Parent–offspring conflicts, "optimal bad motherhood" and the "mother knows best" principles in insect herbivores colonizing novel host plants

Abstract

Specialization of insect herbivores to one or a few host plants stimulated the development of two hypotheses on how natural selection should shape oviposition preferences: The "mother knows best" principle suggests that females prefer to oviposit on hosts that increase offspring survival. The "optimal bad motherhood" principle predicts that females prefer to oviposit on hosts that increase their own longevity. In insects colonizing novel host plants, current theory predicts that initial preferences of insect herbivores should be maladaptive, leading to ecological traps. Ecological trap theory does not take into account the fact that insect lineages frequently switch hosts at both ecological and evolutionary time scales. Therefore, the behavior of insect herbivores facing novel hosts is also shaped by natural selection. Using a study system in which four Cephaloleia beetles are currently expanding their diets from native to exotic plants in the order Zingiberales, we determined if initial oviposition preferences are conservative, maladaptive, or follow the patterns predicted by the "mother knows best" or the "optimal bad motherhood" principles. Interactions with novel hosts generated parent–offspring conflicts. Larval survival was higher on native hosts. However, adult generally lived longer on novel hosts. In Cephaloleia beetles, oviposition preferences are usually associated with hosts that increase larval survival, female fecundity, and population growth. In most cases, Cephaloleia oviposition preferences follow the expectations of the "mothers knows best" principle.