Jones Patricia L, Petschenka Georg, Flacht Lara, Agrawal Anurag A
Department of Biology, Bowdoin College, Brunswick, ME, USA.
Institute for Insect Biotechnology, Justus-Liebig-Universität Giessen, Giessen, Germany.
J Chem Ecol. 2019 Mar;45(3):264-277. doi: 10.1007/s10886-019-01055-7. Epub 2019 Feb 22.
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.
黑脉金斑蝶（Danaus plexippus）会进行远距离迁徙，在此过程中它们会遇到含有毒性差异很大的强心甾类化合物的寄主植物。对于在这类毒素含量不同的寄主植物上产卵的鳞翅目昆虫的解毒机制，人们了解得非常少。我们使用强心甾类化合物浓度相差十倍以上的近缘马利筋属寄主植物，从机制上研究了黑脉金斑蝶对强心甾类化合物的摄取、解毒和排泄情况。我们发现，在强心甾类化合物含量高的植物物种上，成年蝴蝶体内的强心甾类化合物会饱和，导致其体内浓度低于叶片中的浓度；而在强心甾类化合物含量低的植物上，蝴蝶会富集毒素。蝴蝶似乎将解毒作用集中在特定化合物上，因为强心甾类化合物的多样性在植物叶片中最高，在粪便中较低，而在成年蝴蝶体内最少。在植物产生的各种强心甾类化合物中，被解毒的化合物对蝴蝶自身的毒性可能较小，因为它们的平均极性比叶片中的化合物更大。与此一致的是，基于抑制钠钾ATP酶（强心甾类化合物的生理靶点）的体外试验结果表明，在两种马利筋属植物上，包括强心甾类化合物含量高的多年生马利筋（Asclepias perennis），按强心甾类化合物浓度标准化后，蝴蝶提取物的抑制作用比叶片低，这表明蝴蝶从这些寄主植物中选择性地解毒了毒性较小的化合物。为了了解个体发育如何影响解毒过程，我们在幼虫发育过程中检测了其身体组织和血淋巴中的强心甾类化合物浓度。幼虫在低龄期比高龄期积累更高浓度的强心甾类化合物，但在五龄期内，浓度随体重增加。虽然看起来大量的解毒作用发生在低龄期，但一项寄主转换实验表明，幼虫可以通过在五龄期大量解毒来弥补在强心甾类化合物含量低的寄主植物上取食的不足。我们强调了根据寄主植物化学性质和发育阶段，解毒机制的共性和显著差异，这对黑脉金斑蝶的防御具有重要意义。
