Ontogenetic differences in the chemical defence of flea beetles influence their predation risk

Abstract

Several insect species have evolved two-component chemical defences that enable the rapid release of deterrent or toxic metabolites upon predator attack. However, whether these chemical defences vary across insect ontogeny and how this affects the predation risk of different life stages has rarely been addressed. The horseradish flea beetle Phyllotreta armoraciae possesses a two-component chemical defence that consists of sequestered glucosinolates and an insect myrosinase capable of converting the non-toxic glucosinolates to deterrent isothiocyanates. Here, we show that the levels of sequestered glucosinolates only varied 2-fold across beetle ontogeny, but that insect myrosinase activity differed up to 43-fold among ontogenetic stages. Specifically, glucosinolate levels were 1.5-fold lower in the larvae of P. armoraciae than in pupae, but they showed 43.4-fold higher levels of myrosinase activity. Consistent with the distinct levels of myrosinase activity in larvae and pupae, only larvae released high amounts of toxic isothiocyanates when they were attacked by the generalist predator Harmonia axyridis. P. armoraciae larvae deterred the predator and survived one attack, whereas pupae were killed. Feeding of P. armoraciae larvae on plants that differed in glucosinolates and plant myrosinase activity influenced the accumulation of glucosinolates in larvae and their subsequent interaction with H. axyridis. Larvae with low levels of sequestered glucosinolates were much more susceptible to predation than larvae containing high glucosinolate levels. Our results demonstrate that sequestered plant defence metabolites selectively protect specific ontogenetic stages of P. armoraciae from predation. The strong influence of plant defensive chemistry on sequestration indicates that predators have played an important role in the evolution of host use in this specialist herbivore. The distinct life styles of flea beetle life stages and their strategies to prevent predation by biologically relevant predator communities deserve further investigations. A free Plain Language Summary can be found within the Supporting Information of this article.