Host plant effects on the outcomes of defensive symbioses in the pea aphid complex

Abstract

There is increasing evidence that microbial symbionts play pivotal roles in protecting their hosts. Most studies on defensive symbioses have analyzed interaction effects of host-symbiont genotypes on fitness value of defense but very few have considered how local environment could influence symbiont-mediated phenotypes. Our study assessed the effects of environmental variation on the intensity and cost of protection against adverse organisms in lineages of the pea aphid, Acyrthosiphon pisum differing by their composition in secondary symbionts. This aphid is frequently infected by Hamiltonella defensa, singly or in co-infection with Fukatsuia symbiotica, and both bacterial symbionts generally confer a resistance against parasitoids but also induce fitness costs to their hosts. The pea aphid forms a complex of plant-adapted biotypes, each specialized on one or a few legume species (i.e., native host). These biotypes can all feed on broad bean, considered as a “universal” host plant. Since plants constitute the primary environment of aphids in providing both habitat and resources, we tested if symbiont-mediated protection was influenced by whether plant-specialized aphids fed on their native or universal hosts. For this purpose, parasitism resistance as well as constitutive and induced fitness costs of 21 pea aphid lineages differing in biotype and symbiotic complement were measured on both native and universal host plants. We showed that host plant could exert some influence on the outcomes of symbiotic defenses: while the host plant species had very little effect on the protection level against parasitoids, we showed that both costs of symbiotic association and costs induced by parasitism challenge varied in a plant-dependent manner.