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.

Indirect ecological effects interact with community genetic effects in a host-parasite system and dramatically reduce parasite burden.

Community genetic (CG) effects and ecological factors create a complex set of interactions that are key drivers of evolutionary dynamics in ecological systems. To date, most studies investigating trait variation have focused on either effects of intraspecific genetic variation or on genotype by environment (GxE) interactions in isolation. Poorly investigated but very important are the interactions between CGs and indirect ecological effects (IEEs) that are caused by plant-soil interactions. Here, we tested how CGs in a cabbage host and its aphid parasite depended on the ecological conditions under which the host was grown. We established microcosms of different cabbage cultivars and aphid genotypes on soils inoculated with samples of other soils previously trained with onion. We hypothesized that such IEEs will have significantly different outcomes for ecosystems than predicted from simpler CG or GxE studies. Our analysis demonstrated a large IEE that differed by context and aphid genotype causing reduced parasite population sizes by up to 90%. The IEE is induced by insect-repellent properties and the microbiome of the onion. Our results highlight the importance of interacting IEEs and CGs for ecosystems dynamics showing that IEEs offer sustainable solutions by dramatically reducing parasite burden on cash crops.

Novel resilience in response to revitalisation after exposure to lethal salinity causes differential reproductive success in an extremely plastic organism.

Phenotypic plasticity is central to an organism's ability to adapt to variable environmental conditions. For aquatic organisms, exposure to elevated salt levels poses a challenge and organisms may fail to tolerate or survive much higher levels short-term. Here we demonstrate, for the first time, in a laboratory study of Daphnia magna that exposure to levels of salinity higher than those previously shown to lead to apparent death (paralysis) can be reversed following a transfer to optimal conditions. We established experimental populations from one clone of D. magna, each with five replicates, that were exposed to different short periods of three different lethal levels of salinity (12.27 PSU [45, 60, 90 and 120 min], 18.24 PSU [45, 60 and 90 min] and 24.22 PSU [45, 60 and 90 min]). In all populations, all individuals were paralysed at the end of their exposure, usually classified in the literature as dead. Subsequently, all individuals were transferred to optimal conditions. However, after the transfer, a proportion of the individuals not only came back from the verge of death (i.e. were revitalised), but also showed afterwards differential reproductive success over a period of 20 days, depending on the level and the length of exposure before revitalisation. Both exposure level and time had an overall negative effect on population size that differed across all treatments. Revitalisation occurred within an hour after the transfer to optimal conditions for 18.24 PSU but took 14-16 h for 12.27 PSU. There was no instantaneous revitalisation nor was there any revitalisation after 16 h no matter how long the paralysed Daphnia individuals were left in the optimal conditions. Our findings cast new light on resilience in cladocerans and suggest that abrupt environmental change can reveal novel plastic responses to extreme conditions.