Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles

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.

Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids*

“…Even though we find little evidence for protection against A. ervi in the present study, it should be added that Spiroplasma may still reduce the risk of parasitism indirectly via a plant‐mediated effect, because A. ervi is more attracted to volatiles from plants infested by Spiroplasma ‐free aphids than from plants with Spiroplasma ‐infected aphids, as recently shown by Frago et al. (). Such an effect would have been missed by our non‐choice assays.…”

Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection

“…Other widespread endosymbionts of arthropods are bacteria of the genus Spiroplasma , infecting 4%–7% of species, often with a low prevalence (Duron et al, ; Regassa, ), although prevalence can be high in some cases, such as in Myrmica ants (Ballinger, Moore, & Perlman, ) and in Harmonia axyridis (Goryacheva, Blekhman, Andrianov, Romanov, & Zakharov, ). Known effects of Spiroplasma also include reproductive parasitism (e.g., Anbutsu, Lemaitre, Harumoto, & Fukatsu, ; Sanada‐Morimura, Matsumura, & Noda, ; Tabata et al, ) as well as defence against at least three different kinds of parasites (Ballinger & Perlman, ; Frago et al, ; Lukasik, Guo, Van Asch, Ferrari, & Godfray, ; Xie, Butler, Sanchez, & Mateos, ).…”

“…A symbiont that experiences solely vertical transmission can persist in a host population as a reproductive parasite, or by providing a benefit to offset the cost it inflicts on the host. For example, Spiroplasma may protect pea aphids against entomopathogenic fungi (Lukasik, van Asch, Guo, Ferrari, & Godfray, ) or parasitoid wasps (Frago et al, ). However, this cost‐benefit balance varies depending on the environment, which is thought to be the main reason for the observed polymorphism of facultative symbiont communities.…”

Metacommunity theory for transmission of heritable symbionts within insect communities

“…The microbiome is a broad term that defines the microscopic, symbiotic organisms associated with a particular host, and which can provide essential services for their host (e.g., aiding in immunity and digestion), thus providing insight into the health of the host organism (Fierer et al, ). The microbiome can have strong influence on the ecological niche occupied by the host species (Henry, Maiden, Ferrari, & Godfray, ; Hoffmann, Ross, & Rašić, ), and these symbiont‐induced changes to host ecology have increasingly clear impacts on the identity, strength, and outcome of interactions between hosts within communities (Berry & Widder, ; Cusumano et al, ; Frago, Dicke, & Godfray, ; Frago et al, ; Hrček, McLean, & Godfray, ; McLean, Parker, Hrček, Henry, & Godfray, ; Oliver, Smith, & Russell, ; Xie, Vilchez, & Mateos, ; Zhu et al, ). Understanding the spatiotemporal distribution and function of symbiont communities therefore has implications for basic and applied ecological theory.…”