Tuesday, April 3, 2012

Infectious Selflessness: How an Ant Colony Becomes a Social Immune System


Ants work together to battle a deadly fungus by diluting the infection across the colony
ant-on-leafSOCIAL IMMUNITY An ant colony can act as one giant immune system when battling a pathogen, like an infectious fungus.Image: Luke Elstad, Wikimedia Commons
In the 2011 blockbuster thriller Contagion, a virus infects and kills 26 million people around the world. But even those who evade the virus are infected with something else:crippling fear. To contain the outbreak, the military imposes a quarantine. People stay indoors, refusing to interact with anyone outside their families. Touching anyone or anything becomes a risk, because the virus lingers everywhere.

Ants do things differently. When a deadly fungus infects an ant colony, the healthy insects do not necessarily ostracize their sick nest mates. Instead, they welcome the contagious with open arms—or, rather, open mouths—often licking their neighbors to remove the fungal spores before the pathogens sprout and grow. Apparently, such grooming dilutes the infection, spreading it thinly across the colony. Instead of leaving their infected peers to deal with the infection on their own and die, healthy ants share the burden, deliberately infecting everyone in the colony with a tiny dose of fungus that each individual's immune system can clear on its own. Such "social immunization" also primes the immune systems of healthy ants to battle the infection. These are the conclusions of a new study in the April 3 issue of PLoS Biology.

When you encounter a particular pathogen—a virus, a fungus—for the first time, your immune system has to learn how to deal with it. The second time you meet the same pathogen, your immune system is ready—it has developed some resistance. Researchers have found that when some members of an ant colony are exposed to a pathogen for the first time, all members of that colony—even the ones that were not initially infected—build resistance to the pathogen. How this happens was never clear.

To investigate the mystery, Sylvia Cremer of the Institute of Science and Technology in Austria and her colleagues studied Lasius neglectus, a rather common-looking ant that forms supercolonies, and Metarhizium anisopliae, a parasitic fungus that feeds on and kills many insects. Once the fungal spores settle on an insect's body, they germinate and penetrate the exoskeleton with rootlike structures called hyphae. Eventually the fungus sucks out all the nutrients from the insect and encrusts its emptied husk in what looks like green mold.

To interrupt the pathogen's life cycle, some ants lick fungal spores off of others. As the ants groom one another, bacteria on their skin—as well as specialized glands in the mouth called infrabuccal pockets—kill most of the spores that they lap up. Later, the ants spit out a compacted ball of dead spores. But Cremer and her colleagues suspected that not all of the spores are killed and that, by tending to infected peers, healthy ants end up with some spores on their bodies.

Cremer and her teammates tested these hunches by first tagging M. anisopliae spores with a protein that glows red under ultraviolet light and subsequently exposing 15 ants to the signature spores. Two days later the researchers dissected the ants under a microscope and detected the blushing spores on 17 of 45 ants that they had not directly exposed to the fungus. Cremer concluded that these ants must have picked up the spores by grooming their infected nest mates. The infection had rippled through the colony. When the researchers dissected the ants and placed their body parts in agar plates, fungi grew on 64 percent of the ants that had not been directly exposed to the spores—an even larger portion of the colony than the scientists had first detected with UV light.

"Even though 60 to 80 percent of nest mates contracted the disease, only about 2 percent of the ants died," Cremer explains. "Such low-level infections were actually beneficial because they saved the directly exposed ants and built up resistance in the healthy ants."

When Cremer analyzed the gene activity of ants that picked up spores from infected peers, she found that genes coding for antifungal proteins, as well as more general immune proteins, were more active than usual. Removing fungal spores from a peer seems to prime the immune system to battle any collateral infections. When Cremer prevented healthy ants from touching infected ants, the infection did not spread, the uninfected nestmates did not rev up their immune systems and many of the lone ants died. Cremer also observed that healthy ants are especially attentive to sick nest mates in the first two days after infection, which makes sense because if the spores are not removed within that period, it is usually too late to prevent full-blown infection and death.

Cremer and her colleagues think that the newly observed interactions between healthy and sick ants—as well as the genetic evidence of increased immune responses—explain how an entire ant colony develops resistance to a pathogen, even if only some of the ants are directly exposed to that pathogen. Although each insect has its own immune system, ants seem to have evolved a second immune system—a colony-wide immune response to infection. To thwart contagion, ants embrace it.

Rebeca Rosengaus of Northeastern University was impressed with the variety of experiments and analyses in the new study, which she says "provides further support that social immunity is a real phenomenon, not only in ants, but also in termites and probably eusocial wasps and bees, too." In earlier work Rosengaus discovered that termites exposed to a fungus warn one another by "essentially having a seizure"—hopping around like crazy and banging their heads against their nest walls to keep healthy peers away. She also found evidence that ants spread immunity to bacterial infections by transmitting immune proteins in droplets of food passed from one ant's mouth to another. "It goes against what you might think. Because there are so many individuals living so closely together, if one gets sick, chances are someone else would get sick, but through social immunization the entire colony seems to be doing better."
 

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