The price of defence: toxins, visual signals and oxidative state in an aposematic butterfly

Abstract

SUMMARYIn a variety of aposematic species, the conspicuousness of an individual’s warning signal and the quantity of its chemical defence are positively correlated. This apparent honest signalling in aposematism is predicted by resource competition models which assume that the production and maintenance of aposematic defences compete for access to antioxidant molecules that have dual functions as pigments directly responsible for colouration and in protecting against oxidative lipid damage. Here we study a model aposematic system—the monarch butterfly (Danaus plexippus) and make use of the variable phytochemistry of its larval host-plant, milkweeds (Asclepiadaceae), to manipulate the concentration of sequestered cardenolides. We test two fundamental assumptions of resource competition models: that (1) the possession of secondary defences is associated with costs in the form of oxidative lipid damage and reduced antioxidant defences; and (2) that oxidative damage or decreases in antioxidant defences can reduce the capacity of individuals to produce aposematic displays. Monarch caterpillars that sequestered the highest concentrations of cardenolides exhibited higher levels of oxidative lipid damage as adults. The relationship between warning signals, cardenolide concentrations and oxidative damage differed between the sexes. In male monarchs conspicuousness was explained by an interaction between oxidative damage and sequestration: as males sequester more cardenolides, those with high levels of oxidative damage become less conspicuous, while those that sequester lower levels of cardenolides equally invest in conspicuous with increasing oxidative damage. There was no significant effect of oxidative damage or concentration of sequestered cardenolides on female conspicuousness. Our results demonstrate physiological linkage between the production of coloration and protection from autotoxicity, that warning signals can be honest indicators of defensive capability, and that the relationships are different between the sexes.