Abstract

Certain butterflies utilize plant-acquired alkaloids for their own chemical defense and/or for producing male sex pheromone; a trait known as pharmacophagy. Males of the danaine butterfly, Parantica sita, have been reported to ingest pyrrolizidine alkaloids (PAs) as adults to produce two PA-derived sex pheromone components, viz. danaidone (major) and 7R-hydroxydanaidal. We found, however, that not all PAs that can be precursors for the pheromone serve for mating success of males. Here we show that although the sex pheromone is regarded as a requisite for successful mating, uptake of specific PA(s) (lycopsamine-type PAs) is also imperative for the males to achieve copulation. The increase in the levels of two biogenic amines, octopamine and/or serotonin, in the brain and thoracic ganglia of males fed with specific PA(s) suggested that these alkaloids most likely enhance male mating activity. The results can present new evidence for the evolutionary provenance of pharmacophagous acquisition of PAs in PA-adapted insects.

Highlights

  • Animals require nutrients for growth and development but occasionally or routinely ingest particular phytochemicals for the purpose of self-medication, chemical defense against predatory enemies, or pheromone biosynthesis

  • We have previously shown that the males possess DO as a major component along with a much smaller amount of 7R-HD (7R-enantiomer of HD) in both the sex brand and hairpencil, and further demonstrated that either or both of these compounds act as the sex pheromone[21]

  • We first tested the effect of ingestion of some pyrrolizidine alkaloids (PAs)-related substances on male mating success (Fig. 2); PA substances administered to the males were a mixture composed of intermedine and lycopsamine, heliotrine, and a hydrolysate mixture of I/L

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Summary

Introduction

Animals require nutrients for growth and development but occasionally or routinely ingest particular phytochemicals for the purpose of self-medication, chemical defense against predatory enemies, or pheromone biosynthesis. Among the most intensively and extensively studied plant chemicals that are involved in insect-plant interactions are pyrrolizidine alkaloids (PAs), which are well-known hepatotoxic plant secondary (specialized) metabolites that play diverse roles in terrestrial ecosystems and are closely associated with arctiid moths and butterflies in the subfamilies Danainae and Ithomiinae (Nymphalidae)[11,16,17] In these PA-adapted lepidopterans, PAs, acquired by larvae or adults from host or non-host plants, are utilized as precursors for the biosynthesis of male sex pheromones[18,19,20,21] and for chemical defense against predators, parasitoids, or pathogens[22,23]. This study further examined how PA uptake by males affect their courtship behaviour, focusing on their activity in the sequence of precopulatory aerial interactions with females, and determined the levels of biogenic amines (known to function as neurotransmitters, neuromodulators, or neurohormones35–37) present in the brain and thoracic ganglia of males to deduce possible relationships between PA uptake and male mating success

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