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

Abstract

In 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. To test for such trade-offs, we raised monarch butterflies ( Danaus plexippus ) on different species of their milkweed host plants (Apocynaceae) that vary in quantities of cardenolides to test whether (i) the sequestration of cardenolides as a secondary defence is associated with costs in the form of oxidative lipid damage and reduced antioxidant defences; and (ii) lower oxidative state is associated with a reduced capacity 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 became less conspicuous with increased sequestration of cardenolides, whereas those with low oxidative damage became 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 oxidative state, and differential costs of sequestration and signalling in monarch butterflies.

Diet influences resource allocation in chemical defence but not melanin synthesis in an aposematic moth

“…Phenotypic variation in aposematic signals is puzzling because predators avoid defended prey that are common but attack rarer ones (Müller 1878). Trade-offs in resource allocation have been suggested to account for some of the variation found in natural aposematic populations (Wang, 2011; Burdfield-Steel et al, 2019; Blount et al, 2023). However, the phenotypic correlations between primary and secondary defences do not necessarily prove this connection, as interactions between such complex traits can be shaped by genetic correlations, pleiotropic effects or simply variable environmental conditions (e.g., food availability, environmental stochasticity, presence of predators).…”

“…A study on the Asian lady beetle, Harmonia axyridis , found no phenotypic correlation between the reflex bleeding response (frequency of secretion of the defensive chemicals) and the beetle colouration, even though reflex bleeding is costly and affects life-history traits (Grill and Moore, 1998). Recent work on monarch butterflies Danaus plexippus showed a link between toxin sequestration and warning signals, with male conspicuousness inversely correlated with oxidative damage (due to an increase in concentrations of sequestered cardenolides) (Blount et al, 2023). Previous work by Lindstedt et al, (2010) showed that the aposematic, generalist herbivore Arctia plantaginis (hereafter referred to as the wood tiger moth) develops a paler, orange warning signal when reared on Plantago lanceolata with high concentrations of iridoid glycosides (IG) compared to the more conspicuous, dark red warning signal of individuals fed on a strain of the same plant with low concentrations of IG.…”

Antioxidant availability trades off with warning signals and toxin sequestration in the large milkweed bug (Oncopeltus fasciatus)

“…In Blount et al's ( 2009 ) resource competition framework, pigments that are used in prey warning signals play a role both in producing the signal and in preventing self‐damage when storing toxins (due to their antioxidant properties). When antioxidants are required to enable high levels of toxicity, then the most toxic species are predicted to be the most conspicuous because they gain access to more antioxidants (or are genetically disposed to produce more), than those that are less bright and less toxic (see figure 1 in Blount et al, 2023 ). There are many critiques of the idea that warning signals are costly, one of which is that it is unclear whether warning signals ‘use up’ resources that are needed to produce chemical defenses (Guilford & Dawkins, 1993 ).…”

“…There are many critiques of the idea that warning signals are costly, one of which is that it is unclear whether warning signals ‘use up’ resources that are needed to produce chemical defenses (Guilford & Dawkins, 1993 ). The potential influence of antioxidant availability and oxidative stress on the development of aposematic displays has received limited empirical attention (Ojala et al, 2005 ; Sandre et al, 2007 ), though Blount et al ( 2023 ) found that monarch butterflies ( Danaus plexippus ) that sequestered higher concentrations of chemical defense experienced higher levels of oxidative damage, and monarchs with lower oxidative damage allocated more resources to color and toxicity than monarchs with higher oxidative damage. Because Blount et al ( 2023 ) reared monarchs on different milkweed hostplants ( Apocynaceae ) to manipulate the amounts of toxins the butterflies sequestered, and because different hostplants vary in many traits (not just chemical defense), the costs that Blount et al ( 2023 ) detect may not result only from varied sequestration.…”

“…The potential influence of antioxidant availability and oxidative stress on the development of aposematic displays has received limited empirical attention (Ojala et al, 2005 ; Sandre et al, 2007 ), though Blount et al ( 2023 ) found that monarch butterflies ( Danaus plexippus ) that sequestered higher concentrations of chemical defense experienced higher levels of oxidative damage, and monarchs with lower oxidative damage allocated more resources to color and toxicity than monarchs with higher oxidative damage. Because Blount et al ( 2023 ) reared monarchs on different milkweed hostplants ( Apocynaceae ) to manipulate the amounts of toxins the butterflies sequestered, and because different hostplants vary in many traits (not just chemical defense), the costs that Blount et al ( 2023 ) detect may not result only from varied sequestration. A study that varies chemical defense content while holding other traits constant could provide a clearer test for a mechanistic link between oxidative stress, warning colors, and sequestration of chemical defenses.…”