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

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.

可重复的宏观演化模式为生物学规律的探寻带来了希望，尤其是当我们能够解析其背后的作用机制时。本研究综合分析了以具有强心苷（cardiac glycoside）防御机制的植物为宿主的专食性植食性昆虫的自然历史、遗传适应性与毒素储集（toxin sequestration）现象。针对帝王蝶的相关研究为储毒专性综合征的演化提供了经典模型：该昆虫的钠钾ATP酶（Na+/K+-ATPase）上的特定氨基酸替换与三类核心特征相关：1）高毒素抗性（靶标位点不敏感，TSI）、2）毒素储集作用、3）警戒色（aposematic coloration）。我们针对鳞翅目（Lepidoptera）、鞘翅目（Coleoptera）、双翅目（Diptera）、半翅目（Hemiptera）、膜翅目（Hymenoptera）及直翅目（Orthoptera）内部及类群间的上述性状开展趋同演化评估，研究覆盖了数百种适应毒素的昆虫物种。基于约28次专食性起源的全新与已有数据集，我们证实帝王蝶模型在5个昆虫分类目中独立演化（双翅目除外）。另有一类综合征在5个目中独立出现：具备中等偏低至中等水平TSI的警戒色储毒类群（膜翅目除外）。事实上，所有储毒昆虫均具有警戒色，且仅1个物种例外，其余均至少具备中等偏低水平的TSI。此外，部分物种为具有警戒色但不储毒的类群（潜在的贝茨拟态（Batesian mimic）者），这类性状组合在TSI水平各异的物种中多次演化形成。最后，我们还发现了上述策略在各分类目内存在的部分偏倚现象。这个生命微观缩影中的生物多样性在6个分类目中反复演化出高度相似的性状模式，但我们同时也识别出了其他的性状组合以及类群特异性的演化结局。