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      Parasitic wasp responses to symbiont-based defense in aphids

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          Abstract

          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 secondary endosymbiont). 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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          Most cited references46

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          Facultative bacterial symbionts in aphids confer resistance to parasitic wasps.

          Symbiotic relationships between animals and microorganisms are common in nature, yet the factors controlling the abundance and distributions of symbionts are mostly unknown. Aphids have an obligate association with the bacterium Buchnera aphidicola (the primary symbiont) that has been shown to contribute directly to aphid fitness. In addition, aphids sometimes harbor other vertically transmitted bacteria (secondary symbionts), for which few benefits of infection have been previously documented. We carried out experiments to determine the consequences of these facultative symbioses in Acyrthosiphon pisum (the pea aphid) for vulnerability of the aphid host to a hymenopteran parasitoid, Aphidius ervi, a major natural enemy in field populations. Our results show that, in a controlled genetic background, infection confers resistance to parasitoid attack by causing high mortality of developing parasitoid larvae. Compared with uninfected controls, experimentally infected aphids were as likely to be attacked by ovipositing parasitoids but less likely to support parasitoid development. This strong interaction between a symbiotic bacterium and a host natural enemy provides a mechanism for the persistence and spread of symbiotic bacteria.
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            Variation in resistance to parasitism in aphids is due to symbionts not host genotype.

            Natural enemies are important ecological and evolutionary forces, and heritable variation in resistance to enemies is a prerequisite for adaptive responses of populations. Such variation in resistance has been previously documented for pea aphids (Acyrthosiphon pisum) attacked by the parasitoid wasp Aphidius ervi. Although the variation was presumed to reflect genotypic differences among the aphids, another potential source of resistance to A. ervi is infection by the facultative bacterial symbiont Hamiltonella defensa. Here, we explored whether variation among symbiont isolates underlies variation among A. pisum clones in resistance to A. ervi. Although maternally transmitted, H. defensa is sometimes horizontally transferred in nature and can be experimentally established in clonal aphid lineages. We established five H. defensa isolates in a common A. pisum genetic background. All of the five isolates tested, including one originating from another aphid species, conferred resistance. Furthermore, isolates varied in levels of resistance conferred, ranging from 19% to nearly 100% resistance. In contrast, a single H. defensa isolate established in five different aphid clones conferred similar levels of resistance; that is, host genotype did not influence resistance level. These results indicate that symbiont-mediated resistance to parasitism is a general phenomenon in A. pisum and that, at least for the isolates and genotypes considered, it is the symbiont isolate that determines the level of resistance, not aphid genotype or any interaction between isolate and genotype. Thus, acquisition of a heritable symbiont appears to be a major mode of adaptation to natural enemy pressure in these insects.
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              Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont.

              Recent studies have shown that some plants and animals harbor microbial symbionts that protect them against natural enemies. Here we demonstrate that a maternally transmitted bacterium, Spiroplasma, protects Drosophila neotestacea against the sterilizing effects of a parasitic nematode, both in the laboratory and the field. This nematode parasitizes D. neotestacea at high frequencies in natural populations, and, until recently, almost all infections resulted in complete sterility. Several lines of evidence suggest that Spiroplasma is spreading in North American populations of D. neotestacea and that a major adaptive change to a symbiont-based mode of defense is under way. These findings demonstrate the profound and potentially rapid effects of defensive symbionts, which are increasingly recognized as major players in the ecology of species interactions.
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                Author and article information

                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central
                1741-7007
                2012
                24 February 2012
                : 10
                : 11
                Affiliations
                [1 ]Department of Entomology, University of Georgia, Athens, GA 30605, USA
                [2 ]Department of Biological Production, Akita Prefectural University, Akita, Japan 010-0195
                [3 ]Department of Entomology, University of Arizona, Tucson, AZ 85721, USA
                [4 ]Department of Biosphere 2, University of Arizona, Tucson, AZ 85721, USA
                Article
                1741-7007-10-11
                10.1186/1741-7007-10-11
                3312838
                22364271
                f211da45-d735-4b00-b01d-e28a73894a34
                Copyright ©2012 Oliver et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 5 October 2011
                : 24 February 2012
                Categories
                Research Article

                Life sciences
                Life sciences

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