Evolutionary significance of phytochemical diversity:Cardenolides as a model system
Final Report Abstract
The coevolutionary arms race between herbivorous insects and their host plants is considered to generate much of the biodiversity seen on earth and it is widely assumed that plant toxins are a major evolutionary driver of plant-insect interactions. Plants typically produce a great structural diversity of chemically related toxins but the adaptive significance of this "phytochemical diversity" is not well understood. During my research fellowship I used milkweeds (Asclepias, Apocynaceae) producing various cardenolides and caterpillars of the monarch butterfly (Danaus plexippus) to address the effect of phytochemical diversity on a specialized insect herbivore. Cardenolides are highly toxic inhibitors of animal Na+/K+-ATPase and monarch butterflies are known to possess a Na+/K+-ATPase with increased cardenolide resistance. Monarchs moreover store cardenolides from its milkweed hosts as a defense against predators (sequestration). Besides the monarch butterfly I also studied two related milkweed butterflies, the queen butterfly (D. gilippus) and the common crow (Euploea core), which use cardenolide producing milkweeds (Apocynaceae) as well. Importantly, the three caterpillar species express Na+/K+-ATPases with different sensitivity to cardenolides (E. core: sensitive, D. gilippus: intermediately, and D. plexippus: highly resistant). This quantitative framework provided me with an unprecedented opportunity to test coevolutionary hypotheses. Surprisingly, I found that dietary cardenolides did not negatively influence caterpillar growth but the three levels of Na+/K+-ATPase resistance were paralleled by the amount of cardenolides sequestered (E. core: none, D. gilippus: intermediate, D. plexippus: highest). Our finding thus suggests that sequestration (i.e. protection from natural enemies), and not dietary tolerance, was the evolutionary driver for this specific resistance trait against plant toxins and advances coevolutionary theory as not only the first trophic level (plants) but also the third trophic level (predators and parasitoids) can spur coevolutionary escalation. As we have shown that cardenolides did not have a detrimental effect on specialized herbivores (at the level of the whole organism) but Na+/K+-ATPase resistance is linked to sequestration I shifted the focus of my project to the mechanisms of sequestration and the interplay of cardenolides with the target site Na+/K+-ATPase to test for coevolutionary interactions. The application of individual cardenolides on isolated monarch Na+/K+-ATPase revealed that different cardenolides can have dramatically different effects even on the relatively cardenolide resistant Na+/K+-ATPase of the monarch butterfly. We furthermore found that cardenolide glycosides seem to be more potent than the corresponding genins and that cardenolides show specific interactions with differentially resistant Na+/K+-ATPases. Moreover, monarchs seem to preferentially sequester the most toxic cardenolides. Focusing on sequestration we found that early instar monarch caterpillars sequester disproportionately high amounts of cardenolides which might be a mechanistic explanation for high mortality observed in early instars. The amount of sequestered cardenolides in the monarch apparently depends on plant cardenolide concentration and sequestration is selective. During my DFG-funded work at Cornell University I was able to perform five experiments which revealed novel important insights on evolutionary mechanisms.
Publications
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(2013): Functional evidence for physiological mechanisms to circumvent neurotoxicity of cardenolides in an adapted and a non-adapted hawkmoth species. Proceedings of the Royal Society B 280
Petschenka, G., Pick, C, Wagschal, V., Dobler, S.
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(2013): Stepwise evolution of resistance to toxic cardenolides via genetic substitutions in the Na+/K+-ATPase of milkweed butterflies (Lepidoptera: Danaini). Evolution 67, 2753-2761
Petschenka, G., Fandrich, S., Sander, N., Boppr6, M., Dobler, S.
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(2014): Amphibian myiasis. Blowfly larvae (Lucilia bufonivora, Diptera: Calliphoridae) coping with the poisonous skin secretion of the common toad (Bufo bufo). Chemoecology 24, 159-164
Mebs, D., Petschenka, G., Pogoda, W., Toennes, S.W., Amendl, J., Zajac, B.K., Dobler, S.
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(2015): Convergent adaptive evolution - How insects master the challenge of cardiac glycoside-containing host plants. Entomologia Experimentalis et Applicata
Dobler, S., Petschenka, G., Wagschal, V., Flacht, L.
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(2015): Na+/K+-ATPase resistance and cardenolide sequestration: basal adaptations to host plant toxins in the milkweed bugs (Hemiptera: Lygaeidae: Lygaeinae). Proceedings of the Royal Society B 282
Bramer, C, Dobler, S., Deckert, J., Stemmer, M.. Petschenka, G.
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Milkweed butterfly resistance to plant toxins is linked to sequestration, not coping with a toxic diet. Proc. R. Soc. B, 7 November 2015, Volume 282, issue 1818, 1865 (9 S.)
Petschenka, G., Agrawal, A.A.
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How herbivores coopt plant defenses: natural selection, specialization, and sequestration. Current opinion in insect science, 2016, Vol 14, pp. 17-24
Petschenka, G., Agrawal, A.A.
