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Toxin sequestration of milkweed insects and inhibition of their sodium pump constructs

Agrawal, Anurag1; Dobler, Susanne2

Published Mar 19, 2024; Updated Mar 25, 2024 on Dryad. https://doi.org/10.5061/dryad.1zcrjdg0n

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Mar 19, 2024 version files 74.14 KB
Mar 25, 2024 version files 74.94 KB
Mar 25, 2024 version files 75.64 KB

Abstract

Repeatable macroevolutionary patterns provide hope for rules in biology, especially when we can decipher the underlying mechanisms. Here we synthesize natural history, genetic adaptations, and toxin sequestration in herbivorous insects that specialize on plants with cardiac glycoside defenses. Work on the monarch butterfly provided a model for evolution of the sequestering specialist syndrome, where specific amino acid substitutions in the insect’s Na+/K+-ATPase are associated with 1) high toxin-resistance (target site insensitivity, TSI), 2) sequestration of toxins, and 3) aposematic coloration. We evaluate convergence for these traits within and between Lepidoptera, Coleoptera, Diptera, Hemiptera, Hymenoptera and Orthoptera, encompassing hundreds of toxin-adapted species. Using new and existing data on ~28 origins of specialization, we show that the monarch model evolved independently in five taxonomic orders (but not Diptera). An additional syndrome occurs in five orders: aposematic sequesterers with modest to medium TSI (all but Hymenoptera). Indeed, all sequestering species were aposematic and all but one had at least modest TSI. Additionally, several species were aposematic non-sequesterers (potential Batesian mimics), and this combination evolved in species with a range of TSI levels. Finally, we identified some biases among these strategies within taxonomic orders. Biodiversity in this microcosm of life evolved repeatedly with a high degree of similarity across six taxonomic orders, yet we identified alternative trait combinations as well as lineage-specific outcomes.