Differences in gene expression and genetic variation underlying preference-performance mismatches: insights from a specialized native herbivore on an invasive toxic plant.

Specialist phytophagous insects have a narrow hostplant range for optimal development and survival. Mismatches between female oviposition preference and larval performance can lead to high fitness costs. Understanding the mechanistic basis of this decoupling can help us understand evolutionary constraints and aid in predicting outcomes of error-prone oviposition. We investigated the causes for preference-performance mismatches in a specialist native herbivore laying eggs on an invasive toxic plant. Transcriptomic analyses revealed host-plant-specific gene expression signatures in larvae feeding on different plants, while there was no differential gene expression in gustatory/olfactory organs of adult females with different oviposition preferences. However, genomic analysis revealed significant genetic differentiation in several genes underlying signal transduction in adult females with different oviposition preferences. The larvae feeding on toxic plants showed lower expression of specialized detoxification enzymes and higher expression of general digestive enzymes, indicating the inability of larvae to detoxify toxic compounds present in the toxic plants. We additionally found that genes related to successful detoxification and adaptive feeding were enriched in larvae feeding on native plants, while genes related to toxic responses, apoptosis, and accelerated development were enriched in larvae feeding on toxic plants. Our findings dissect the underlying mechanisms behind a preference-performance mismatch, quantifying the impact of error-prone oviposition on larval performance in a specialized species interaction.