Evolution of koinobiont parasitoid host regulation and consequences for indirect plant defence

Tritrophic interactions among plants, herbivorous insects and their parasitoids have been well studied in the past four decades. Recently, a new angle has been uncovered: koinobiont parasitoids, that allow their host to keep feeding on the plant for a certain amount of time after parasitism, indirectly alter plant responses against herbivory via the many physiological changes induced in their herbivorous hosts. By affecting plant responses, parasitoids may indirectly affect the whole community of insects interacting with plants induced by parasitized herbivores and have extended effects on plant fitness. These important findings have renewed research interests on parasitoid manipulation of their host development. Parasitoids typically arrest their host development before the last instar, resulting in a lower final weight compared to unparasitized hosts. Yet, some parasitoids prolong their host development, leading to larger herbivores that consume more plant material than unparasitized ones. Furthermore, parasitoid host regulation is plastic and one parasitoid species may arrest or promote its host growth depending on the number of eggs laid, host developmental stage and species as well as environmental conditions. The consequences of plasticity in parasitoid host regulation for plant-insect interactions have received very little attention over the last two decades, particularly concerning parasitoids that promote their host growth. In this review, we first synthesize the mechanisms used by parasitoids to regulate host growth and food consumption. Then, we identify the evolutionary and environmental factors that influence the direction of parasitoid host regulation in terms of arrestment or promotion of host growth. In addition, we discuss the implication of different host regulation types for the parasitoid's role as agent of plant indirect defence. Finally, we argue that the recent research interests about parasitoid plant-mediated interactions would strongly benefit from revival of research on the mechanisms, ecology and evolution of host regulation in parasitoids.