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Tricky parasites winning the evolutionary arms race

Two papers this week describe recently discovered sophisticated adapatations of two different parasites: Gall insects can avoid and alter indirect plant defenses, published in New Phytologist by John Tooker and colleagues, and Parasite-induced fruit mimicry in a tropical canopy ant, published in American Naturalist by Steve Yanoviak and colleagues (if you're in a hurry, skip to the end for amazing photos).

Various plants recruit "bodyguards" when attacked by insects. For example, when caterpillars start munching on corn (maize) plants, the plants (including uninjured leaves) release gaseous chemicals called terpenoids. These terpenoids attract parasitic wasps, which lay their eggs into the caterpillars. This eventually kills the caterpillars, which presumably benefits the plant. But what if the caterpillars could prevent the plant from signaling to the wasps? As far as I know, caterpillars haven’t evolved this trick (yet), but there are apparently some insects – the Hessian fly, Mayetiola destructor (say) – that do not trigger signaling when they feed on wheat plants. There are at least two possible explanations…

1) Maybe the plants don’t detect flies as well as they do caterpillars. This was a plausible hypothesis, because the plants detect specific chemicals in caterpillar saliva, not just the damage they cause.
2) Maybe the flies actively suppress signaling somehow. If so, then you might expect reduced production of volatiles from plants attacked by caterpillars, if they were attacked by signal-suppressing flies first. However, plants attacked by caterpillars increased total daytime production of volatiles about the same amount, whether or not they were also attacked by flies. Some specific chemicals apparently decreased with flies+caterpillars, however, relative to caterpillars alone, so that might affect signaling.

This week’s first paper looked at a similar phenomenon in goldenrod (Solidago) attacked by various insects. Three of the four insect species triggered no increase in volatiles. Caterpillars did trigger volatile release, but this signaling response to caterpillars was less if the plant was also under attack by the gall-forming fly Eurosta (no relation to the train, for those of you with Boston accents). Does preventing signaling in response to caterpillars reduce predation on helpless fly larvae, developing inside galls? If, so it is interesting that another gall-forming species did not suppress signaling in response to caterpillar damage. Gall-formers manipulate the biochemistry of their plant hosts so much anyway, to make them form galls, that effects on volatile signaling could be a side-effect, rather than the result of active manipulation of the “distress signal? pathway.

I don't know whether anyone has worked out the evolutionary history of plant-to-bodyguard signaling. My guess is that all insect-damaged plants release some volatile chemicals, which predatory insects (or parasites that lay their eggs in plant-eating insects) evolved the ability to detect and follow to their prey. That then selected for plants that produce even more of the volatile chemical -- "Hey! I've got more caterpillars than those other plants!" (whether or not that's true) -- at which point it seems reasonable to call it a signal. Someone has genetically engineered plants to produce these signals even when they're not under attack, as a possible form of ecological pest control. This isn't necessarily a good idea, for reasons I'll explain in my book on Darwinian Agriculture.

Parasites manipulate their hosts in other ways as well. Host with brains may have their behavior manipulated. For example, Toxoplasma gondii infects rats, but then needs to move to a cat to complete its life cycle. So it manipulates the rats (presumably by producing a hormone-like chemical) so that they are less afraid of cats. T. gondii also infects humans, and there may even be cultural differences among societies, depending on the frequency of infection. It sounds like science fiction, and Biology in Science Fiction (among my favorite blogs) has additional examples.

But there's nothing fictitious about this week's second paper. In this case, the parasite is a tiny worm-like nematode that infects ants. The ants actually infect their own larvae by feeding them a diet that includes bird droppings containing the nematodes. But how do the nematodes get into the bird droppings? By manipulating the ants so that they get eaten by birds. They somehow make the ants rear section turn red -- it's normally black -- resembling a ripe fruit. They make the ant's skin transparent, and the hind section is full of nematode eggs that look red. Fruit-eating birds are fooled into eating the ants and then excrete the parasite in their droppings. The droppings are collected by ants and the cycle repeats. Seems like a lot of trouble. You would think that the ants would pass the nematodes in their own feces and reinfect each other that way, but apparently their digestive system doesn't work that way.

Both papers this week are examples of what Dawkins called the "extended phenotype." Normally we think of the phenotype as a physical, biochemical, or behavioral trait of an organism that is controlled by that organism's genes. But, Dawkins points out, if beaver genes control the behavior that controls the shape of a beaver dam, then the shape of the dam could be considered an extension of the beaver's phenotype. In this case, ant rear sections that look like fruit are the phenotype resulting from one or more nematode genes. It would be interesting to mutate the nematodes to see which genes are involved.
Above: infected ant, with real fruits for comparison. Below: normal and infected ants. (All photos by Stephen Yonoviak)


how a catterpillar manipulate an ants?

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