The evolution of chemical defenses in passion vine butterflies: biosynthesis, sequestration, and functional diversification of cyanogenicglucosides in Heliconius

Érika Cristina Pinheiro de Castro

Abstract

The bright and colorful Neotropical butterflies of the Heliconius genus are avoided by most insectivorous predators. Inexperienced birds and lizards may bite Heliconius butterflies, but immediately release them due to their toxic taste. The distastefulness of these butterflies is associated with the presence of defense compounds called cyanogenic glucosides (CNglcs), which deter predators because of their bitterness and the release of hydrogen cyanide upon degradation. Heliconius butterflies and basal heliconiines biosynthesize the aliphatic CNglcs linamarin and lotaustralin. Additionally, Heliconius larva can take up the cyclopentenyl CNglc epivolkenin from Passiflora, their obligatory host plants.The research presented in this PhD thesis demonstrates that sequestration of cyclopentenyl CNglcs is not exclusively a trait of Heliconius, and probably arose in a common ancestor of the entire heliconiine subfamily. Despite sequestration of these compounds being an older adaptation than expected, biosynthesis of aliphatic CNglcs is hypothesized to be even more ancient, arising in lepidopterans before butterflies and moths diverged from a common ancestor.

In addition, this study shows that epivolkenin is not the only CNglc that Heliconius larvae can sequester from Passiflora. Many other cyclopentenyl CNglcs were found in Heliconius imagines, and feeding assays demonstrated that aliphatic and aromatic CNglcs can also be taken up by these larvae, although these structures are not as common in Passiflora as cyclopentenoids. Modified CNglcs were not sequestered, and Passiflora could therefore have diversified their repertoire of CNglcs in order to decrease their nutritional value to heliconiines. Heliconius use CNglcs not only for defence:. These butterflies have more CNglcs than they can actually degrade into cyanide.. During its life cycle, Heliconius melpomene is most cyanogenic when it is a mature adult, due to intense biosynthesis of aliphatic CNglcs. Males of this species transfer linamarin and lotaustralin during copula to females, confirming earlier suggestions that CNglcs are used as nuptial gifts by Heliconius. Mature adults contain cyclopentenyl CNglcs consumed and accumulated during the larval stage, but these compounds are not transferred to peers during mating or to the offspring. We speculate that the mature adults catabolise these CNglcs to retrieve nitrogen and/or to utilize their volatile degradation products during mating communication between males and females

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