Enemy-free space promotes maintenance of host races in an aphid species

The enormous biodiversity of herbivorous insects may arise from ecological speciation via continuous host-plant switches. Whether such switches are successful depends on the trade-off between different selection pressures that act on herbivores. Decreased herbivore performance due to suboptimal nutrition might be compensated for by a reduced natural enemy pressure. As a consequence, an "enemy-free space" on a certain plant might facilitate host-plant switches and maintain biotypes. To test this hypothesis, we used the pea aphid (Acyrthosiphon pisum) complex, which consists of at least 11 genetically distinct host races that are native to specific legume host plants but can all develop on the universal host plant Vicia faba. Three A. pisum host races native to Trifolium pratense, Pisum sativum, and Medicago sativa were investigated in experiments on their respective host plants and on the universal host plant V. faba. We found that hoverflies preferred to oviposit on P. sativum and the universal host V. faba. Since feeding by hoverfly larvae suppressed aphid population growth on these host plants, the native hosts M. sativa and T. pratense provided enemy-free space for the respective A. pisum races. Mobile predators, such as ants and ladybird beetles, preferred Pisum race aphids on V. faba over P. sativum. Thus, all three of the native host plants studied supply enemy-free space for A. pisum compared to the universal host V. faba. Reducing encounters between aphid races on V. faba would reduce gene flow among them and could contribute to maintaining the host races.