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 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 and in protecting against oxidative damage. We raised monarch butterflies (Danaus plexippus) on their milkweed host-plants (Apocynaceae) with increasing quantities of cardenolides to test whether (1) the sequestration of secondary defences is associated with costs in the form of oxidative lipid damage and reduced antioxidant defences; and (2) that reduced oxidative state can decrease the capacity of individuals to produce aposematic displays. In male monarchs conspicuousness was explained by an interaction between oxidative damage and sequestration: males with high levels of oxidative damage become less conspicuous with increased sequestration of cardenolides, whereas those with low oxidative damage become more conspicuous with increased levels of cardenolides. There was no significant effect of oxidative damage or concentration of sequestered cardenolides on female conspicuousness. Our results demonstrate a physiological linkage between the production of coloration and protection from autotoxicity, and differential costs of signalling in monarch butterflies.