Transfer to different host grapevines causes rapid and widespread transcriptional plasticity in the specialist insect Daktulosphaira vitifoliae

Insect herbivores employ many adaptive mechanisms to successfully colonize host plants. Transcriptional plasticity is one important mechanism that enables host use in polyphagous insects that maintain a broad host range. However, whether specialist herbivores also rely on transcriptional plasticity to feed successfully on different hosts remains largely unexplored. Here, we measure genome-wide transcriptional plasticity of grape phylloxera, Daktulosphaira vitifoliae , a grapevine ( Vitis spp.) specialist, after transfer onto different host grapevines for a single generation using RNA-seq. We show that the transcriptome of D. vitifoliae is highly plastic and responsive to host genotype – 4,820 genes (37% of the 12,876 expressed genes) are significantly differentially expressed in at least one contrast comparing host genotypes. Genes with functions related to host manipulation (predicted secretory effectors), cuticle and chitin, detoxification of xenobiotics, and development were enriched among host-responsive genes, with predicted secretory effectors being most strongly enriched (Fisher’s exact test odds ratio = 8.3, BH-adjusted p-value = 0). We further linked gene co-expression modules to D. vitifoliae fitness using weighted gene co-expression network analysis. The co-expression module most strongly correlated with fitness was enriched for predicted secretory effectors, including a novel group of proline-rich genes that exist as a tandem gene cluster. The only module negatively correlated with fitness was enriched for genes encoding glycoside hydrolase enzymes that function in carbohydrate metabolism. Overall, our results show that the phylloxerid transcriptome is highly plastic and rapidly reprogrammed when transferred onto distinct hosts, which may be an adaptive mechanism underlying host use in this clonally reproducing herbivore.