Predation drives specialized host plant associations in preadapted milkweed bugs (Heteroptera: Lygaeinae)

Abstract

Host plant specialization across herbivorous insects varies dramatically, but the underlying evolutionary mechanisms are little-known. The milkweed bugs (Heteroptera: Lygaeinae) are ancestrally associated with plants of the Apocynaceae from which they commonly sequester cardiac glycosides for defense, facilitated by resistant Na+/K+-ATPases and adaptations for transport, storage and discharge of toxins. Here, we show that three Lygaeinae species independently colonized four novel non-apocynaceous hosts, convergently producing cardiac glycosides. A fourth species shifted to a new source of toxins by tolerating and sequestering alkaloids from meadow saffron (Colchicum autumnale, Colchicaceae). Across three species tested, feeding on seeds containing toxins did not improve growth, but sequestration mediated protection against predatory lacewing larvae and birds. We conclude that physiological preadaptations and convergent phytochemistry facilitated novel specialized host associations. Therefore, selection by predators on sequestration of defenses, rather than the exploitation of novel dietary resources, can lead to obligatory specialized host associations in generalist insects.