Milkweed butterfly resistance to plant toxins is linked to sequestration, not coping with a toxic diet

Abstract

Insect resistance to plant toxins is widely assumed to have evolved in response to using defended plants as a dietary resource. We tested this hypothesis in the milkweed butterflies (Danaini) which have progressively evolved higher levels of resistance to cardenolide toxins based on amino acid substitutions of their cellular sodium-potassium pump (Na Our data indicate that major adaptations to plant toxins may be evolutionarily linked to sequestration, and may not necessarily be a means to eat toxic plants. Na þ /K þ -ATPase adaptations thus were a potential mechanism through which predators spurred the coevolutionary arms race between plants and insects.

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

“…As expected (Malcolm, 1990(Malcolm, , 1994Agrawal et al, 2015;Petschenka and Agrawal, 2015), the concentration, diversity, polarity, and composition of cardenolides sequestered by aphids and caterpillars varied strongly among plant species, following plant species-specific differences in cardenolide expression (Table 2, PERMANOVA aphid: Plant species [F (2, 50) = 22.2694, P < 0.001]; caterpillar: Plant species [F (2, 110) = 98.086, P < 0.001]. For instance, aphids and caterpillars sequestered the highest cardenolide concentration and diversity, and most lipophilic (non-polar) cardenolides, when feeding upon the high cardenolide-containing A. curassavica and the least when feeding upon the low cardenolide-containing A. syriaca.…”

“…Oleander aphids appear to sequester cardenolides passively through diffusion of non-polar (lipophilic) cardenolides (Malcolm, 1990;Züst and Agrawal, 2016b). In contrast, monarch caterpillars sequester polar cardenolides selectively (Malcolm and Brower, 1989;Petschenka and Agrawal, 2015;Erb and Robert, 2016), likely through active translocation by transport proteins through gut membranes (Frick and Wink, 1995). Nonetheless, cardenolide sequestration by both oleander aphids and monarch caterpillars is closely correlated with their host plant cardenolides (Malcolm, 1990(Malcolm, , 1994Agrawal et al, 2015;Petschenka and Agrawal, 2015).…”

“…Oleander aphids tolerate cardenolides through regulation of a narrow set of genes involved in canonical detoxification processes (Birnbaum et al, 2017). Monarch caterpillars, in contrast, have NA + /K + -ATPases that are insensitive to cardenolides (Dobler et al, 2012;Petschenka and Agrawal, 2015). Despite being able to tolerate cardenolides, both oleander aphids and monarch caterpillars exhibit reduced performance on host plants with high concentrations of cardenolides (Zalucki et al, 2001a;Agrawal, 2004Agrawal, , 2005Rasmann et al, 2009;de Roode et al, 2011;Colvin et al, 2013;Tao et al, 2016b;Birnbaum et al, 2017).…”

“…The concentration and composition of secondary metabolites that herbivores sequester are tied closely with host plant secondary chemical profiles (Malcolm, 1990(Malcolm, , 1994Agrawal et al, 2015;Petschenka and Agrawal, 2015), and are affected by environmental factors, such as soil nutrient availability (Jamieson and Bowers, 2012;. Herbivores that sequester higher concentrations of secondary metabolites from their host plants are more toxic and deterrent to their natural enemies (Brower et al, 1968;Reichstein et al, 1968;Brower and Moffitt, 1974;Malcolm, 1992;Dyer and Bowers, 1996;Camara, 1997).…”

Host Plant Species Differentiation in a Polyphagous Moth: Olfaction is Enough

“…This strategy allows fine-tuned adaptation to the defence mechanisms of the host(s), such as observed in Asclepias-associated monarch butterflies, which have evolved an ability to sequester and tolerate cardenolides (Petschenka and Agrawal 2015). Specific adaptations are also observed in the host search behaviour and the olfactory system.…”