Gut-specific cardenolide-resistant sodium pump primed an omnivore to feed on toxic oleander

Apocynaceae plants produce toxic cardenolides to defend against their herbivores. Cardenolides could inhibit the α subunit of Na⁺⁄K⁺-ATPase (ATPα), which plays critical roles in biological processes such as muscle contraction, neural function, and osmoregulation. Numerous herbivores that specialized on cardenolides-producing milkweeds carry parallel molecular changes in ATPα that confer resistance. We found that Pacific Ducetia (Ducetia japonica), an omnivorous katydid, could feed on cardenolides-rich oleander leaves. ATPα in D. japonica has undergone parallel molecular changes just like milkweed specialists. These changes evolved at the common ancestors of the leaf katydids before the diversification of Apocynaceae and may prime species in this lineage to feed on cardenolides-rich food. In summary, we reported the first case of cardenolide resistance in katydid, with convergent molecular evolution in ATPα, also an unusual case of cardenolides resistance in nonspecialist species that evolved earlier than the currently known cardenolide-producing plants.