Genomes of Two Monophagous Weevils and Their Host Plant Provide Insights Into Evolution of Plant Defence and Insect Counter-Defence

Plant secondary metabolites play important roles in defence against herbivorous insects. However, many insects can overcome plant defences even when they produce a rich toxin load, and an arms race between plants evolving new toxins and insects evolving to counter them is expected. Here, we deciphered genomic features linked to a potential race between the tree of heaven and two monophagous weevils that only feed on this tree species, with the tree of heaven producing a rich set of secondary metabolites involving about 745 compounds. We first assembled chromosome-level genomes for the tree of heaven and the two weevils. Comparative genomics showed an expansion of genes related to synthesising secondary metabolites in the tree, while in the weevils, genes related to detoxification and chemosensing expanded. The expansion of core genes involved in quassinoid biosynthesis in the tree was linked to tandem duplication and whole genome duplication, while the expansion of detoxifying GST and chemosensing SNMP genes in the two weevils was linked to tandem duplication and novel genes, respectively. The results indicate that plants and insect herbivores both reshaped their genomes through gene expansion, while the host tree also underwent whole genome duplication and the two weevils evolved novel genes. These changes likely reflect an arms race of defence and counter-defence, providing an understanding of genome evolution driven by trophic interactions.