North American horned lizards of the genus Phrynosoma are largely myrmecophagous and squirt systemic blood from circumocular sinuses during encounters with certain mammalian predators. The predators react with distinct revulsion. Using bioassay-guided fractionation of blood plasma, we endeavored to identify the source and characteristics of the active chemical compound(s) responsible for this negative oral response. Our results of coyote bioassays and a series of novel mouse bioassay experiments were largely concordant. The active compound(s) was likely plasma-borne with a molecular weight (mw) of between 800 and 1,600. To identify the source of the active compound(s), we noted bioassay responses of different species of horned lizards. The active compound(s) was present in plasma fractions of species known to eat Pogonomyrmex and squirt blood, and it was absent in the plasma fractions of species that do not squirt blood and eat other ants or arthropods. Plasma fractions from individuals of P. cornutum, a blood-squirting species, fed Pogonomyrmex had more aversive levels of the active compound(s) compared to those given a cricket diet. In addition, extracts from Pogonomyrmex indicate that the active compound(s) in lizard plasma is associated with the abdomen of these ants, where venom is stored. The toxic enzymes of ant venom may be metabolized by horned lizards resulting in one or more small peptides that act as the active ingredient(s) in the lizard’s circulating blood. We suggest that utilization of this widely dispersed, venomous, and abundant diet only became available to stem horned lizards with the evolution of unique prey capture techniques. This broadened diet then led to incorporation of the compound(s) from Pogonomyrmex spp. into their blood plasma, facilitating the evolution of antipredator blood-squirting. These transformative events apparently established an evolutionarily stable configuration that led to or expanded the unique “Phrynosoma suite” of characteristics from which subsequent diverse clades have evolved across arid North America.

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