Symbiont infection affects aphid defensive behaviours

Dion, Emilie; Polin, Sarah; Simon, Jean‐Christophe; Outreman, Yannick

doi:10.1098/rsbl.2011.0249

Cited by 68 publications

(71 citation statements)

References 11 publications

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“…In groups of symbiont-defended aphids, the release of lower amounts of EBF could be adaptive, as dropping from the plant, or dispersing is risky [58] while staying put may be a better strategy if one is likely to survive a parasitoid attack. A recent report found that A. pisum infected with H. defensa exhibited fewer escape behaviors and reduced aggressiveness relative to uninfected counterparts [59], consistent with reduced levels of EBF. More generally, heritable variation in escape behavior among A. pisum clones has been reported [60]; and heritable symbiont influences on EBF titers could explain some of this variation.…”

Section: Discussionmentioning

confidence: 70%

Parasitic wasp responses to symbiont-based defense in aphids

et al. 2012

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Background Recent findings indicate that several insect lineages receive protection against particular natural enemies through infection with heritable symbionts, but little is yet known about whether enemies are able to discriminate and respond to symbiont-based defense. The pea aphid, Acyrthosiphon pisum , receives protection against the parasitic wasp, Aphidius ervi , when infected with the bacterial symbiont Hamiltonella defensa and its associated bacteriophage APSE ( Acyrthosiphon pisum s econdary e ndosymbiont). Internally developing parasitoid wasps, such as A. ervi , use maternal and embryonic factors to create an environment suitable for developing wasps. If more than one parasitoid egg is deposited into a single aphid host (superparasitism), then additional complements of these factors may contribute to the successful development of the single parasitoid that emerges. Results We performed experiments to determine if superparasitism is a tactic allowing wasps to overcome symbiont-mediated defense. We found that the deposition of two eggs into symbiont-protected aphids significantly increased rates of successful parasitism relative to singly parasitized aphids. We then conducted behavioral assays to determine whether A. ervi selectively superparasitizes H. defensa -infected aphids. In choice tests, we found that A. ervi tends to deposit a single egg in uninfected aphids, but two or more eggs in H. defensa -infected aphids, indicating that oviposition choices may be largely determined by infection status. Finally, we identified differences in the quantity of the trans-β-farnesene, the major component of aphid alarm pheromone, between H. defensa -infected and uninfected aphids, which may form the basis for discrimination. Conclusions Here we show that the parasitic wasp A. ervi discriminates among symbiont-infected and uninfected aphids, and changes its oviposition behavior in a way that increases the likelihood of overcoming symbiont-based defense. More generally, our results indicate that natural enemies are not passive victims of defensive symbionts, and that an evolutionary arms race between A. pisum and the parasitoid A. ervi may be mediated by a bacterial symbiosis.

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Section: Discussionmentioning

confidence: 70%

Parasitic wasp responses to symbiont-based defense in aphids

et al. 2012

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“…That aphid behavioral defenses may vary discretely at the subspecific level (aphid clone or higher level, e.g. host plant biotype), particularly in concert with other aphid traits playing a role in parasitism such as color and anti-parasitoid bacterial symbionts has not received much attention ([58] and references therein).…”

Section: Discussionmentioning

confidence: 99%

“…Populations of A. pisum are genetically structured according to host plant [29], but even small populations exhibit discontinuous traits affecting parasitism, in particular anti-parasitoid bacterial symbionts that can modify traits such as aphid body color [62] and behavior [58]. Symbionts are not intrinsic to aphid genetic variation, but aphid hospitality to endosymbiotic bacteria may be a key aspect of aphid genetic variation that deserves further study.…”

Section: Discussionmentioning

confidence: 99%

Survival to Parasitoids in an Insect Hosting Defensive Symbionts: A Multivariate Approach to Polymorphic Traits Affecting Host Use by Its Natural Enemy

et al. 2013

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Insect parasitoids and their insect hosts represent a wide range of parasitic trophic relations that can be used to understand the evolution of biotic diversity on earth. Testing theories of coevolution between hosts and parasites is based on factors directly involved in host susceptibility and parasitoid virulence. We used controlled encounters with potential hosts of the Aphidius ervi wasp to elucidate behavioral and other phenotypic traits of host Acyrthosiphon pisum that most contribute to success or failure of parasitism. The host aphid is at an advanced stage of specialization on different crop plants, and exhibits intra-population polymorphism for traits of parasitoid avoidance and resistance based on clonal variation of color morph and anti-parasitoid bacterial symbionts. Randomly selected aphid clones from alfalfa and clover were matched in 5 minute encounters with wasps of two parasitoid lineages deriving from hosts of each plant biotype in a replicated transplant experimental design. In addition to crop plant affiliation (alfalfa, clover), aphid clones were characterized for color morph (green, pink), Hamiltonella defensa and Regiella insecticola symbionts, and frequently used behaviors in encounters with A. ervi wasps. A total of 12 explanatory variables were examined using redundancy analysis (RDA) to predict host survival or failure to A. ervi parasitism. Aphid color was the best univariate predictor, but was poorly predictive in the RDA model. In contrast, aphid host plant and symbionts were not significant univariate predictors, but significant predictors in the multivariate model. Aphid susceptibility to wasp acceptance as reflected in host attacks and oviposition clearly differed from its suitability to parasitism and progeny development. Parasitoid progeny were three times more likely to survive on clover than alfalfa host aphids, which was compensated by behaviorally adjusting eggs invested per host. Strong variation of the predictive power of intrinsic (body color) and extrinsic traits (symbionts, host plant), indicate that host variables considered as key predictors of outcomes strongly interact and cannot be considered in isolation.

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“…Finally, in addition to their direct effects on aphid and parasitoid survival, symbionts may have indirect effects on food webs, e.g. via manipulating aphid behavioural traits (Dion et al, 2011) in a manner that affects hyperparasitoid foraging success.…”

Section: Discussionmentioning

confidence: 99%

Cascading effects of herbivore protective symbionts on hyperparasitoids

McLean

Hrček

Parker

et al. 2017

Ecological Entomology

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Abstract. 1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity.2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids).3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species.4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid-parasitoid-hyperparasitoid interactions we studied.5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.

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Symbiont infection affects aphid defensive behaviours

Cited by 68 publications

References 11 publications

Parasitic wasp responses to symbiont-based defense in aphids

Parasitic wasp responses to symbiont-based defense in aphids

Survival to Parasitoids in an Insect Hosting Defensive Symbionts: A Multivariate Approach to Polymorphic Traits Affecting Host Use by Its Natural Enemy

Cascading effects of herbivore protective symbionts on hyperparasitoids

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