Fine-tuning the 'plant domestication-reduced defense' hypothesis: specialist vs generalist herbivores.

Domesticated plants are assumed to have weakened chemical defenses. We argue, however, that artificial selection will have maintained defense traits against specialized herbivores that have coexisted with the crops throughout their domestication. We assessed the performance of eight species of insect herbivores from three feeding guilds on six European maize lines and six populations of their wild ancestor, teosinte. A metabolomics approach was used in an attempt to identify compounds responsible for observed differences in insect performance. Insects consistently performed better on maize than on teosinte. As hypothesized, this difference was greater for generalist herbivores that are normally not found on teosinte. We also found clear differences in defense metabolites among the different genotypes, but none that consistently correlated with differences in performance. Concentrations of benzoxazinoids, the main chemical defense in maize, tended to be higher in leaves of teosinte, but the reverse was true for the roots. It appears that chemical defenses that target specialized insects are still present at higher concentrations in cultivated maize than compounds that are more effective against generalists. These weakened broad-spectrum defenses in crops may explain the successes of novel pests.

A specialist root herbivore exploits defensive metabolites to locate nutritious tissues.

The most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots.