An unhealthy glow: Parasites may equip hosts with warning colors

ResearchBlogging.orgEarlier this month at ScienceOnline2011 (a professional meeting of science bloggers and others using the web to communicate about science), Brian Malow – aka. the Science Comedian – gave a wonderful impromptu performance. On the topic of viruses, Brian described a viral infection as “Your cells: Under new management.” It’s a clever but quite apt description – viruses co-opt the genetic machinery of host cells, forcing those cells to produce the DNA, RNA, and proteins required to make more viruses.

But viruses just manipulate single cells. Some parasites play puppet-master with their entire multicellular host, bending its behavior to suit their needs. Consider the parasitoid wasp Hymenoepimecis argyraphaga. Many wasp species lay their eggs on spiders, the wasp larva slowly consuming (and ultimately killing) its host as it develops – gruesome, yes, but not particularly inventive. This is exactly how a larval H. argyraphaga begins its life, feeding on the hemolymph (essentially, the “blood”) of its host spider. And for a couple of weeks, the spider continues to go about its business quite normally.

But then something changes, and the spider begins to spin a web unlike anything it has ever built before; this custom-built structure will support the parasitic wasp as it pupates and transforms into an adult. Once the web is complete, the wasp has no further use for its host, and it kills and consumes the spider before beginning its metamorphosis. The exact biochemical mechanism enabling this manipulation still isn’t known, but somehow the wasp manages to override the spider’s natural behavior patterns, compelling it to build a safe resting place for its own future killer.

Heterorhabditis nematodes emerge en masse from a dead waxworm. Photo by Peggy Greb, USDA.

In a paper published in Animal Behavior this month, researchers investigate another fascinating parasite, one that might enhance its own survival and transmissions by altering its host’s color.

Nematodes in the genus Heterorhabditis are tiny worms that parasitize insect larvae. The young worms live in the soil, and when they find a potential host they invade its body through the mouth, anus, or spiracles (the holes through which insects breathe). But the worms don’t just eat the host – thing get much more bizarre than that. Within the worms live symbiotic bacteria (Photorhabdus luminescens). Once the worms enter their insect host, they release these bacteria, which quickly begin to dissolve the host’s tissues. The worms slurp up the resulting goo, grow, and reproduce. The flesh of a single host insect may support the worms for several generations, long after the host is dead. After a couple of weeks, the host insect splits open, releasing enormous numbers of worm larvae back into the soil and beginning the cycle anew.

In addition to killing their hosts in a sublimely cruel way, the parasites induce a striking change in their dead host’s appearance. A few days after the infection begins, the host actually begins to glow, and it remains an intense pink or red color even after the glow subsides.

A dramatic color change occurs in host insects following infection. (a) Before infection, all waxworm larvae have similar reflectance. (b) Seven days after infection, infected waxworms (plotted in red) have high reflectance in wavelengths 600-700nm – i.e., they are red!

Why would the parasites do such a thing? Well, luciferase, an enzyme involved in the bacterial bioluminescence, may also help eliminate “reactive oxygen species” (ROS) – oxygen-containing compounds that might otherwise build up in the insect carcass as it is digested, causing damage to the bacteria or worms. This idea remains to be tested, but seems promising.

A live (left) and infected dead waxworm (center). Note the substantial difference in color. Photo by Peggy Greb, USDA.

Biologist Andy Fenton and colleagues set out to test a different hypothesis about this parasite-induced color change. If a bird eats an infected insect, plump with a nematode-bacteria broth, it’s “game over” for the parasites within. They can’t survive a trip through a bird’s digestive tract. Perhaps the bright pink color of the infected host is analogous to the conspicuous warning coloration of many toxic animal species – a message to potential predators: “Don’t eat me, I’m unpalatable.”

If this were true, then birds should avoid infected larvae. And if they do, the infected larvae must be distasteful, or else this avoidance behavior would not persist.

The authors presented infected and uninfected waxworms to wild European Robins (Erithacus rubecula) to test whether the birds avoided infected prey. Each robin was given an array of 20 waxworms (10 infected, 10 uninfected) and allowed to choose prey freely for 30 minutes. Then, the authors noted which waxworms were consumed, and analyzed the fraction that belonged to the infected group. The robins avoided infected waxworms, even when the alternative was an uninfected waxworm that had been dead equally long. Moreover, this avoidance seemed to become more pronounced as the infection progressed.

Robins consume more uninfected waxworms (gray bars) than infected waxworms (white bars), and this effect increases as the infection progresses.

The authors also claim that robins were less likely to consume another infected waxworm after they had encountered their first infected prey item. If true, this would be evidence in favor of the infected insects’ noxiousness. This claim is based on the behavior of only six robins, however, and the authors are vague about the statistical methods that led them to this conclusion; I think it is wise to take this result with a grain of salt.

The authors present convincing evidence that wild predators avoid insects infected with the Heterorhabditis nematode. This may represent a new form of host manipulation by parasites – a parasite-induced color change to reduce the risk of predation. If the authors can demonstrate more convincingly that the infected prey are actually distasteful, their hypothesis will be even more convincing. At the very least, there is some fascinating natural history at work in these parasitic worms, and this study provides some cautious support of a novel mechanism of host manipulation.

Note: I am a photographer as well as a biologist, and I have to conclude by saying that I was flabbergasted that the authors did not include one photograph in their paper! With such a visually compelling study system, I consider this a huge wasted opportunity to make the study accessible to an audience much broader than other behavioral biologists. Lucky for me, the USDA had some nice images I could use to illustrate this post.

References:

Fenton, A., Magoolagan, L., Kennedy, Z., & Spencer, K. (2011). Parasite-induced warning coloration: a novel form of host manipulation Animal Behaviour, 81 (2), 417-422 DOI: 10.1016/j.anbehav.2010.11.010

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