Convergent resistance to GABA receptor neurotoxins through plant-insect coevolution

Antagonistic coevolution of plants and insects is hypothesized to promote biological diversity. This study shows convergent evolution of a gene that encodes the GABA receptor, a target of plant toxins, in herbivorous insects and their predators. It further demonstrates that the evolution of resistant GABA receptors is associated with insect diversification. The molecular mechanisms of coevolution between plants and insects remain elusive. GABA receptors are targets of many neurotoxic terpenoids, which represent the most diverse array of natural products known. Over deep evolutionary time, as plant terpene synthases diversified in plants, so did plant terpenoid defence repertoires. Here we show that herbivorous insects and their predators evolved convergent amino acid changing substitutions in duplicated copies of the Resistance to dieldrin (Rdl) gene that encodes the GABA receptor, and that the evolution of duplicated Rdl and terpenoid-resistant GABA receptors is associated with the diversification of moths and butterflies. These same substitutions also evolved in pests exposed to synthetic insecticides that target the GABA receptor. We used in vivo genome editing in Drosophila melanogaster to evaluate the fitness effects of each putative resistance mutation and found that pleiotropy both facilitates and constrains the evolution of GABA receptor resistance. The same genetic changes that confer resistance to terpenoids across 300 Myr of insect evolution have re-evolved in response to synthetic analogues over one human lifespan.

Automated summary

This study reveals the convergent evolution of a gene encoding the GABA receptor in herbivorous insects and their predators. It also suggests that the evolution of resistant GABA receptors is linked to the diversification of insects. The molecular mechanisms of coevolution between plants and insects remain elusive.