Adaptation via Symbiosis: Recent Spread of a
            <i>Drosophila</i>
            Defensive Symbiont

Jaenike, John; Unckless, Robert L.; Cockburn, Sarah N.; Boelio, Lisa M.; Perlman, Steve J.

doi:10.1126/science.1188235

Cited by 478 publications

(553 citation statements)

References 36 publications

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“…While documented fitness benefits of symbionts have been primarily nutritional, a number of recent studies have reported protective effects of symbiont infection, suggesting that defense against natural enemies may be another major route facilitating invasion of heritable symbionts into host populations [5-7]. Insect symbionts of diverse bacterial lineages have been shown to provide substantial protection against fungal pathogens [8,9], viruses [10,11], predators [12,13], parasitoids [14-17] and parasitic nematodes [18]. Despite increasing awareness of the roles of these bacteria in protecting hosts, little is known about natural enemy responses to this line of defense.…”

Section: Introductionmentioning

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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Section: Introductionmentioning

confidence: 99%

Parasitic wasp responses to symbiont-based defense in aphids

et al. 2012

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“…Although our results do not allow us to distinguish between these, observation of similar effects of two Spiroplasma strains (MSRO and hy1; poulsonii clade), in two distantly related Drosophila hosts (D. hydei and D. melanogaster) against two congeneric but distantly related parasitoid wasps (Lh and Lb), suggests that the mechanism might be quite general. Furthermore, the mycophagous fly D. neotestacea harbors a non-male-killing Spiroplasma strain (also within the poulsonii clade) that inhibits growth of Howardula aoronymphium, a parasitic nematode of adult hemocoel (Jaenike et al, 2010b). Thus, assuming the same mechanism is responsible for growth inhibition of the two types of endo-macroparasites (i.e., wasps and nematodes), this trait may have been present in the ancestor of the poulsonii clade, which includes male-killing and non-male-killing strains associated with several other species of Drosophila (e.g., D. nebulosa, D. willistoni and D. simulans; Haselkorn et al, 2009).…”

Section: Wasp-killing Mechanismmentioning

confidence: 99%

“…Several bacterial symbionts of aphids confer protection against parasitoid wasps (Oliver et al, 2003(Oliver et al, , 2005Vorburger et al, 2009) and fungi (Scarborough et al, 2005;Lukasik et al, 2012). Spiroplasma bacteria confer protection against fungi in the pea aphid (Lukasik et al, 2012), against a nematode in Drosophila neotestacea (Jaenike et al, 2010b) and against a parasitoid wasp in Drosophila hydei . Wolbachia has been shown to increase resistance or tolerance of Drosophila and mosquitoes against RNA viruses and against the protozoan parasite Plasmodium (Hedges et al, 2008;Teixeira et al, 2008;Moreira et al, 2009;Osborne et al, 2009;Bian et al, 2010;Frentiu et al, 2010;Zele et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

et al. 2013

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Maternally transmitted associations between endosymbiotic bacteria and insects are diverse and widespread in nature. Owing to imperfect vertical transmission, many heritable microbes have evolved compensational mechanisms to enhance their persistence in host lineages, such as manipulating host reproduction and conferring fitness benefits to host. Symbiont-mediated defense against natural enemies of hosts is increasingly recognized as an important mechanism by which endosymbionts enhance host fitness. Members of the genus Spiroplasma associated with distantly related Drosophila hosts are known to engage in either reproductive parasitism (i.e., male killing) or defense against natural enemies (the parasitic wasp Leptopilina heterotoma and a nematode). A male-killing strain of Spiroplasma (strain Melanogaster Sex Ratio Organism (MSRO)) co-occurs with Wolbachia (strain wMel) in certain wild populations of the model organism Drosophila melanogaster. We examined the effects of Spiroplasma MSRO and Wolbachia wMel on Drosophila survival against parasitism by two common wasps, Leptopilina heterotoma and Leptopilina boulardi, that differ in their host ranges and host evasion strategies. The results indicate that Spiroplasma MSRO prevents successful development of both wasps, and confers a small, albeit significant, increase in larva-toadult survival of flies subjected to wasp attacks. We modeled the conditions under which defense can contribute to Spiroplasma persistence. Wolbachia also confers a weak, but significant, survival advantage to flies attacked by L. heterotoma. The host protective effects exhibited by Spiroplasma and Wolbachia are additive and may provide the conditions for such cotransmitted symbionts to become mutualists. Occurrence of Spiroplasma-mediated protection against distinct parasitoids in divergent Drosophila hosts suggests a general protection mechanism.

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“…In insects, bacterial symbionts can improve host fitness, and recent studies have shown that these symbionts respond to the selection on their host's phenotype by increasing in frequency, hence permitting the adaptation of the host [4][5][6][7][8] . For example, within a few years, a strain of a maternally transmitted bacterium belonging to the Spiroplasma genus has invaded many North American populations of its host, Drosophila neotestacea, because of the protection it provides against a parasitic nematode 6 .…”

mentioning

confidence: 99%

“…Again, such conflicts are well-described in insect-bacterium associations. Indeed, several bacteria that have recently been shown to be involved in host adaptation were previously known as parasitic manipulators of sex determinism and reproduction (for example, REFS 5,6). Conflicts may even occur when components of inclusive inheritance are transmitted in the same manner.…”

mentioning

confidence: 99%