Why Do Herbivorous Mites Suppress Plant Defenses?

C. Joséphine H. Blaazer, Ernesto A. Villacis-Perez, Rachid Chafi, Thomas Van Leeuwen, Merijn R. Kant, Bernardus C. J. Schimmel

Plants have evolved numerous defensive traits that enable them to resist herbivores. In turn, this resistance has selected for herbivores that can cope with defenses by either avoiding, resisting or suppressing them. Several species of herbivorous mites, such as the spider mites Tetranychus urticae and Tetranychus evansi, were found to maximize their performance by suppressing inducible plant defenses. At first glimpse it seems obvious why such a trait will be favored by natural selection. However, defense suppression appeared to readily backfire since mites that do so also make their host plant more suitable for competitors and their offspring more attractive for natural enemies. This, together with the fact that spider mites are infamous for their ability to resist (plant) toxins directly, justifies the question as to why traits that allow mites to suppress defenses nonetheless seem to be relatively common? We argue that this trait may facilitate generalist herbivores, like T. urticae, to colonize new host species. While specific detoxification mechanisms may, on average, be suitable only on a narrow range of similar hosts, defense suppression may be more broadly effective, provided it operates by targeting conserved plant signaling components. If so, resistance and suppression may be under frequency-dependent selection and be maintained as a polymorphism in generalist mite populations. In that case, the defense suppression trait may be under rapid positive selection in subpopulations that have recently colonized a new host but may erode in relatively isolated populations in which host-specific detoxification mechanisms emerge. Although there is empirical evidence to support these scenarios, it contradicts the observation that several of the mite species found to suppress plant defenses actually are relatively specialized. We argue that in these cases buffering traits may enable such mites to mitigate the negative side effects of suppression in natural communities and thus shield this trait from natural selection.