Significance: Interactions between plants and herbivores constitute a major pathway of energy transfer up the food chain. As a consequence, evolution by natural selection has honed the chemically mediated antagonistic interactions between these groups. Monarch butterflies and milkweeds serve as royal representatives in deciphering such coevolution, and our study takes a mechanistic and manipulative approach to understand how the tropical milkweed, Asclepias curassavica , defends itself against monarch butterflies, which would seem to be impervious feeders. By directly observing plant–herbivore interactions and coupling this with experiments on isolated toxins and the monarch’s neural sodium-potassium pump enzymes, we show that tropical milkweed produces a burdensome cardenolide toxin, and monarchs convert it to less toxic compounds, the latter sequestered for their own benefit.

Environmental clines in organismal defensive traits are usually attributed to stronger selection by enemies at lower latitudes or near the host’s range center. Nonetheless, little functional evidence has supported this hypothesis, especially for coevolving plants and herbivores. We quantified cardenolide toxins in seeds of 24 populations of common milkweed ( Asclepias syriaca ) across 13 degrees of latitude, revealing a pattern of increasing cardenolide concentrations toward the host's range center. The unusual nitrogen-containing cardenolide labriformin was an exception and peaked at higher latitudes. Milkweed seeds are eaten by specialist lygaeid bugs that are even more tolerant of cardenolides than the monarch butterfly, concentrating most cardenolides (but not labriformin) from seeds into their bodies. Accordingly, whether cardenolides defend seeds against these specialist bugs is unclear. We demonstrate that Oncopeltus fasciatus (Lygaeidae) metabolized two major compounds (glycosylated aspecioside and labriformin) into distinct products that were sequestered without impairing growth. We next tested several isolated cardenolides in vitro on the physiological target of cardenolides (Na ⁺ /K ⁺ -ATPase); there was little variation among compounds in inhibition of an unadapted Na ⁺ /K ⁺ -ATPase, but tremendous variation in impacts on that of monarchs and Oncopeltu s. Labriformin was the most inhibitive compound tested for both insects, but Oncopeltus had the greater advantage over monarchs in tolerating labriformin compared to other compounds. Three metabolized (and stored) cardenolides were less toxic than their parent compounds found in seeds. Our results suggest that a potent plant defense is evolving by natural selection along a geographical cline and targets specialist herbivores, but is met by insect tolerance, detoxification, and sequestration.

ISHS International Postharvest Science Conference Postharvest 96 INFLUENCE OF POSTHARVEST CURING TREATMENT ON THE SYNTHESIS OF THE VOLATILE FLAVOR COMPONENTS IN SWEETPOTATO