Does host plant adaptation lead to pesticide resistance in generalist herbivores?

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Highlights

  • Link between host plant adaptation and resistance evolution was critically assessed.

  • No clear causal relationship was found between both evolutionary phenomena.

  • Rapid resistance evolution in generalist herbivores rather reflects pest status.

  • Other factors probably play a more predominant role in resistance development.

Most herbivorous arthropods feed on one or a few closely related plant species; however, certain insect and mite species have a greatly expanded host range. Several of these generalists also show a remarkable propensity to evolve resistance to chemical pesticides. In this review, we ask if the evolution of mechanisms to tolerate the diversity of plant secondary metabolites that generalist herbivores encounter, has pre-adapted them to resist synthetic pesticides. Critical examination of the evidence suggests that a generalist life-style per se is not a predictor of rapid resistance evolution to pesticides. Rather the prevalence of pesticide resistance in generalist herbivores probably reflects their economic importance as pests and thus the strong selection imposed by intensive pesticide use.

Introduction

Herbivorous insects and mites are exposed to a myriad of chemicals produced by the host plant(s) they feed on, some highly toxic. This observation has led to the proposal that generalist herbivores will, over evolutionary time, be exposed to a greater variety of chemicals than specialists, and that their ability to transport, sequester and detoxify such compounds may pre-adapt them to ‘novel’ xenobiotics such as insecticides (recently also reviewed in [1]). This ‘pre-adaptation’ hypothesis, that polyphagous pests might be genetically predisposed to more rapidly develop pesticide resistance, can be traced back nearly 60 years. In 1961, Gordon [2] proposed that “R [resistance] genes that by selection and recombination under insecticide pressure give rise to R strains are alleles of common genes, the normal function of which is metabolism of biochemicals present in the normal insect [diet]”. He observed further that “the larval feeding stages of relatively polyphagous holometabolous insects often show extraordinarily high and generalized tolerance to contact insecticides” [2]. This idea gained credence following a study by Krieger et al. [3] who observed higher activities of P450 enzymes in polyphagous than in monophagous species (but did not relate such differences to resistance). It is now understood that adaptation to both plant toxins and pesticides can involve more than just metabolism (detoxification) and that target site modification, transport (excretion) and sequestration can all play important roles in this process [4, 5, 6, 7, 8]. In this review, we examine the relationship between insect adaptation to toxic plant secondary metabolites and resistance to pesticides, and critically evaluate the evidence that suggests generalist herbivores are more prone to develop resistance to pesticides than specialists.

Section snippets

Resistance to insecticides and tolerance of plant toxins

Although the word resistance is often used to describe the lower susceptibility of one species to a plant toxin when compared to another species, in this review we use the term tolerance for this differential toxicity. We reserve the term resistance to refer to a ‘genetically based decrease in susceptibility to a pesticide’ [9]. Resistance and tolerance are facets of a continuum, with similar molecular genetic mechanisms leading to similar biochemical and physiological phenotypic outcomes.

How strong is the evidence for the pre-adaptation hypothesis?

Rosenheim et al. examined [11] the evidence for the pre-adaptation hypothesis by literature-based comparative analyses and concluded that arthropods that feed on phloem or xylem (which are less strongly chemically defended than other tissues) had a lower incidence of resistance evolution than species feeding by chewing or sucking on cell contents. While these results supported the pre-adaptation hypothesis, Rosenheim et al. [11] warned that this correlation between feeding mode and resistance

Are the biochemical and physiological effectors the same?

It is clear that the targets, enzymes and transporters involved in host plant tolerance and pesticide resistance are basically the same. Targets for pesticides are predominantly neuroactive, favouring fast action [10] while plant compounds can often have slower effects on a more diverse array of targets [5, 7]. Some are exactly the same, for example, the nicotinic acetylcholine receptor is the receptor for the plant alkaloid nicotine and the synthetic neonicotinoid insecticides [16]. For both

Are the molecular genetic mechanisms the same?

Although there is a clear overlap among the enzymes and transporters, and to a lesser extent targets, involved in pesticide resistance and plant toxin tolerance, a comparison between the underlying molecular genetic mechanisms that are at play is more difficult to make. The molecular genetic mechanisms of insecticide resistance [6] can be categorized as three primary types of mutation that result in different outcomes on a resistance gene: Firstly, mutations affecting the coding sequence of the

Adaptive plasticity, transcriptional changes affecting the toxicity of chemicals

The ability of different host plants, specific plant chemicals, insecticides or more generally xenobiotics to affect expression levels of detoxification genes and hence the toxicity of pesticides (and vice versa) is well known [5, 18, 58]. Studies on induction of single or few genes have recently been overshadowed by more global approaches at the transcriptome level, for example, [21•, 51••, 59, 60, 61, 62, 63, 64, 65, 66, 67•]. It is important to note that inducibility of one or more genes,

Faster resistance evolution in generalists than specialists?

The dynamics of resistance evolution depend on three factors  genetic, biological/ecological and operational [71]. Most of these factors have been studied extensively in theory and practice but few studies have explicitly considered their relationship with monophagy/polyphagy. A greater genetic diversity has, in some cases, been attributed to generalists compared to specialists (e.g. [56]), and might result in a higher phenotypic variation available for selection to act.

Georghiou consistently

Conclusions

Despite the inherent attractiveness of the pre-adaptation hypothesis, the broad host range of generalist herbivores is neither necessary nor sufficient to drive the dynamics of pesticide resistance. Recent work indicates that some generalist herbivores have an expanded ‘defensome’ but other genetic, biological and operational factors (as defined by Georghiou and Taylor [71]) are likely to play a more predominant role in resistance development. In some cases, for example, M. persicae, resistance

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We gratefully acknowledge the great research value of the Arthropod Pesticide Resistance Database. We apologize in advance to all our colleagues whose publications we did not cite for lack of space. WD is a postdoctoral fellow of the Research Foundation Flanders (FWO, Belgium). This project was supported by NWO (The Netherlands) under the FACCE-JPI ERA-NET Plus framework (GENOMITE, project ID 137) and the Research Foundation Flanders (FWO, Belgium) (grant G009312N to TVL and grant G053815N to

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