resistance: (A) by de novo mutation; (B) by selection from standing genetic variation.

Figure 2

Phylogenetic origins of pesticide‐resistant alleles. The upper part of each panel shows genes superimposed onto a species tree; the lower part shows the resulting gene tree. (A) Allele transfer by horizontal gene transfer or adaptive introgression; (B) parallel evolution by independent de novo mutations; (C) collateral selection from pre‐speciation standing variation. AS: species A, sensitive allele; BS: species B, sensitive allele; AR: species A, resistant allele; BR: species B, resistant allele. Grey lines, sensitive allele; black lines, resistant allele; dashed lines, sensitive allele may have been lost from sister species if resistance has previously reached fixation.

Figure 3

Proposed model for determining whether resistance will evolve from standing variation or de novo mutations for a given pest–pesticide system. Factors influencing the outcome of each question are discussed in the text sections referred to in the grey text.