High evolutionary potential in the chemical defenses of an aposematic Heliconius butterfly

Chemical defences against predators underlie the evolution of aposematic coloration and mimicry, which represent classic examples of adaptive evolution. Yet, unlike color patterns, little is known about the evolutionary potential of chemical defences. Neotropical Heliconius butterflies exhibit incredibly diverse warning color patterns and widespread mimicry. Their larvae feed exclusively on cyanogenic Passiflora vines, can metabolize and sequester host plant toxins, as well as biosynthesize defensive cyanogenic toxins themselves. Here, we investigate variation in biosynthesized toxicity both in wild populations along environmental gradients and in common-garden broods and feeding treatments in Heliconius erato, together demonstrating considerable intraspecific variation and evolutionary potential in this important chemical defense trait. Toxicity varied markedly among wild populations from Central and South America. Within wild populations, the distribution of toxicity was consistently skewed, indicative of automimic “cheaters” that may exploit, and consequently deplete, the protection of the warning coloration. In a common-garden rearing design comprising more than 300 butterflies across 20 broods, variation in host-plant nutritional quality or cyanogen levels did not translate into differences in toxicity of butterflies feeding on these plants. Instead, toxicity had a significant heritable genetic component, in part explained by maternal inheritance. The evolvability of toxicity was high (eμ=1.55%), suggesting that toxicity can evolve rapidly. Through its link with the evolution of warning color pattern mimicry, the high evolutionary potential of cyanogenic toxicity may have facilitated diversification and ecological speciation in Heliconius, highlighting the importance of understanding the evolution of chemical defense in aposematic and mimetic species.