Hoverfly preference for high honeydew amounts creates enemy-free space for aphids colonizing novel host plants

The existence of an enemy-free space can play an important role in aphid host race formation processes, but little is known about the mechanisms that create an area of low predation pressure on particular host plants. In this paper we identify a mechanism generating lower predation pressure that promotes the maintenance of the different host races of the pea aphid (Acyrthosiphon pisum) complex, a well-studied model for ecological speciation. The pea aphid consists of at least 15 genetically distinct host races which are native to specific host plants of the legume family, but can all develop on the universal host plant Vicia faba. Previous work showed that hoverfly (Episyrphus balteatus) oviposition preferences contribute to the enemy-free space that helps to maintain the different pea aphid host races, and that higher amounts of honeydew are more attractive to ovipositing hoverflies. Here we demonstrated that aphid honeydew is produced in large amounts when aphid reproduction rate was highest, and so is an important oviposition cue for hoverflies under field conditions. However, on less suitable host plants, where honeydew production is reduced, pea aphids enjoy lower predation rates. A reduction in enemy pressure can mitigate the performance disadvantages of aphids colonizing a novel host, and probably plays an important role in pea aphid host race formation.