Abstract
The evolution of sequestration (uptake and accumulation) relative to de novo biosynthesis of chemical defense compounds is poorly understood, as is the interplay between these two strategies. The Burnet moth Zygaena filipendulae (Lepidoptera) and its food-plant Lotus corniculatus (Fabaceae) poses an exemplary case study of these questions, as Z. filipendulae belongs to the only insect family known to both de novo biosynthesize and sequester the same defense compounds directly from its food-plant. Z. filipendulae and L. corniculatus both contain the two cyanogenic glucosides linamarin and lotaustralin, which are defense compounds that can be hydrolyzed to liberate toxic hydrogen cyanide. The overall amounts and ratios of linamarin and lotaustralin in Z. filipendulae are tightly regulated, and only to a low extent reflect the ratio in the ingested food-plant. We demonstrate that Z. filipendulae adjusts the de novo biosynthesis of CNglcs by regulation at both the transcriptional and protein level depending on food plant composition. Ultimately this ensures that the larva saves energy and nitrogen while maintaining an effective defense system to fend off predators. By using in situ PCR and immunolocalization, the biosynthetic pathway was resolved to the larval fat body and integument, which infers rapid replenishment of defense compounds following an encounter with a predator. Our study supports the hypothesis that de novo biosynthesis of CNglcs in Z. filipendulae preceded the ability to sequester, and facilitated a food-plant switch to cyanogenic plants, after which sequestration could evolve. Preservation of de novo biosynthesis allows fine-tuning of the amount and composition of CNglcs in Z. filipendulae.
Highlights
A driving force in speciation is to evolve, exploit and handle chemical defenses
In order to test if the larvae regulate the de novo biosynthesis of Cyanogenic glucosides (CNglcs) in relation to CNglc content of the food plant, transcript levels of the biosynthetic genes were analyzed by quantitative realtime PCR and RNA-Seq in seventh instar larvae collected in the field and reared for 2 weeks on (+)diet and (2)diet respectively
Z. filipendulae larvae are seldom expected to feed on completely acyanogenic plants in vivo, and thereby to rely solely on de novo biosynthesis, the larvae would need to be able to adjust their CNglc levels due to the polymorphism in cyanogenesis in L. corniculatus populations, in order to maintain the optimal content and ratio of CNglcs during their life-cycle [11]
Summary
Two central issues with regards to insect chemical defenses are how cost-efficient defenses against predators have evolved and how these are regulated. Insects acquire chemical defense compounds either through de novo biosynthesis, sequestration (uptake, accumulation and storage [1] of plantderived defense compounds) or by a combination of the two strategies [2]. Sequestration relies on the composition of the compounds in the food-plant and enables less control by the insect, but is a more cost-efficient strategy since the compounds do not have to be produced de novo. While some specialized leaf beetle (Chrysomelinae) species have evolved to biosynthesize defense compounds de novo, others sequester them from plants and metabolize them to generate new defense compounds [2]. The larvae of Zygaena moths (Zygaenoidae, Lepidoptera), are unique in that they can obtain the same chemical defense compounds through both de novo biosynthesis [4] and sequestration [6]
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