Tritrophic interactions reinforce a negative preference–performance relationship in the tobacco hornworm ( Manduca sexta )

Host plants that promote development of insect herbivores are sometimes less preferred to more toxic plants, which are co‐opted for protection from natural enemies, resulting in higher fitness in communities with strong top‐down control. However, the degree to which variation in growth rate and risk of natural enemy attack drive insect plant preferences is an open question, with little field data available across diverse plant families. The present study investigated the preference–performance relationship and tritrophic interactions involving the hornworm Manduca sexta , its natural enemies, and plants in the nightshade family (Solanaceae) using a 2‐year common garden containing 18 wild and domesticated species. The degree to which natural enemy pressure explained field patterns in the laboratory was then tested using targeted assays involving parasitism by the wasp Cotesia congregata . In the field, the most preferred plants for female oviposition tended to be inversely correlated with the species providing optimal larval growth. Hawkmoths preferred plants in the subgenus Potatoe , Nicotiana , and Datura compared with Capsicum , Physalis , and the other Solanum subgenera. However, larval parasitism by C. congregata was only significant for hornworms on Potatoe / Datura and not Nicotiana (i.e. 33% vs. 12% vs. 4% parasitism on Potatoe , Datura , and Nicotiana , respectively). Experimental laboratory rearing confirmed that wasp survival is lower on Nicotiana sp. than Solanum lycopersicum , which could be driven by nicotine. The data obtained in the present study show that the negative preference‐performance relationship in hornworms across solanaceous plants is maintained in part because by utilising noxious food plants M. sexta gains protection against parasitism.