Vector manipulation by a semi-persistent plant virus through disease symptom expression

The greenhouse whitefly (GWF), Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) is rarely associated with potato plants yet is the only known vector of the Potato yellow vein virus (PYVV). A host shift related with vectors cognition often requires neural alterations by the virus. However, PYVV, being semi-persistent, is not supposed to directly affect vector physiology. As such, we propose that changes in potato plants caused by PYVV infection should manipulate insect behaviour to increase transmission. Here, we studied the effect of PYVV infection and symptom expression on GWF biological parameters, and attraction towards infected and uninfected potato plants. We compared survival and development rates of GWF nymphs fed with PYVV-infected plants (symptomatic and asymptomatic) and healthy plants under controlled conditions. We also carried out free-choice tests to determine host preference of GWF adults as a function of PYVV infection and disease symptom expression. We found that PYVV infection (both symptomatic and asymptomatic) reduce GWF survival while increasing development time (in symptomatic plants). Combined, a prolonged development time and reduced survival should favour viral uptake and trigger migration of vectors from symptomatic plants short after acquiring the virus. We also found that symptom expression (yellowing) causes significantly greater GWF attraction and establishment compared to healthy or asymptomatic plants. Interestingly, we found that GWF adults that have previously fed on infected plants switch their host preference choosing and establishing on healthy potato plants, which clearly increases horizontal transmission rates. The mechanism through which this behavioural manipulation takes place is not yet well understood. Our results show that symptoms associated with PYVV infection may account for a set of behavioural modifications that make an improbable vector, such as the GWF, into an efficient agent that increases horizontal transmission rates of PYVV. HighlightsO_LIPYVD reduces the survival of GWF and increases development time when symptoms occur C_LIO_LIPYVD symptom makes potato, a non-host plant, attractive to GWF C_LIO_LIAfter feeding on infected plants, GWF preference changes to prefer uninfected plants C_LIO_LIPYVV modulates GWF behaviour to enhance horizontal transmission between plants C_LI