Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts

Dion, Emilie; Zélé, Flore; Simon, Jean‐Christophe; Outreman, Yannick

doi:10.1111/j.1420-9101.2010.02207.x

Cited by 76 publications

(94 citation statements)

References 57 publications

(74 reference statements)

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“…Such specificity in genotype by genotype interactions may be directed toward either aphid- or symbiont-based components of resistance, and while duplicated services may not provide an advantage against the average wasp genotype, it may provide protection against a wider range of enemy genotypes. As mentioned above, the wasp A. ervi appears capable of evolving virulence toward symbiont-based protection [74], but it is unclear if it can do so against aphid-based defenses. Such genotype by genotype interactions have been best studied in the black bean aphid- H. defensa-L. fabarum interaction, where they occur between parasitoid genotypes and defensive symbiont strains, but have not been found between parasitoid and uninfected host genotypes [52,86,87].…”

Section: Discussionmentioning

confidence: 99%

“…Prior studies have shown that isofemale lines of A. ervi wasps can vary in their counter-resistance (i.e. virulence), defined as their ability to successfully parasitize pea aphids [73], suggesting also that virulence, at least toward symbiont-mediated resistance, may evolve rapidly [74]. Although we have not observed substantial variation in wasp virulence (Oliver, personal observation), we designed our parasitism assays to minimize such potential effects.…”

Section: Methodsmentioning

confidence: 99%

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Aphid-encoded variability in susceptibility to a parasitoid

et al. 2014

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BackgroundMany animals exhibit variation in resistance to specific natural enemies. Such variation may be encoded in their genomes or derived from infection with protective symbionts. The pea aphid, Acyrthosiphon pisum, for example, exhibits tremendous variation in susceptibility to a common natural enemy, the parasitic wasp Aphidius ervi. Pea aphids are often infected with the heritable bacterial symbiont, Hamiltonella defensa, which confers partial to complete resistance against this parasitoid depending on bacterial strain and associated bacteriophages. That previous studies found that pea aphids without H. defensa (or other symbionts) were generally susceptible to parasitism, together with observations of a limited encapsulation response, suggested that pea aphids largely rely on infection with H. defensa for protection against parasitoids. However, the limited number of uninfected clones previously examined, and our recent report of two symbiont-free resistant clones, led us to explicitly examine aphid-encoded variability in resistance to parasitoids.ResultsAfter rigorous screening for known and unknown symbionts, and microsatellite genotyping to confirm clonal identity, we conducted parasitism assays using fifteen clonal pea aphid lines. We recovered significant variability in aphid-encoded resistance, with variation levels comparable to that contributed by H. defensa. Because resistance can be costly, we also measured aphid longevity and cumulative fecundity of the most and least resistant aphid lines under permissive conditions, but found no trade-offs between higher resistance and these fitness parameters.ConclusionsThese results indicate that pea aphid resistance to A. ervi is more complex than previously appreciated, and that aphids employ multiple tactics to aid in their defense. While we did not detect a tradeoff, these may become apparent under stressful conditions or when resistant and susceptible aphids are in direct competition. Understanding sources and amounts of variation in resistance to natural enemies is necessary to understand the ecological and evolutionary dynamics of antagonistic interactions, such as the potential for coevolution, but also for the successful management of pest populations through biological control.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Aphid-encoded variability in susceptibility to a parasitoid

et al. 2014

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“…This report provides evidence that natural enemies are sometimes able to counteract symbiont-based defense. Recent reports have documented: 1) the evolution of increased A. ervi virulence when faced with symbiont-carrying resistant A. pisum lines [44] and 2) genotypic variation in the parasitoid Lysiphlebus fabarum 's ability to successfully parasitize H. defensa -infected Aphis fabae (black bean aphid) [16]. The experimental design of these studies, however, does not allow conclusive partitioning of increased virulence towards symbiont- versus host-based defensive factors, but these reports do indicate that parasitic wasps likely have additional mechanisms for overcoming symbiont-based resistance.…”

Section: Discussionmentioning

confidence: 99%

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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“…While parasitoids, including A . ervi , have been shown to rapidly evolve counter-resistance specific to symbiont-based defenses [47, 50, 51], this mechanism also appears insufficient to explain the rapid turnover observed. It is also possible that some unknown factor, such as disease, contributed to the rapid decline in P .…”

Section: Discussionmentioning

confidence: 99%

Aphid symbionts and endogenous resistance traits mediate competition between rival parasitoids

et al. 2017

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Insects use endogenous mechanisms and infection with protective symbionts to thwart attacks from natural enemies. Defenses that target specific enemies, however, potentially mediate competition between rivals and thereby impact community composition. Following its introduction to North America to control pea aphids (Acyrthosiphon pisum), the parasitoid Aphidius ervi competitively displaced other parasitoids, except for the native Praon pequodorum. The pea aphid exhibits tremendous clonal variation in resistance to A. ervi, primarily through infection with the heritable bacterial symbiont Hamiltonella defensa, although some symbiont-free aphid genotypes encode endogenous resistance. Interestingly, H. defensa strains and aphid genotypes that protect against A. ervi, provide no protection against the closely related, P. pequodorum. Given the specificity of aphid defenses, we hypothesized that aphid resistance traits may contribute to the continued persistence of P. pequodorum. We conducted multiparasitism assays to determine whether aphid resistance traits mediate internal competition between these two solitary parasitoid species, but found this was not the case; P. pequodorum was the successful internal competitor across lines varying in susceptibility to A. ervi. Next, to determine whether resistance traits influence competitive interactions resulting in the stable persistence of P. pequodorum, we established replicated cages varying in the proportion of resistant aphids and recorded successful parasitism for each wasp species over time. As expected, A. ervi outcompeted P. pequodorum in cages containing only susceptible aphids. However, P. pequodorum not only persisted, but was the superior competitor in populations containing any proportion (20–100%) of resistant aphids (20–100%). Smaller scale, better replicated competition cage studies corroborated this finding, and no-competition and behavioral assays provide insight into the processes mediating competition. Genetic variation, including that acquired via infection with protective symbionts, may provide a supply of hosts susceptible only to particular enemies, mediating competition with effects on community richness and stability.

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Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts

Cited by 76 publications

References 57 publications

Aphid-encoded variability in susceptibility to a parasitoid

Aphid-encoded variability in susceptibility to a parasitoid

Parasitic wasp responses to symbiont-based defense in aphids

Aphid symbionts and endogenous resistance traits mediate competition between rival parasitoids

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