Pea-adapted biotype of the aphid Acyrthosiphon pisum induces susceptibility of pea to non-adapted biotype enabling improved feeding and performance

Abstract

Most insect herbivores are adapted to feed on a few host plants only, but the mechanisms underlying plant specialization are poorly understood. One of the dominant hypotheses is that insects inject an oral secretion into the plant that manipulates the plants defences resulting in induced susceptibility. We tested this hypothesis on the pea aphid (Acyrthosiphon pisum), which forms multiple biotypes, each specialized on specific legume hosts. In particular, we tested whether a pea-adapted biotype can induce host susceptibility on pea, which should positively affect the fitness of a non-pea-adapted biotype. We found that survival and fecundity of an alfalfa-adapted biotype on pea were enhanced by co-infestation but not pre-infestation with a pea-adapted biotype. The electrical penetration graph (EPG) method was then used to dissect the components of alfalfa biotype feeding behaviour on pea with and without co-infestation by the pea biotype. While probing time did not differ between these two conditions, differences were observed in most other EPG parameters. When co-infested with the pea-adapted biotype, the alfalfa-adapted biotype was more likely to establish a phloem feeding and exhibited a longer ingestion time on pea. Our results clearly indicated that the pea-adapted biotype induced pea susceptibility by increasing the accessibility of non-pea-adapted aphids to the host phloem sap, and as a result, the alfalfa biotype increased its survival rate and fecundity. These results contribute to understanding how aphids manipulate their specific host plants.