A central problem in ecology and evolution is to understand the extent to which herbivorous insect host plant specialization has been shaped by bottom-up natural selection from host-plant chemical defenses or top-down natural selection from natural enemies. Here, we show that the stepwise evolution of ATP target-site insensitivity (TSI) in the monarch butterfly lineage consistently tracked a dietary association with cardenolide-defended Asclepias host plants. We further show that Drosophila melanogaster flies edited with CRISPR-Cas9 genome engineering to carry the monarch butterfly's more derived ATP genotype maintain survival across Asclepias host-plant diets that span a broad cardenolide defense gradient, whereas flies carrying early-diverging ATP genotypes in the monarch lineage show lower survival. We conclude that a resistance trait linked to sequestration and enemy protection also expanded dietary resistance to highly defended host plants, revealing how a single molecular adaptation may have been driven by both top-down and bottom-up selective pressures during herbivore specialization.
Weksler, N., Astourian, M., Yip, D., Ordeman, E., Verster, K., Korablev, B., Bernstein, S., Agrawal, A. A., Whiteman, N. K., Karageorgi, M.
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