Research Article: Ethanol confers differential protection against generalist and specialist parasitoids of Drosophila melanogaster

Date Published: July 12, 2017

Publisher: Public Library of Science

Author(s): Zachary R. Lynch, Todd A. Schlenke, Levi T. Morran, Jacobus C. de Roode, Efthimios M. C. Skoulakis.

http://doi.org/10.1371/journal.pone.0180182

Abstract

As parasites coevolve with their hosts, they can evolve counter-defenses that render host immune responses ineffective. These counter-defenses are more likely to evolve in specialist parasites than generalist parasites; the latter face variable selection pressures between the different hosts they infect. Natural populations of the fruit fly Drosophila melanogaster are commonly threatened by endoparasitoid wasps in the genus Leptopilina, including the specialist L. boulardi and the generalist L. heterotoma, and both wasp species can incapacitate the cellular immune response of D. melanogaster larvae. Given that ethanol tolerance is high in D. melanogaster and stronger in the specialist wasp than the generalist, we tested whether fly larvae could use ethanol as an anti-parasite defense and whether its effectiveness would differ against the two wasp species. We found that fly larvae benefited from eating ethanol-containing food during exposure to L. heterotoma; we observed a two-fold decrease in parasitization intensity and a 24-fold increase in fly survival to adulthood. Although host ethanol consumption did not affect L. boulardi parasitization rates or intensities, it led to a modest increase in fly survival. Thus, ethanol conferred stronger protection against the generalist wasp than the specialist. We tested whether fly larvae can self-medicate by seeking ethanol-containing food after being attacked by wasps, but found no support for this hypothesis. We also allowed female flies to choose between control and ethanol-containing oviposition sites in the presence vs. absence of wasps and generally found significant preferences for ethanol regardless of wasp presence. Overall, our results suggest that D. melanogaster larvae obtain protection from certain parasitoid wasp species through their mothers’ innate oviposition preferences for ethanol-containing food sources.

Partial Text

Populations involved in antagonistic interactions often experience episodes of rapid, coupled evolutionary change. Host or prey populations undergo natural selection for new traits that confer enhanced resistance or tolerance against their enemies, and these new traits are repeatedly countered by adaptations in enemy populations. For example, plant defenses can increase in strength due to selection pressures from herbivores [1, 2] and parasites can evolve to avoid or impair host immune responses [3, 4]. However, we expect coevolutionary trajectories to differ between parasites that infect one or a few hosts (specialists) and parasites that infect a broader range of hosts (generalists). Populations of specialist parasites are distributed across narrower host ranges every generation, causing selection pressures to be more consistent across generations. Therefore, antagonistic coevolution is more likely between specialist parasites and their hosts, and specialist parasites will be more likely to counter host defenses than generalist parasites [5, 6].

We investigated whether D. melanogaster larvae can use ethanol for protection against parasitoid wasps. We also tested whether ethanol use is driven by choices at the larval or adult stages and whether its effectiveness differs against generalist vs. specialist wasps. We found that unparasitized second-instar fly larvae were equally likely to survive to adulthood when they consumed 0% or 6% ethanol food (Fig 1), suggesting that ethanol consumption may not carry fitness costs in the absence of parasitoids. A previous study that also used the D. melanogaster wild-type strain Oregon R similarly found that 4% to 8% ethanol food did not affect fly survival [32], although studies using different wild-type strains have found reduced fly survival at ethanol concentrations above 3% [40, 41]. Second-instar larvae that consumed 6% ethanol food in the 24 hours before exposure to wasps were not less likely to be parasitized by the generalist L. heterotoma or the specialist L. boulardi. Consuming ethanol before exposure to L. heterotoma led to lower parasitization intensities and higher fly survival, but food consumed in the 24 hours after exposure had no effect on fly survival against either wasp (Fig 2). When we placed third-instar larvae in 6% ethanol food and immediately exposed them to wasps, parasitization rates and intensities were only reduced for L. heterotoma, although fly survival was higher against both wasp species (Fig 3). However, significantly increased fly survival was only coupled with significantly reduced wasp survival in one scenario, when fly larvae were placed in 6% ethanol food and then immediately exposed to the generalist L. heterotoma (Fig 3C). When ethanol was administered 24 hours before exposure, fly and wasp survival were both significantly increased (Fig 2C). This suggests that constant access to ethanol is highly beneficial to the long-term persistence of D. melanogaster populations threatened by the generalist wasp. Overall, we found that ethanol provides effective protection against the generalist L. heterotoma but limited protection against the specialist L. boulardi, similar to the findings of Milan et al. [32].

 

Source:

http://doi.org/10.1371/journal.pone.0180182

 

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