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First published online December 14, 2005
Journal of Experimental Biology 209, vi (2006)
Copyright © 2006 The Company of Biologists Limited
doi: 10.1242/jeb.01998
Outside JEB |
ON FABACEAE, NO ONE CAN HEAR YOU SCREAM
University of Texas at Austin
art.woods{at}mail.utexas.edu
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One of the more gruesome Hollywood subgenres is the alien-parasite thriller, the signature moment of which is undoubtedly the `birth' scene from Alien (1979). What the public doesn't suspect is how disturbingly real these scenarios can be, at least for insects. All herbivorous insect species are parasitized by one or more species of parasitoids, usually flies or wasps. Female parasitoids lay eggs in, on or near the intended host, and the young parasitoid, if it establishes itself successfully, eats host tissues and may ultimately consume it from the inside out. The sight of Cotesia wasp larvae emerging from barely living Manduca caterpillars is enough to make any horror director smile.
Parasitism poses a conundrum, because insects are not always defenceless - for example, Drosophila possess an immune system that sometimes encapsulates (and thereby kills) parasitoid eggs deposited in its blood. Why then don't all insects resist such an important and persistent source of mortality? One intriguing possibility is that maintaining a vigilant, effective immune system imposes costs that may not always be worth paying.
Gwynn and colleagues studied this problem in the pea aphid (Acyrthosiphon pisum), a pest on legumes (Fabaceae). Pea aphids host a number of wasp parasitoids, among them Aphidius ervi. When A. ervi oviposits into an aphid, the egg doesn't always hatch, but not because aphids possess a Drosophila-style encapsulation response. Rather, the wasp egg simply fails to develop and ends up breaking down. Why? Current thinking implicates endosymbiotic bacteria. Pea aphids often carry bacteria known as PASS(R) and PABS(T), and experimental infection of aphids with these bacteria confers increased resistance to parasitoids. Why then don't all aphids carry PASS(R) and PABS(T)? Perhaps the resistance they confer is offset by other fitness costs.
The team present a direct test of this idea. They collected aphids from the wild and established clonal lineages on bean plants. The authors first confined aphids from each clone for six hours on bean plants together with mated female A. ervi. To determine the clones' resistance to A. ervi, the authors counted aphid survivors and `mummies' (containing wasps) 10 days later. To determine each clone's fecundity, they placed aphids from each clone on bean plants and left them unmolested for several days, after which they counted the aphid offspring. Resistance and fecundity showed a clear inverse relationship - clones with the highest number of offspring had low resistance to A. ervi.
What mechanism underlies this trade-off? Gwynn and coworkers suspect, but did not show, that it's mediated by PASS(R) and PABS(T) bacteria. Such a role would be consistent with prior work showing that experimentally induced infection with these bacteria boosts resistance to parasitoids and with other recent work showing that PASS(R) and PABS(T) infections lower aphid fecundity and longevity. Indeed, PASS(R) and PABS(T) are known to reduce intra-aphid population sizes of obligate endosymbiotic Buchnera aphidicola bacteria, which likely provide nutrients to their aphid hosts. Gwynn et al. speculate that the resistance-fecundity trade-off is mediated via bacterial interactions - that PASS(R) and PABS(T) provide resistance at the cost of obtaining fewer offspring-destined nutrients from Buchnera. More broadly, the authors suggest that variation in resistance stems from temporal and spatial variation in selection on survival and fecundity. Pity the aphid, whose fate appears increasingly determined by competing alien genomes.
References
Gwynn, D. M., Callaghan, A., Gorham, J., Walters, K. F. A. and Fellowes, M. D. E. (2005). Resistance is costly: trade-offs between immunity, fecundity and survival in the pea aphid. Proc. R. Soc. Lond. B 272,1803 -1808.[Medline]
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