Plant defense responses against insect herbivores are induced through wound-induced signaling and the specific perception of herbivore-associated molecular patterns (HAMPs). In addition, herbivores can deliver effectors that suppress plant immunity. Here we review plant immune recognition of HAMPs and effectors, and argue that these initial molecular interactions upon a plant–herbivore encounter mediate and structure effective resistance. While the number of distinct HAMPs and effectors from both chewing and piercing–sucking herbivores has expanded rapidly with omics-enabled approaches, paired receptors and targets in the host are still not well characterized. Herbivore-derived effectors may also be recognized as HAMPs depending on the host plant species, potentially through the evolution of novel immune receptor functions. We compile examples of HAMPs and effectors where natural variation between species may inform evolutionary patterns and mechanisms of plant–herbivore interactions. Finally, we discuss the combined effects of wounding and HAMP recognition, and review potential signaling hubs, which may integrate both sensing functions. Understanding the precise mechanisms for plant sensing of herbivores will be critical for engineering resistance in agriculture.

Pesticide resistance arises rapidly in arthropod herbivores, as can host plant adaptation, and both are significant problems in agriculture. These traits have been challenging to study as both are often polygenic and many arthropods are genetically intractable. Here, we examined the genetic architecture of pesticide resistance and host plant adaptation in the two-spotted spider mite, Tetranychus urticae, a global agricultural pest. We show that the short generation time and high fecundity of T. urticae can be readily exploited in experimental evolution designs for high-resolution mapping of quantitative traits. As revealed by selection with spirodiclofen, an acetyl-CoA decarboxylase inhibitor, in populations from a cross between a spirodiclofen resistant and a susceptible strain, and which also differed in performance on tomato, we found that a limited number of loci could explain quantitative resistance to this compound. These were resolved to narrow genomic intervals, suggesting specific candidate genes, including acetyl-CoA decarboxylase itself, clustered and copy variable cytochrome P450 genes, and NADPH cytochrome P450 reductase, which encodes a redox partner for cytochrome P450s. For performance on tomato, candidate genomic regions for response to selection were distinct from those responding to the synthetic compound and were consistent with a more polygenic architecture. In accomplishing this work, we exploited the continuous nature of allele frequency changes across experimental populations to resolve the existing fragmented T. urticae draft genome to pseudochromosomes. This improved assembly was indispensable for our analyses, as it will be for future research with this model herbivore that is exceptionally amenable to genetic studies.

Significance: Honey bees pollinate the majority of crops, but their survival is under threat. The bee parasitic mite Varroa destructor is a major cause of honey bee decline. The successful control of Varroa mites depends on a small number of in-hive acaricides. Species-specific activation of the chemical coumaphos is a powerful “pro-drug” approach to attain this selective toxicity and protect bees. We identified a coumaphos-resistant Varroa population that escapes toxicity by down-regulating the activating enzyme, a P450 monooxygenase. Decreased activation is a rare but evolutionarily powerful solution to achieve resistance. It demonstrates that the current proinsecticide approach is under threat, as it can be circumvented, and highlights the need to restart the pipeline to develop selective pest control agents.