Does a plant‐eating insect's diet govern the evolution of insecticide resistance? Comparative tests of the pre‐adaptation hypothesis

Abstract

According to the pre‐adaptation hypothesis, the evolution of insecticide resistance in plant‐eating insects co‐opts adaptations that initially evolved during chemical warfare with their host plants. Here, we used comparative statistics to test two predictions of this hypothesis: (i) Insects with more diverse diets should evolve resistance to more diverse insecticides. (ii) Feeding on host plants with strong or diverse qualitative chemical defenses should prime an insect lineage to evolve insecticide resistance. Both predictions are supported by our tests. What makes this especially noteworthy is that differences in the diets of plant‐eating insect species are typically ignored by the population genetic models we use to make predictions about insecticide resistance evolution. Those models surely capture some of the differences between host‐use generalists and specialists, for example, differences in population size and migration rates into treated fields, but they miss other potentially important differences, for example, differences in metabolic diversity and gene expression plasticity. Ignoring these differences could be costly.

When do herbivorous insects compete? A phylogenetic meta‐analysis

“…It could be because sap-feeders tend to reproduce rapidly and form dense and persistent aggregations on their hosts. Internal feeders also have persistent relationships with their hosts, but seldom reproduce as rapidly or form such dense aggregations (Ibbotson & Kennedy 1951;Hardy et al 2018). It could also be because the relatively poor diet of sap-feeders leaves them especially vulnerable to changes in host plant physiology (Hardy 2018).…”

“…This information was taken from Hardy et al . () (Supporting Information ). We also examined models in which diet breadth was a binary variable – that distinguished between specialists (one host plant family) and generalists (two or more host plant families).…”

Escalating insecticide resistance in Australian grain pests: contributing factors, industry trends and management opportunities

“…4), thus demonstrating the value of such approaches. Using a compiled data set on the biological traits of 902 arthropod species, Hardy et al 26 identified strong associations between diet breath and voltinism, and the propensity of a pest to evolve resistance (as well as the number of MoA groups to which resistance has evolved). Such approaches not only help to explain how resistance might evolve, but can promote resistance management of high-risk species before it evolves.…”

Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

“…Despite the considerable economic impact associated with these species, there is a lack of understanding as to how certain species evolve rapidly to agroecosystems (Chen and Schoville 2018). The organismal traits linked to pest success in agricultural environments remains open to debate, but could include pre-adaptive qualities such as: coevolution with chemically defensive plants, generalist herbivory behavior, high fecundity, high mutation rate, and short generation time (Dermauw et al 2013; Cingel et al 2016; Hardy et al 2017; Dermauw et al 2018). Additionally, due to contemporary genomic studies, certain features of species’ genomes appear advantageous to rapid evolution: elevated standing genetic diversity (Pearse et al, 2014; Lai et al, 2019), mutability linked to transposable elements (Baucom et al 2009; Ayarpadikannan and Kim 2014; Pereira and Ryan 2019), gene family diversification (Hahn et al 2007), and positive selection of regulatory and structural genes (Whitehead et al 2017).…”