Trans-generational transcriptomic response to natural variation in host plant toxicity and insecticides in a specialist insect.

Abstract

Insects have been challenged by plant secondary metabolites throughout their evolutionary history. An important mechanism thought to promote insecticide resistance is the ability of insects to use preexisting detoxification systems originally evolved for tolerance of plant defenses. However, it remains unclear what level of convergence exists in metabolic mechanisms employed against various natural and xenobiotic chemicals? How do transcriptomic responses to these stressors change in response to novel and long-term exposure? We employ an experimental evolution approach in a milkweed- specialist aphid (Aphis nerii) model to test the effects of a more toxic host plant species and two insecticides commonly used in rotation in agriculture (a neonicotinoid, Imidacloprid, and a general homopteran blocker, Pymetrozine) on aphid gene expression and fitness over multiple generations of selection. Aphids were selected on three stress treatments: a toxic host plant species and two pesticides (Imidacloprid and Pymetrozine) for five generations. Whole transcriptome gene expression changes and changes in development time and fecundity were compared at generations one and five. While there were no consistent fitness costs or benefits to long-term exposure, exposure to stress is associated with increased transcriptional plasticity and changes in genes associated with the metabolism of secondary metabolites as well as genes important in transcription, translation, and post-translation processes.