Costs and benefits of a superinfection of facultative symbionts in aphids

Abstract

Symbiotic associations between animals and inherited micro-organisms are widespread in nature. In many cases, hosts may be superinfected with multiple inherited symbionts. Acyrthosiphon pisum (the pea aphid) may harbour more than one facultative symbiont (called secondary symbionts) in addition to the obligate primary symbiont, Buchnera aphidicola. Previously we demonstrated that, in a controlled genetic background, A. pisum infected with either Serratia symbiotica or Hamiltonella defensa (called R- and T-type in that study) were more resistant to attack by the parasitoid Aphidius ervi. Here, we examined the consequences of A. pisum superinfected with both resistance-conferring symbionts. We found that an A. pisum line co-infected with both S. symbiotica and H. defensa symbionts exhibits even greater resistance to parasitism by A. ervi than either of the singly infected lines. Despite this added benefit to resistance, superinfections of S. symbiotica and H. defensa symbionts appeared rare in our survey of Utah A. pisum symbionts, which is probably attributable to severe fecundity costs. Quantitative polymerase chain reaction estimates indicate that while the density of H. defensa is similar in singly and superinfected hosts, S. symbiotica densities increased dramatically in superinfected hosts. Over-proliferation of symbionts or antagonistic interactions between symbionts may be harmful to the aphid host. Our results indicate that in addition to host-symbiont interactions, interactions among the symbionts themselves probably play a critical role in determining the distributions of symbionts in natural populations.

Figure 1

Back-transformed logistical regression estimates of reductions in successful parasitism of Acyrthosiphon pisum by Aphidius ervi in singly and superinfected lines relative to the uninfected control line. Numbers above columns represent the total numbers of aphids counted as alive or parasitized (***p<0.001).

Figure 2

Comparison of SS densities in singly versus superinfected A. pisum. (a) Densities of H. defensa in singly infected aphids (light bar) and superinfected aphids (dark bar); (b) the densities of Serratia symbiotica in singly infected aphids (light bar) and superinfected aphids (dark bar).