De novo Synthesis vs. Sequestration: Negatively Correlated Metabolic Traits and the Evolution of Host Plant Specialization in Cyanogenic Butterflies

Larvae of Heliconius butterflies (Nymphalidae: Heliconiinae) feed exclusively on cyanogenic leaves of Passiflora (passion vine). Most Heliconius manufacture cyanogenic glycosides (cyanogens) and some species sequester cyanogens from host plants. We compare ability to sequester simple monoglycoside cyclopentenyl (SMC) cyanogens and manufacture aliphatic cyanogens in 12 Heliconius species, including larvae that are specialized (single host species) and generalized (many host species). All butterflies tested higher for cyanide concentrations when reared on plants that larvae can sequester from (SMC plants) than when reared on plants that larvae do not sequester from (non-SMC plants). Specialists in the sara–sapho clade sequestered SMC cyanogens from specific host plants at seven times that of Passiflora generalists fed the same hosts. In contrast, sara–sapho clade species reared on non-SMC plants had significantly lower cyanide concentrations from de novo synthesis than generalists fed the same plants. Furthermore, cyanogen analyses indicated that Heliconius sara butterflies reared on an SMC host had a greater proportion of sequestered SMC cyanogens (95.0%) than de novo-synthesized aliphatic cyanogens (5.0%). Thus, sequestration and de novo synthesis are negatively correlated traits. Results suggest that losing the ability to synthesize cyanogens has restricted sara–sapho clade species to specific hosts containing SMC cyanogens and explains dietary restriction in this clade. We dedicate our paper to the memory of the Honorable Miriam Rothschild, F.R.S., a friend, colleague and supporter of many young scientists. Her enthusiasm and delight in chemical ecology and natural history continued to the last weeks of her life.