Variation in resistance to parasitism in aphids is due to symbionts not host genotype

Abstract

Natural enemies are important ecological and evolutionary forces, and heritable variation in resistance to enemies is a prerequisite for adaptive responses of populations. Such variation in resistance has been previously documented for pea aphids (Acyrthosiphon pisum) attacked by the parasitoid wasp Aphidius ervi. Although the variation was presumed to reflect genotypic differences among the aphids, another potential source of resistance to A. ervi is infection by the facultative bacterial symbiont Hamiltonella defensa. Here, we explored whether variation among symbiont isolates underlies variation among A. pisum clones in resistance to A. ervi. Although maternally transmitted, H. defensa is sometimes horizontally transferred in nature and can be experimentally established in clonal aphid lineages. We established five H. defensa isolates in a common A. pisum genetic background. All of the five isolates tested, including one originating from another aphid species, conferred resistance. Furthermore, isolates varied in levels of resistance conferred, ranging from 19% to nearly 100% resistance. In contrast, a single H. defensa isolate established in five different aphid clones conferred similar levels of resistance; that is, host genotype did not influence resistance level. These results indicate that symbiont-mediated resistance to parasitism is a general phenomenon in A. pisum and that, at least for the isolates and genotypes considered, it is the symbiont isolate that determines the level of resistance, not aphid genotype or any interaction between isolate and genotype. Thus, acquisition of a heritable symbiont appears to be a major mode of adaptation to natural enemy pressure in these insects.

Fig. 1.

Proportion of A. pisum successfully parasitized by A. ervi. Each treatment in these graphs represents different A. pisum clones, each harboring the same H. defensa isolate (NY1). A and B correspond to separate experiments with different A. pisum clones. Numbers above the bars represent the total number of aphids examined (alive plus parasitized).

Fig. 2.

Proportion of A. pisum parasitized by A. ervi. Each treatment in these graphs represents different lineages of the same A. pisum clone (5A), each with a distinct H. defensa isolate. A and B correspond to separate experiments with different H. defensa isolates. Numbers above the bars represent the total number of aphids examined (alive plus parasitized).