Symbiont-conferred immunity interacts with effects of parasitoid genotype and intraguild predation to affect aphid immunity in a clone-specific fashion

Abstract

Background: Host-parasite interactions represent complex co-evolving systems in which genetic and associated phenotypic variation within a species can significantly affect selective pressures on traits, such as host immunity, in the other. While often modelled as a two-species interaction between host and parasite, some systems are more complex due to effects of host enemies, intraguild predation, and endosymbionts, all of which affect host immunity. However, it remains unclear how these factors, combined with genetic variation in the host and the parasitoid, affect host immunity. We address this question in an important agricultural pest system, the pea aphid Acyrthosiphon pisum, which shows significant intraspecific variability in immunity to the parasitoid wasp Aphidius ervi. In a complex experiment, we use a quantitative genetic design in the parasitoid, two ecologically different aphid lineages and the aphid lion Chrysoperla carnea as an intraguild predator to unravel the complex interdependencies.

Results: We demonstrate that aphid immunity as a key trait of this complex host-parasite system is affected by intraspecific genetic variation in the parasitoid and the aphid, the interaction of intraspecific genetic variation with intraguild predation, and differences in defensive endosymbionts between aphid lineages. Further, aphid lineages differ in their altruistic behaviour whereby infested aphids move away from the clonal colony to facilitate predation.

Conclusions: Our findings provide new insights into the influence of endosymbiosis and genetic variability in an important host-parasitoid system which is influenced by natural enemies of the parasitoid and the aphid, including its endosymbiont communities. We show that endosymbiosis can mediate or influence the evolutionary arms race between aphids and their natural enemies. The outcome of these complex interactions between species has significant implications for understanding the evolution of multitrophic systems, including eco-agricultural settings.

Keywords: Endosymbiont; Host–parasite system; Indirect ecological effects; Inter-species indirect genetic effects; Intraguild predation; Intraspecific genetic variation effects; Pea aphid.

Fig. 1

Aphid immunity subject to intraguild predation (IGP). The means (± SE) of IR (immunity ratio), representing aphid immunity to the parasitoid wasp, are shown centrally per aphid lineage with (light grey) and without (dark grey) IGP by the aphid lion. IR percentages, without IGP, are shown in dark grey; and in light grey with IGP. Each mean IR proportion is accompanied with detailed IR proportions for IR under the effect of the parasitoid genotype (daughters) that were the result of the Sire x Dam mating system (quantitative genetic design). In the absence of IGP sample sizes were as follows: n = 30 parasitoid daughters in the case of N116, and n = 30 in the case of Q1. In the presence of IGP: n = 43 parasitoid daughters in the case of N116, and n = 15 in the case of Q1. In total, there were 118 parasitoid daughters. The smallest uniform rectangles shown in the detailed IR illustration refer to IR of 0% i.e., lack of immunity

Fig. 2

Proportions of mummies off-plant subject to intraguild predation (IGP). Percentages of aphid mummies (means ± SE) recorded off the plant are shown for N116 and Q1 exposed to the effect of the parasitoid genotype (daughters) in the absence of IGP (dark grey) and the presence of IGP (light grey). Sample sizes were as follows: In the absence of IGP: n = 20 parasitoid daughters in the case of N116, and n = 29 in the case of Q1. In the presence of IGP: n = 19 parasitoid daughters in the case of N116, and n = 13 in the case of Q1. In total there were 81 parasitoid daughters. The smallest uniform rectangles shown in the detailed illustration refer to the off-plant mummy proportion of 0%. The parasitoid genotype (daughters) were the result of the Sire × Dam mating system (quantitative genetic design)

Fig. 3

Experimental design. The diagram shows the full experimental design, with n sires being mated to at least three dams (D1 – Dm). The sire × dam mating groupings produced the intraspecific genetic variability in the parasitoid (genotype/daughters [sibs, and half-sibs]). Overall, there were 119 parasitoid daughters. Each group of daughters of the (S1 – Sn) combinations was then split into two populations, with one (n = 73) being provided with pea aphids of the N116 lineage as a provision, while the other (n = 45) provided with pea aphids of the Q1 lineage. Each of these populations where further split into two groups, with one group exposed to intraguild predation by the aphid lion larva (n = 43, in the case of N116, and n = 15 in the case of Q1) and the other group not (n = 30, in the case of N116, and n = 30 in the case of Q1). The effects of parasitoid and aphid genetic variability (with and without the aphid lion) on aphid immunity ratio (IR) were investigated in microcosms. IR is the proportion of healthy aphids (non-mummified i.e. unparasitoidised) after 11 days of exposure to the parasitoid genotype relative to the entire population of aphids (healthy and mummified) per aphid lineage