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J Chem Ecol. 2019 Mar;45(3):264-277. doi: 10.1007/s10886-019-01055-7. Epub 2019 Feb 22.

Cardenolide Intake, Sequestration, and Excretion by the Monarch Butterfly along Gradients of Plant Toxicity and Larval Ontogeny.

Author information

1
Department of Biology, Bowdoin College, Brunswick, ME, USA. pjones3@bowdoin.edu.
2
Institute for Insect Biotechnology, Justus-Liebig-Universit├Ąt Giessen, Giessen, Germany.
3
Department for Structural Infection Biology, Centre for Structural Systems Biology, Hamburg, Germany & Helmholtz-Centre for Infection Research, Braunschweig, Germany.
4
Heinrich Pette Institute, Leibniz Institute for Experimental Virology, Hamburg, Germany.
5
Department of Ecology & Evolutionary Biology, Cornell University, Ithaca, NY, USA.
6
Department of Entomology, Cornell University, Ithaca, NY, USA.

Abstract

Monarch butterflies, Danaus plexippus, migrate long distances over which they encounter host plants that vary broadly in toxic cardenolides. Remarkably little is understood about the mechanisms of sequestration in Lepidoptera that lay eggs on host plants ranging in such toxins. Using closely-related milkweed host plants that differ more than ten-fold in cardenolide concentrations, we mechanistically address the intake, sequestration, and excretion of cardenolides by monarchs. We show that on high cardenolide plant species, adult butterflies saturate in cardenolides, resulting in lower concentrations than in leaves, while on low cardenolide plants, butterflies concentrate toxins. Butterflies appear to focus their sequestration on particular compounds, as the diversity of cardenolides is highest in plant leaves, lower in frass, and least in adult butterflies. Among the variety of cardenolides produced by the plant, sequestered compounds may be less toxic to the butterflies themselves, as they are more polar on average than those in leaves. In accordance with this, results from an in vitro assay based on inhibition of Na+/K+ ATPase (the physiological target of cardenolides) showed that on two milkweed species, including the high cardenolide A. perennis, extracts from butterflies have lower inhibitory effects than leaves when standardized by cardenolide concentration, indicating selective sequestration of less toxic compounds from these host plants. To understand how ontogeny shapes sequestration, we examined cardenolide concentrations in caterpillar body tissues and hemolymph over the course of development. Caterpillars sequestered higher concentrations of cardenolides as early instars than as late instars, but within the fifth instar, concentration increased with body mass. Although it appears that large amounts of sequestration occurs in early instars, a host switching experiment revealed that caterpillars can compensate for feeding on low cardenolide host plants with substantial sequestration in the fifth instar. We highlight commonalities and striking differences in the mechanisms of sequestration depending on host plant chemistry and developmental stage, which have important implications for monarch defense.

KEYWORDS:

Asclepias; Cardiac glycoside; Caterpillar developmental stage; Danaus plexippus; Milkweed; Plant-insect interactions; Sequestration; Sodium-potassium ATPase

PMID:
30793231
DOI:
10.1007/s10886-019-01055-7
[Indexed for MEDLINE]

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