Monarch caterpillars are specialist herbivores on milkweed plants that contain toxic compounds called cardenolides. Monarchs have evolved resistance to the cardenolides, and actually use them as medicines. Specifically, the cardenolides in milkweed help to protect monarchs from infection by a protozoan parasite that otherwise reduces monarch lifespan and reproduction.

In the “From the Cover” paper in the Sept. 23, 2019 issue of Molecular Ecology, the authors asked whether reliance on medicinal milkweeds was related to the expression of immunity genes. They compared the evidence for two alternatives; that medicinal plants would boost the expression of native immunity or, in contrast, reduce the reliance of monarchs on typical immunity genes found in other insects. The authors conducted an experiment in which they fed monarch caterpillars on high- or low-cardenolide species of milkweed, both in the presence or absence of the protozoan parasite.

Intriguingly, the authors discovered that parasite infection alone caused very few changes in gene expression, suggesting that the monarchs do not mount a typical insect immune defense to infection.

“In stark contrast, monarchs fed on the high cardenolide diet differentially expressed hundreds of genes when compared with those on the low cardenolide diet,” said Mark Hunter, Earl E. Werner Distinguished University Professor of Ecology and Evolutionary Biology, one of the paper’s authors. “The genes that were differentially expressed were associated with detoxification. Overall, the results illustrate how heavily monarchs rely on the medicinal chemistry of their host plants to protect them from parasite infection, perhaps at the expense of a strong immune system.

"We expected that infection with the parasite would cause upregulation of immunity genes. That would be a typical animal response to parasite infection. Rather, infected monarch butterflies seem to rely very heavily on the natural medicines found in their milkweed host plants rather than on the expression of immunity genes. It really emphasizes the importance of conserving a diverse landscape of plant chemicals for the health of animal species like the monarch butterfly, which rely on pharmaceuticals in plants to combat their parasites."

Most of the authors are from the Department of Biology, Emory University, including first author Wen-Hao Tan and senior author Jacobus C. de Roode. Also among the collaborating institutions are the Department of Ecology and Evolutionary Biology University of Kansas and the Department of Ecosystem Science and Management, Pennsylvania State University, State College.

The article was the subject of a News and Views Perspective

Compiled by Gail Kuhnlein