Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants

The colorful heliconiine butterflies are distasteful to predators due to their content of defense compounds called cyanogenic glucosides (CNglcs), which they biosynthesize from aliphatic amino acids. Heliconiine larvae feed exclusively on Passiflora plants where ~30 kinds of CNglcs have been reported. Among them, some CNglcs derived from cyclopentenyl glycine can be sequestered by some Heliconius species. In order to understand the evolution of biosynthesis and sequestration of CNglcs in these butterflies and its consequences for their arms race with Passiflora plants, we analyzed the CNglc distribution in selected heliconiine and Passiflora species. Sequestration of cyclopentenyl CNglcs is not an exclusive trait of Heliconius, since these compounds were present in other heliconiines such as Philaethria, Dryas and Agraulis, and in more distantly related genera Cethosia and Euptoieta. Thus, it is likely that the ability to sequester cyclopentenyl CNglcs arose in an ancestor of the Heliconiinae subfamily. Biosynthesis of aliphatic CNglcs is widespread in these butterflies, although some species from the sara‐sapho group seem to have lost this ability. The CNglc distribution within Passiflora suggests that they might have diversified their cyanogenic profile to escape heliconiine herbivory. This systematic analysis improves our understanding on the evolution of cyanogenesis in the heliconiine–Passiflora system.

色彩艳丽的釉蛱蝶亚科（Heliconiinae）蝴蝶对捕食者具有驱避性，这是因为其体内含有由脂肪族氨基酸生物合成的防御化合物——生氰糖苷（cyanogenic glucosides，CNglcs）。釉蛱蝶的幼虫仅以西番莲属（Passiflora）植物为食，目前已在该属植物中报道存在约30种生氰糖苷。其中，部分由环戊烯基甘氨酸衍生而来的生氰糖苷可被某些袖蝶属（Heliconius）物种摄取储存。为阐明此类蝴蝶中生氰糖苷生物合成与摄取储存机制的演化历程，及其与西番莲属植物军备竞赛带来的演化效应，本研究对筛选出的釉蛱蝶类群与西番莲属物种体内的生氰糖苷分布情况展开了分析。环戊烯基生氰糖苷的摄取储存并非袖蝶属的独有性状：此类化合物不仅存在于其他釉蛱蝶类群（如菲袖蝶属Philaethria、亮袖蝶属Dryas以及阿格拉袖蝶属Agraulis）中，还出现在亲缘关系更远的红蛱蝶属Cethosia与豹蛱蝶属Euptoieta内。由此推测，摄取储存环戊烯基生氰糖苷的能力起源于釉蛱蝶亚科的共同祖先。脂肪族生氰糖苷的生物合成在这类蝴蝶中广泛存在，但sara-sapho类群中的部分物种似乎已丧失该能力。西番莲属植物体内的生氰糖苷分布特征表明，该类群可能通过演化生氰糖苷谱型来逃避釉蛱蝶的植食性取食。本项系统性分析加深了我们对釉蛱蝶-西番莲协同演化系统中生氰作用演化历程的认知。