Evidence for tissue-specific defence-offence interactions between milkweed and its community of specialized herbivores

Coevolution between plants and herbivores often involves escalation of defence-offence strategies, but attack by multiple herbivores may obscure the match of plant defence to any one attacker. As herbivores often specialize on distinct plant parts, we hypothesized that defence-offence interactions in coevolved systems may become physiologically and evolutionarily compartmentalized between plant tissues. We report that roots, leaves, flower buds and seeds of the tropical milkweed (Asclepias curassavica) show increasing concentrations of cardenolide toxins acropetally, with latex showing the highest concentration. In vitro assays of the physiological target of cardenolides, the Na+/K+-ATPase (hereafter sodium pump), of three specialized milkweed herbivores (root-feeding Tetraopes tetrophthalmus, leaf-feeding Danaus plexippus, and seed-feeding Oncopeltus fasciatus) show that they are proportionally tolerant to the cardenolide concentrations of the tissues they eat. Indeed, molecular substitutions in the insects' sodium pumps predicted their tolerance to toxins from their target tissues. Nonetheless, the relative inhibition of the sodium pumps of these specialists by the concentration versus composition (inhibition controlled for concentration, what we term potency) of cardenolides from their target versus nontarget plant tissues revealed different degrees of insect adaptation to tissue-specific toxins. In addition, a trade-off between toxin concentration and potency emerged across plant tissues, potentially reflecting coevolutionary history or plant physiological constraints. Our findings suggest that tissue-specific coevolutionary dynamics may be proceeding between the plant and its specialized community of herbivores. This novel finding may be common in nature, contributing to ways in which coevolution proceeds in multispecies communities.

Automated summary

The coevolution between plants and herbivores often involves the escalation of defence-offence strategies. This study found that different tissues of the tropical milkweed have increasing concentrations of toxins, and specialized herbivores show proportionate tolerance to these toxins. However, there are variations in insect adaptation to tissue-specific toxins. These findings suggest the presence of tissue-specific coevolutionary dynamics between the plant and its specialized herbivores.