Abstract

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.

Highlights

  • Many animals exhibit variation in resistance to specific natural enemies

  • Here we show that pea aphid genomes maintain variation in susceptibility to a common natural enemy, the parasitoid A. ervi

  • With prior work showing that infection with the heritable symbiont H. defensa confers varying levels of protection, depending on strain and phage type, it is clear that this aphid employs multiple strategies to thwart attack from parasitoids

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Summary

Introduction

Many animals exhibit variation in resistance to specific natural enemies. Such variation may be encoded in their genomes or derived from infection with protective symbionts. Simultaneous experimental studies, comparing aphid clones with and without symbionts, found that most H. defensa strains, and a single Serratia symbiotica strain, provided defense against the wasp A. ervi [39,43,44,45] Further investigation of this interaction found that bacteriophages called APSEs were required for H. defensa to confer protection to pea aphids [43,46,47] and that levels of resistance to the wasp varied greatly and correlated with symbiont strain and associated virus type; uninfected aphid clones (i.e. no facultative symbionts), on the other hand, exhibited limited variation in resistance and were highly susceptible to attack [43,44]. Aphid-encoded resistance to parasitism has been reported in the peach-potato aphid, Myzus persicae, and the black bean aphid, Aphis fabae [50,51,52]

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