Aphid behavioral responses to virus‐infected plants are similar despite divergent fitness effects

Abstract

AbstractWe compared the settling preferences and reproductive potential of an oligophagous herbivore, the pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), in response to pea plants, Pisum sativum L. cv. ‘Aragorn’ (Fabaceae), infected with two persistently transmitted viruses, Pea enation mosaic virus (PEMV) and Bean leaf roll virus (BLRV), that differ in their distribution within an infected plant. Aphids preferentially oriented toward and settled on plants infected with PEMV or BLRV in comparison with sham‐inoculated plants (plants exposed to herbivory by uninfected aphids), but aphids did not discriminate between plants infected with the two viruses. Analysis of plant volatiles indicated that plants inoculated with either virus had significantly higher green leaf volatile‐to‐monoterpene ratios. Time until reproductive maturity was marginally influenced by plant infection status, with a trend toward earlier nymph production on infected plants. There were consistent age‐specific effects of plant infection status on aphid fecundity: reproduction was significantly enhanced for aphids on BLRV‐infected plants across most time intervals, though mean aphid fecundity did not differ between sham and PEMV‐infected plants. There was no clear pattern of age‐specific survivorship; however, mean aphid lifespan was reduced on plants infected with PEMV. Our results are consistent with predictions of the host manipulation hypothesis, extended to include plant viruses: non‐viruliferous A. pisum preferentially orient to virus‐infected host plants, potentially facilitating pathogen transmission. These studies extend the scope of the host manipulation hypothesis by demonstrating that divergent fitness effects on vectors arise relative to the mode of virus transmission.