Symbiotic relationships between animals and microorganisms are common in nature, yet the factors controlling the abundance and distributions of symbionts are mostly unknown. Aphids have an obligate association with the bacterium Buchnera aphidicola (the primary symbiont) that has been shown to contribute directly to aphid fitness. In addition, aphids sometimes harbor other vertically transmitted bacteria (secondary symbionts), for which few benefits of infection have been previously documented. We carried out experiments to determine the consequences of these facultative symbioses in Acyrthosiphon pisum (the pea aphid) for vulnerability of the aphid host to a hymenopteran parasitoid, Aphidius ervi , a major natural enemy in field populations. Our results show that, in a controlled genetic background, infection confers resistance to parasitoid attack by causing high mortality of developing parasitoid larvae. Compared with uninfected controls, experimentally infected aphids were as likely to be attacked by ovipositing parasitoids but less likely to support parasitoid development. This strong interaction between a symbiotic bacterium and a host natural enemy provides a mechanism for the persistence and spread of symbiotic bacteria.

Aphids engage in symbiotic associations with a diverse assemblage of heritable bacteria. In addition to their obligate nutrient-provisioning symbiont, Buchnera aphidicola, aphids may also carry one or more facultative symbionts. Unlike obligate symbionts, facultative symbionts are not generally required for survival or reproduction and can invade novel hosts, based on both phylogenetic analyses and transfection experiments. Facultative symbionts are mutualistic in the context of various ecological interactions. Experiments on pea aphids (Acyrthosiphon pisum) have demonstrated that facultative symbionts protect against entomopathogenic fungi and parasitoid wasps, ameliorate the detrimental effects of heat, and influence host plant suitability. The protective symbiont, Hamiltonella defensa, has a dynamic genome, exhibiting evidence of recombination, phage-mediated gene uptake, and horizontal gene transfer and containing virulence and toxin-encoding genes. Although transmitted maternally with high fidelity, facultative symbionts occasionally move horizontally within and between species, resulting in the instantaneous acquisition of ecologically important traits, such as parasitoid defense.

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 waspAphidius ervi. Although the variation was presumed to reflect genotypic differences among the aphids, another potential source of resistance toA. erviis infection by the facultative bacterial symbiontHamiltonella defensa. Here, we explored whether variation among symbiont isolates underlies variation amongA. pisumclones in resistance toA. ervi. Although maternally transmitted,H. defensais sometimes horizontally transferred in nature and can be experimentally established in clonal aphid lineages. We established fiveH. defensaisolates in a commonA. pisumgenetic 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 singleH. defensaisolate 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 inA. pisumand 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.

Attacks Wasps: The bacterium Hamiltonella defensa infects aphids and carries virulence determinants from a bacteriophage virus. Oliver et al. (p. 992 ) have now found that the toxin-bearing phage does not harm the aphid host of the bacterium, but targets the larvae of parasitoid wasps that infest the aphids. If an aphid population is not infested by wasps, the allied bacteriophage is shed by the bacterium, presumably because there is a cost to carrying it. If the wasps then resume their predation, the aphids are no longer protected and succumb to the parasitoid.

Vertically transmitted micro-organisms can increase in frequency in host populations by providing net benefits to hosts. While laboratory studies have identified diverse beneficial effects conferred by inherited symbionts of insects, they have not explicitly examined the population dynamics of mutualist symbiont infection within populations. In the pea aphid,Acyrthosiphon pisum, the inherited facultative symbiont,Hamiltonella defensa, provides protection against parasitism by the wasp,Aphidius ervi. Despite a high fidelity of vertical transmission and direct benefits of infection accruing to parasitized aphids,Hamiltonellaremains only at intermediate frequencies in natural populations. Here, we conducted population cage experiments to monitor the dynamics ofHamiltonellaand of another commonA. pisumsymbiont,Serratia symbiotica, in the presence and absence of parasitism. We also conducted fitness assays ofHamiltonella-infected aphids to search for costs to infection in the absence of parasitism. In the population cages, we found that the frequency ofA. pisuminfected withHamiltonellaincreased dramatically after repeated exposure to parasitism byA. ervi, indicating that selection pressures from natural enemies can lead to the increase of particular inherited symbionts in insect populations. In our laboratory fitness assays, we did not detect a cost to infection withHamiltonella, but in the population cages not exposed to parasitism, we found a significant decline in the frequency of bothHamiltonellaandSerratia. The declining frequencies ofHamiltonella-infected aphids in population cages in the absence of parasitism indicate a probable cost to infection and may explain whyHamiltonellaremains at intermediate frequencies in natural populations.