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The phytophagous mite Tetranychus truncatus is a serious pest in East Asia but has a relatively narrower host range than the pest mite Tetranychus urticae, which can feed on over 1200 plant species. Here, we generated a high‐quality chromosomal level genome of T. truncatus and compared it with that of T. urticae, with an emphasis on the genes related to detoxification and chemoreception, to explore the genomic basis underlying the evolution of host range. We also conducted population genetics analyses (in 86 females from 10 populations) and host transfer experiments (in 4 populations) to investigate transcription changes following transfer to a low‐quality host (Solanum melongena, eggplant), and we established possible connections between fitness on eggplant and genes related to detoxification and chemoreception. We found that T. truncatus has fewer genes related to detoxification, transport, and chemoreception than T. urticae, with a particularly strong reduction in gustatory receptor (GR) genes. We also found widespread transcriptional variation among T. truncatus populations, which varied in fitness on eggplant. We characterized selection on detoxification‐related genes through ω values and found a negative correlation between expression levels and ω values. Based on the transcription results, as well as the fitness and genetic differences among populations, we identified genes potentially involved in adaptation to eggplant in T. truncatus. Our work provides a genomic resource for this pest mite and new insights into mechanisms underlying the adaptation of herbivorous mites to host plants. [ABSTRACT FROM AUTHOR]

Simple Summary: Many spider mites are important agricultural pests in both fields and greenhouses worldwide and are diversified in their host plant range. How spider mites perceive their suitable host plants remains not completely clear. In this study, we found that spider mites cannot locate suitable host plants by volatile odours from a long distance, but they can use olfactory sensation in combination with gustatory sensation to make a precise selection for suitable host plants at a short distance. Highly polyphagous species showed strong sensitivity in sensing suitable host plants rather than the expected lowered sensitivity. We also found that the similarity among the five spider mite species in their performance in perceiving suitable host plants was highly correlated with their relative phylogenetic relationship. Spider mites belonging to the genus Tetranychus infest many important agricultural crops in both fields and greenhouses worldwide and are diversified in their host plant range. How spider mites perceive their suitable host plants remains not completely clear. Here, through two-host-choice designs (bean vs. tomato, and bean vs. eggplant), we tested the efficacies of the olfactory and gustatory systems of five spider mite species (T. urticae, T. truncatus, T. pueraricola, T. piercei, and T. evansi), which differ in host plant range in sensing their suitable host plant, by Y-tube olfactometer and two-choice disc experiments. We found that spider mites cannot locate their suitable host plants by volatile odours from a long distance, but they can use olfactory sensation in combination with gustatory sensation to select suitable host plants at a short distance. Highly polyphagous species displayed strong sensitivity in sensing suitable host plants rather than the lowered sensitivity we expected. Intriguingly, our principal component analyses (PCAs) showed that the similarity among five spider mite species in the performance of perceiving suitable host plants was highly correlated with their relative phylogenetic relationships, suggesting a close relationship between the chemosensing system and the speciation of spider mites. Our results highlight the necessity of further work on the chemosensing system in relation to host plant range and speciation of spider mites. [ABSTRACT FROM AUTHOR]

The diet breadth of generalist herbivores when compared to specialists tends to be associated with greater transcriptional plasticity. Here, we consider whether it may also contribute to variation in host range among two generalists with different levels of polyphagy. We examined two related polyphagous spider mites with different host ranges, Tetranychus urticae (1200 plants) and Tetranychus truncatus (90 plants). Data from multiple populations of both species domesticated on common beans and transferred to new plant hosts (cotton, cucumber, eggplant) were used to investigate transcriptional plasticity relative to population‐based variation in gene expression. Compared to T. truncatus, T. urticae exhibited much higher transcriptional plasticity. Populations of this species also showed much more variable expression regulation in response to a plant host, particularly for genes related to detoxification, transport, and transcriptional factors. In response to the different plant hosts, both polyphagous species showed enriched processes of drug/xenobiotics metabolism, with T. urticae orchestrating a relatively broader array of biological pathways. Through co‐expression network analysis, we identified gene modules associated with host plant response, revealing shared hub genes primarily involved in detoxification metabolism when both mites fed on the same plants. After silencing a shared hub CYP gene related to eggplant exposure, the performance of both species on the original bean host improved, but the fecundity of T. truncatus decreased when feeding on eggplant. The extensive transcriptomic variation shown by T. urticae might serve as a potential compensatory mechanism for a deficiency of hub genes in this species. This research points to nuanced differences in transcriptomic variability between generalist herbivores. [ABSTRACT FROM AUTHOR]