Dietary cardenolides enhance growth and change the direction of the fecundity-longevity trade-off in milkweed bugs (Heteroptera: Lygaeinae)

Abstract

1. Sequestration, i.e., the accumulation of plant toxins into body tissues for defence, is primarily observed in specialised insects. Sequestration was frequently predicted to incur a physiological cost mediated by increased exposure to plant toxins and may require resistance traits different from those of non-sequestering insects. Alternatively, sequestering species could experience a cost in the absence of toxins due to selection on physiological homeostasis under permanent exposure of sequestered toxins in body tissues. 2. Milkweed bugs (Heteroptera: Lygaeinae) sequester high amounts of plant-derived cardenolides. Although being potent inhibitors of the ubiquitous animal enzyme Na+/K+-ATPase, milkweed bugs can tolerate cardenolides by means of resistant Na+/K+-ATPases. Both adaptations, resistance and sequestration, are ancestral traits shared by most species of the Lygaeinae. 3. Using four milkweed bug species and the related European firebug (Pyrrhocoris apterus) showing different combinations of the traits ′cardenolide resistance′ and ′cardenolide sequestration′, we set out to test how the two traits affect larval growth upon exposure to dietary cardenolides in an artificial diet system. While cardenolides impaired the growth of P. apterus nymphs neither possessing a resistant Na+/K+-ATPase nor sequestering cardenolides, growth was not affected in the non-sequestering milkweed bug Arocatus longiceps, which possesses a resistant Na+/K+-ATPase. Remarkably, cardenolides increased growth in the sequestering dietary specialists Caenocoris nerii and Oncopeltus fasciatus but not in the sequestering dietary generalist Spilostethus pandurus, which all possess a resistant Na+/K+-ATPase. 4. We then assessed the effect of dietary cardenolides on additional life history parameters, including developmental speed, the longevity of adults, and reproductive success in O. fasciatus. Remarkably, nymphs under cardenolide exposure developed substantially faster and lived longer as adults. However, fecundity of adults was reduced when maintained on cardenolide-containing diet for their entire life-time but not when adults were transferred to non-toxic sunflower seeds. 5. We speculate that the resistant Na+/K+-ATPase of milkweed bugs is selected for working optimally in a ′toxic environment′, i.e. when sequestered cardenolides are stored in the body tissues. Contrary to the assumption that toxins sequestered for defence produce a physiological burden, our data suggest that they can even increase fitness in specialised insects.

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

“…However, it is methodologically difficult to separate the costs of sequestration from the potential effects of other plant defences and nutrient availability that vary between milkweed species [22,64]. Future work could focus on comparative phytochemical profiles to understand resource availability, and experiments that control nutritional content while manipulating toxin content [65].…”

Condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly

“…Handling/detoxifying of defensive compounds in its plant diet also comes at a cost to developmental traits and warning signal expression (Lindstedt et al, 2010; Reudler et al, 2015). Similarly, the fecundity of cardenolide‐sequestering Oncopeltus fasciatus milkweed bugs was reduced when constantly artificially maintained on cardenolide‐containing diet, although in general, cardenolide exposure was associated with positive fitness effects (Pokharel et al, 2021). In the gregarious social Diprion pini pine sawfly, increased allocation to defensive secretion incurs costs in growth, immunity, and survival (Björkman & Larsson, 1991; Lindstedt et al, 2018), and in the pipevine swallowtail ( Battus philenor ) butterfly, toxin content is negatively correlated with fat content (Fordyce & Nice, 2008).…”

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

“…However, it is methodologically difficult to separate the costs of sequestration from other potential effects of plant allelochemicals [56]. Future work could focus on comparative phytochemical profiles to understand resource availability, and experiments that control nutritional content while manipulating toxin content [57].…”