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

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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01991-1.