Condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly

Abstract

Aposematic animals advertise their toxicity or unpalatability with bright warning coloration. However, acquiring and maintaining chemical defenses can be energetically costly, and consequent associations with other important traits could shape chemical defense evolution. Here, we have tested whether chemical defenses are involved in energetic trade‐offs with other traits, or whether the levels of chemical defenses are condition dependent, by studying associations between biosynthesized cyanogenic toxicity and a suite of key life‐history and fitness traits in a Heliconius butterfly under a controlled laboratory setting. Heliconius butterflies are well known for the diversity of their warning color patterns and widespread mimicry and can both sequester the cyanogenic glucosides of their Passiflora host plants and biosynthesize these toxins de novo . We find energetically costly life‐history traits to be either unassociated or to show a general positive association with biosynthesized cyanogenic toxicity. More toxic individuals developed faster and had higher mass as adults and a tendency for increased lifespan and fecundity. These results thus indicate that toxicity level of adult butterflies may be dependent on individual condition, influenced by genetic background or earlier conditions, with maternal effects as one strong candidate mechanism. Additionally, toxicity was higher in older individuals, consistent with previous studies indicating accumulation of toxins with age. As toxicity level at death was independent of lifespan, cyanogenic glucoside compounds may have been recycled to release resources relevant for longevity in these long‐living butterflies. Understanding the origins and maintenance of variation in defenses is necessary in building a more complete picture of factors shaping the evolution of aposematic and mimetic systems.

Pollen-feeding delays reproductive senescence and maintains toxicity ofHeliconius erato

“…Our data demonstrate how strongly H. erato biosynthesize CG during adulthood to maintain their defences while also investing in the protection of their offspring, corroborating previous findings (Castro et al 2020; Mattila et al 2022). Considering that a Heliconius female lays ca.…”

“…Mattila et al (2022) demonstrated that Heliconius butterflies keep their CG concentration at high levels during adulthood until their natural death. Indeed, if these aposematic butterflies lost their toxicity as they age, this would dilute the protection signal of their colour pattern.…”

“…Pedigree experiments with H. erato also found strong maternal effects on offspring toxicity, but no paternal effects (Mattila et al, 2021). Mattila et al (2022) demonstrated that Heliconius butterflies keep their CG concentration at high levels during adulthood until their natural death. Indeed, if these aposematic butterflies lost their toxicity as they age, this would dilute the protection signal of their colour pattern.…”