Pollen feeding, resource allocation and the evolution of chemical defence in passion vine butterflies

Abstract

Evolution of pollen feeding in Heliconius has allowed exploitation of rich amino acid sources and dramatically reorganized life-history traits. In Heliconius, eggs are produced mainly from adult-acquired resources, leaving somatic development and maintenance to larva effort. This innovation may also have spurred evolution of chemical defence via amino acid-derived cyanogenic glycosides. In contrast, nonpollen-feeding heliconiines must rely almost exclusively on larval-acquired resources for both reproduction and defence. We tested whether adult amino acid intake has an immediate influence on cyanogenesis in Heliconius. Because Heliconius are more distasteful to bird predators than close relatives that do not utilize pollen, we also compared cyanogenesis due to larval input across Heliconius species and nonpollen-feeding relatives. Except for one species, we found that varying the amino acid diet of an adult Heliconius has negligible effect on its cyanide concentration. Adults denied amino acids showed no decrease in cyanide and no adults showed cyanide increase when fed amino acids. Yet, pollen-feeding butterflies were capable of producing more defence than nonpollen-feeding relatives and differences were detectable in freshly emerged adults, before input of adult resources. Our data points to a larger role of larval input in adult chemical defence. This coupled with the compartmentalization of adult nutrition to reproduction and longevity suggests that one evolutionary consequence of pollen feeding, shifting the burden of reproduction to adults, is to allow the evolution of greater allocation of host plant amino acids to defensive compounds by larvae.