A virus drives its vector to virus-susceptible plants at the cost of vector fitness

While it is known that plant viruses can be spread by affecting the behaviour of their invertebrate vectors, it is often unclear if the vectors benefit or suffer from these induced changes. Here we examined behavioural effects of tomato yellow leaf curl virus (TYLCV) on its vector, the whitefly Bemisia tabaci Mediterranean (MED), and measured associated fitness consequences for the whitefly. TYLCV induced a preference in the whitefly for plants that were virus-susceptible (i.e. can be infected with TYLCV and have viral infection symptoms) or virus-tolerant (i.e. can be infected with TYLCV without symptoms) over those that were virus-resistant (virus-free), suggesting that TYLCV benefits from altered vector behaviour. Viruliferous whiteflies which fed on susceptible tomato plants infected by the virus-preferred healthy tomato plants (TYLCV-susceptible) and eggplants which support TYLCV, while non-viruliferous whiteflies preferred TYLCV-infected tomato plants. When non-viruliferous whiteflies became viruliferous after 48 h, they developed a preference for healthy tomato plants. The fitness of whiteflies (irrespective of virus status) was higher on cucumber plants (TYLCVnon-host plant) and eggplants than on tomato and cotton plants, showing a disconnect between host preference and performance. A field survey on changes in TYLCV infection rates across host plants showed an increase in the incidence of viruliferous whiteflies both on tomato plants and eggplants but only minor changes on cucumber plants. These results suggest that TYLCV drives the vector to virus-susceptible plants regardless of vector fitness costs, which could be exploited in management programs aimed at reducing virus-related damage.