Department of Nematology, University of California, Riverside, CA 92521, USA.
Department of Integrative Biology and Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, USA.
Curr Biol. 2021 Nov 22;31(22):R1465-R1466. doi: 10.1016/j.cub.2021.10.025.
The community of plant-feeding insects (herbivores) that specialize on milkweeds (Apocynaceae) form a remarkable example of convergent evolution across levels of biological organization. In response to toxic cardiac glycosides produced by these plants, the monarch butterfly (Danaus plexippus) and other specialist herbivores have evolved parallel substitutions in the alpha subunit (ATPA) of the Na/K-ATPase. These substitutions render the pump insensitive to cardiac glycosides, allowing the monarch and other specialists, from aphids to beetles, to sequester cardiac glycosides, which in turn provide defense against attacks by enemies from the third trophic level. The evolution of 'target-site-insensitivity' substitutions in these herbivores poses a fundamental biological question: have predators and parasitoids that feed on cardiac-glycoside-sequestering insects also evolved Na/K-ATPases that are similarly insensitive to cardiac glycosides (as predicted by Whiteman and Mooney)? In other words, can plant toxins cause evolutionary cascades that reach the third trophic level? Here we show that at least four enemies of the monarch and other milkweed herbivores have indeed evolved amino-acid substitutions associated with target-site insensitivity to cardiac glycosides. These attackers represent four major animal clades, implicating cardiac glycosides as keystone molecules and establishing ATPalpha, which encodes ATPA, as a keystone gene with effects that reverberate within ecological communities.
以乳草科植物（Apocynaceae）为食的植食性昆虫（草食性动物）群体形成了一个跨越生物组织层次的趋同进化的显著例子。为了应对这些植物产生的有毒强心苷，帝王蝶（Danaus plexippus）和其他专门的草食性动物在钠/钾-ATP 酶的α亚基（ATPA）中进化出了平行的替代。这些替代使泵对强心苷不敏感，使帝王蝶和其他专家，从蚜虫到甲虫，能够隔离强心苷，这反过来又为抵御来自第三营养级的敌人的攻击提供了防御。这些草食性动物中“靶位不敏感性”替代的进化提出了一个基本的生物学问题：以摄取强心苷隔离昆虫为食的捕食者和寄生蜂是否也进化出了对强心苷同样不敏感的钠/钾-ATP 酶（正如 Whiteman 和 Mooney 所预测的那样）？换句话说，植物毒素是否能引发达到第三营养级的进化级联反应？在这里，我们表明，至少有四种帝王蝶和其他乳草科食草动物的天敌确实进化出了与靶位不敏感性相关的氨基酸替代。这些攻击者代表了四个主要的动物类群，这意味着强心苷作为关键分子，以及编码 ATPA 的 ATPalpha 作为具有在生态群落中产生共鸣的影响的关键基因。
