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.

Host-specific gene expression as a tool for introduction success inNaupactusparthenogenetic weevils

“…This upregulation may indicate that the host plant defenses of organically treated oranges are more stressful for herbivores than those of conventionally treated oranges. Similar results have been proposed as a clear link between exposure to stress and increased transcriptional plasticity, including regulation of transcription and translation processes (43).…”

“…There was a notable overlap in the number of shared DEGs for host detection, detoxification and immune defense genes between Legume vs. Other and farming method comparisons (Fig 3). A greater degree of transcriptional plasticity and changes in genes associated with the metabolism of secondary compounds has been found as a response to exposure to stress in some aphids and other specialist insects (43, 50). The evolution of a conserved mechanism for both more toxic host plants and exposure to other forms of stress would be the least evolutionarily costly (51), and would be especially beneficial for this polyphagous species.…”

“…It is entirely possible that important aspects of weevil acclimation and/or adaptation to feeding on resource-taxing host plants, or on novel hosts, may involve differential regulation of genes beyond the three targeted gene categories of detection, detoxification and immune response. For example, a plastic response, as measured by a wider array of upregulated gene sets, was recorded in milkweed aphids feeding on novel host plants (43), and specific gene expression response trajectories were elicited in response to different sugar-mimic alkaloids in silk moths (44).…”

Host-specific gene expression as a tool for introduction success in Naupactus parthenogenetic weevils

“…It is entirely possible that important aspects of weevil acclimation and/or adaptation to feeding on resource-taxing host plants, or on novel hosts, may involve differential regulation of genes beyond the three targeted gene categories of detection, detoxification and immune response. For example, a plastic response, as measured by a wider array of upregulated gene sets, was recorded in milkweed aphids feeding on novel host plants [44], and specific gene expression response trajectories were elicited in response to different sugar-mimic alkaloids in silk moths [45]. Other studies on herbivore transcriptional plasticity at the gene set level frequently identify categories associated with metabolic processes, transporter activity, digestion, membrane structure, and reproduction [46].…”

“…There was a notable overlap in the number of shared DEGs for host detection, detoxification and immune defense genes between Legume vs. Other and farming method comparisons (Fig 3 ). A greater degree of transcriptional plasticity and changes in genes associated with the metabolism of secondary compounds has been found as a response to exposure to stress in some aphids and other specialist insects [44,55]. The evolution of a conserved mechanism for both more toxic host plants and exposure to other forms of stress would be the least evolutionarily costly [56], and would be especially beneficial for this polyphagous species.…”