Facultative bacterial symbionts in aphids confer resistance to parasitic wasps

Abstract

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.

Figure 1

Effect of SS infection on susceptibility of A. pisum to parasitism by A. ervi. Each value is the mean number of mummies (= successful parasitism) out of a possible 30, ± SE. In all experiments, the same aphid clonal lineage served as a source of uninfected aphids and as a recipient for artificial infection with the U-, R-, or T-type SS. Aphids infected with either the R- or the T- type SS were significantly less likely to succumb to parasitism. Numbers above columns are replicates (N). *, P < 0.05; ***, P < 0.001.

Figure 2

Comparison of the mean number of A. ervi eggs found (within 4 h of oviposition) and the mean number of mummies formed (10 days postoviposition) in singly parasitized R- and T-infected A. pisum vs. uninfected controls. A. ervi were as likely to oviposit in aphids infected with the R- and T-type SS as in uninfected controls (CON), but significantly fewer progeny developed to pupation (P value < 0.0001). Numbers above columns are replicates (N).

Figure 3

Percent of A. ervi larvae found in singly parasitized hosts and the percent of found larvae that were healthy in R-infected A. pisum vs. uninfected controls. Dissections were performed during the interval between 3 and 4 days and between 4 and 5 days. Significantly fewer larvae in R-infected aphids were healthy at 4–5 days; the remainder were dead or moribund. For R-infected aphids, n = 177 for 3–4 days and 223 for 4–5 days, whereas for uninfected aphids, n = 180 for 3–4 days and 215 for 4–5 days. ***, P < 0.001.