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Plant and insect microbial symbionts alter the outcome of plant–herbivore–parasitoid interactions: implications for invaded, agricultural and natural systems
1. Understanding how soil microbial communities influence plant interactions with other organisms,
and how this varies with characteristics of the interacting organisms, is important for multiple systems.
Solanum spp. are a suitable model for trophic interactions in studies of agricultural and natural
systems and can also provide useful corollaries in invaded systems. This study examined the influence
of soil mutualist arbuscular mycorrhizal (AM) fungi on growth of different Solanum types fed
on by the potato aphid, Macrosiphum euphorbiae, in relation to the presence of the aphid facultative
endosymbiont Hamiltonella defensa.
2. Four Solanum types comprising two wild species, S. berthaultii and S. polyadenum, and two
accessions of S. tuberosum, were grown with or without AM fungi and infested with one of four
clonal lines of a single M. euphorbiae genotype (two with and two without H. defensa). Two experiments
were conducted to (i) characterize plant responses to AM fungi and aphids and (ii) assess
whether soil AM fungi could influence the success of the parasitoid wasp Aphidius ervi when attacking
aphids reared on each Solanum type.
3. In both experiments, similar patterns of plant biomass were observed in relation to AM fungal
and aphid treatments. Solanum biomass depended on plant type and aphid infection with H. defensa.
Plants exposed to aphids harbouring H. defensa had smaller root biomass, and therefore total plant
biomass, compared to plants infested with H. defensa-free aphids. M. euphorbiae performance varied
with aphid clonal line, Solanum type and the presence of AM fungi.
4. Parasitoid success, measured as the proportion of aphids from which a wasp emerged, was highest
from aphids that had fed on plants colonized by AM fungi, although this result also varied with
Solanum type and aphid clonal line.
5. Synthesis. The presence of soil AM fungi, combined with within-species plant and insect variation
in key traits, can have subtle – but significant – effects on plant fitness and insect success. This
study highlights the importance of exploring genotypic variation in plant and pest responses to soil
microbiota to identify suitable biocontrol options.
Key-words: aphid, Aphidius ervi, arbuscular mycorrhizal fungi, genotype-by-genotype interaction,
Hamiltonella defensa, invasion ecology, Macrosiphum euphorbiae, multitrophic interaction, plant–
soil (below-ground) interactions, Solanum spp.
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