Transcriptomic divergences of larval labial salivary glands facilitate host-plant range oscillations between specialist and generalist Helicoverpa species.

Host plant range of insect herbivores may evolve towards generalization and specialization. However, how generalist herbivores achieve polyphagy and what facilitate host-plant range oscillation remains elusive. Our recent finding of a negative correlation between host-plant range and genome size in the Helicoverpa lineage predicts that the generalist Helicoverpa armigera, rather than its ancestral specialist sibling Helicoverpa assulta, should have a larger secretome size to modify host defenses, nutrients and/or structure, and should purge a significant amount of transposable elements (TEs) to minimize pseudogenization of genes associated with host utilization. To test these two predictions, we compared the sizes and compositions of the larval labial salivary gland transcriptomes of these two species, as well as the numbers of pseudogenes in four host defense detoxification gene families in their genomes. Indeed, the labial salivary gland transcriptome of H. armigera was significantly greater than that of H. assulta at both the contig and gene levels, especially for the Gene Ontology (GO) terms and KEGG pathways associated the main functions of the larval salivary gland, such as protein synthesis and secretion, herbivore offence, digestion, detoxification. By contrast, H. assulta had more contigs inserted with TEs, more transcripts involved in transposition of TEs, and more pseudogenized host defense detoxification genes. These results not only match the predictions but also demonstrate that oscillation of host plant range evolution in Helicoverpa species is at least in part facilitated by TE-mediate pseudogenization (shutdown) and reactivation (on) of host use and secretion-related genes.