Venom exaptation and adaptation during the trophic switch to blood-feeding by kissing bugs

Kissing bugs are known to produce anticoagulant venom that facilitates blood-feeding. However, it is unknown how this saliva evolved and if the venom produced by the entomophagous ancestors of kissing bugs would have helped or hindered the trophic shift. In this study, we show that venoms produced by extant predatory assassin bugs have strong anticoagulant properties mediated chiefly by proteolytic degradation of fibrinogen, and additionally contain anticoagulant disulfide-rich peptides. However, venom produced by predatory species also has pain-inducing and membrane-permeabilizing activities that would be maladaptive for blood-feeding, and which venom of the blood-feeding species lack. This study demonstrates that venom produced by the predatory ancestors of kissing bugs was exapted for the trophic switch to blood-feeding by virtue of its anticoagulant properties. Further adaptation to blood-feeding occurred by downregulation of venom toxins with proteolytic, cytolytic, and pain-inducing activities, and upregulation and neofunctionalization of toxins with anticoagulant activity independent of proteolysis.