Abstract
Plants respond to insect attack by releasing blends of volatile chemicals that attract their herbivores’ specific natural enemies, while insect herbivores may carry endosymbiotic microorganisms that directly improve herbivore survival after natural enemy attack. Here we demonstrate that the two phenomena can be linked. Plants fed upon by pea aphids release volatiles that attract parasitic wasps, and the pea aphid can carry facultative endosymbiotic bacteria that prevent the development of the parasitic wasp larva and thus markedly improve aphid survival after wasp attack. We show that these endosymbionts also attenuate the systemic release of volatiles by plants after aphid attack, reducing parasitic wasp recruitment and increasing aphid fitness. Our results reveal a novel mechanism through which symbionts can benefit their hosts and emphasise the importance of considering the microbiome in understanding insect ecological interactions.
Highlights
Plants respond to insect attack by releasing blends of volatile chemicals that attract their herbivores’ specific natural enemies, while insect herbivores may carry endosymbiotic microorganisms that directly improve herbivore survival after natural enemy attack
We investigated whether pea aphids benefit from carrying the symbiont H. defensa by influencing the release of volatiles and reducing parasitic wasp recruitment, and whether any effect on volatile release was localised to the site of aphid attack or systemic
Our study shows that plants infested with aphids carrying different symbiont species and strains are less attractive to the parasitic wasp A. ervi through systemic changes in herbivoreinduced plant volatiles, reducing parasitic wasp recruitment and increasing aphid fitness
Summary
Plants respond to insect attack by releasing blends of volatile chemicals that attract their herbivores’ specific natural enemies, while insect herbivores may carry endosymbiotic microorganisms that directly improve herbivore survival after natural enemy attack. Symbiont-conferred protection against pathogens, parasitic wasps and predators has been demonstrated in a variety of different species, and recent evidence suggests that they can help herbivores overcome specific induced defences mounted by plants in response to insect attack[4]. We studied symbiont-herbivore-natural enemy interactions on the pea aphid (Acyrthosiphon pisum) feeding on the broad bean Vicia faba This plant is known to respond to pea aphid attack by releasing volatiles that attract the parasitic wasp Aphidius ervi, and olfactometer and biochemical studies have identified the specific volatiles that are involved in wasp attraction[11,12,13,14]. We investigated whether pea aphids benefit from carrying the symbiont H. defensa by influencing the release of volatiles and reducing parasitic wasp recruitment, and whether any effect on volatile release was localised to the site of aphid attack or systemic. The species we studied were (i) Regiella insecticola, which typically protects A. pisum from specialist pathogenic fungi but not parasitic wasps[25]; (ii) Spiroplasma sp. which, depending on the particular isolate, may or may not confer protection against wasps[26, 27]; (iii) Serratia symbiotica, which shows some strain-specific parasitic wasp protection[20] and protects aphids from heat shocks[28]; and (iv) Rickettsiella sp., which is less well characterised but is known to influence aphid body colour and possibly attraction to natural enemies[29]
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