Spite in a Petri Dish

Spiteful bacteria. Two words you probably haven't heard together. Then again, you probably haven't heard of altruistic bacteria either, but both sorts of microbes are out there--and in many cases in you.

Bacteria lead marvelously complicated social lives. As a group of University of Edinburgh biologists reported today in Nature, a nasty bug called Pseudomonas aeruginosa, which causes lung infections, dedicates a lot of energy to helping its fellow P. aeruginosa. The microbes need iron, which is hard for them to find in a usable form in our bodies. To overcome the shortage, P. aeruginosa can release special molecules called siderophores that snatch up iron compounds and make them palatable to the microbe. It takes a lot of energy for the bacteria to make siderophores, and they aren't guaranteed a return for the investment. Once a siderophores harvests some iron, any P. aeruginosa that happens to be near it can gulp it down.

At first glance, this generosity shouldn't exist. Microbes that put a lot of energy into helping other microbes should become extinct--or, more exactly, the genes that produce generosity in them should become extinct. Biologists have discovered mutant P. aeruginosa that cheat--they don't produce siderophores but still suck up siderophores made by the do-gooders. It might seem as if the cheaters should wipe the do-gooders off the face of the Earth. The solution to this sort of puzzle--or at least one solution--is helping out family. Closely related microbes share the same genes. If a relative scoops up the iron and can reproduce, that's all the same for your genes.

To test this hypothesis, the Edinburgh team ran an experiment. They filled twelve beakers with bacteria they produced from a single clone. While the bacteria were all closely related, half were cheaters and half were do-gooders. They let the bacteria feed, multiply, and compete with one another. Then they mixed the beakers together, and randomly chose some bacteria to start a new colony in twelve new beakers. More successful bacteria gradually became more common as they started new rounds. In the end, the researhers found--as they predicted--that these close relatives evolved into cooperators. The do-gooders wound up making up nearly 100% of the population.

That didn't happen when the researchers put together two different clones in the same beakers. When the bacteria had less chance of helping relatives, the do-gooders wound up making up less than half of the population.

But the biologists suspected that even families could turn on themselves. Mathematical models suggest that the benefit of helping relatives drops if relatives are crammed together too closely. They never get a free lunch--siderophores produced by other, unrelated bacteria. Instead, all the benefits of consuming iron are offset by the cost of producing the siderophores. In the end, the benefit doesn't justify the cost.

The Edinburgh team came up with a clever way to test this prediction out. They ran the same colony experiment as before, but now they didn't take a random sample from the mixed beakers to start a new colony. Instead, they took a fixed number of bacteria from each beaker. This new procedure meant that there was no longer a benefit to being in a beaker where the bacteria were reproducing faster than the bacteria in other beakers. The only way to survive to the next round of the experiment was to outcompete the other bacteria in your own beaker--even if they were your own relatives. The researchers discovered that when closely related bacteria were forced to compete this way, utopia disappeared. Instead, the ratio of cheaters to do-gooders remained about where it started, around 50:50.

The evolutionary logic of altruism also has a dark side, known as spite, which the Edinburgh have explored in a paper in press at the Journal of Evolutionary Biology. (They've posted a pdf on their web site.) It's theoretically possible that you can help out your relatives (and even yourself) by doing harm to unrelated members of your same species, even if you have to pay a cost to do it. You might even die in the process, but if you could wreak enough havoc with your competitors, this sort of behavior could be favored by evolution. Biologists call this sort of behavior spite.

It turns out that many bacteria are spiteful in precisely this way. They produce antibiotics known as bacteriocins that are poisonous to their own species. These poisons take a lot of energy to make, and the bacteria often die as they release them. But these spiteful bacteria don't kill their own kin. Each strain of bacteria that makes a bacteriocin also makes an antidote to that particular kind of bacteriocin. Obviously, evolution won't favor a lineage of microbes that all blow themselves up. But it may encourage a certain balance of spite--a balance that will depend on the particular conditions in which the bacteria evolve.

Understanding the evolution of spiteful and altruistic bacteria will help scientists come up with new ways to fight diseases. (The altruism of P. aeruginosa can make life hell for people with cystic fibrosis, because the bacteria cooperate to rob a person of the iron in his or her lungs.) But bacteria can serve as a model for other organisms who can be altruistic or spiteful--like us. While some glib sociobiologists may see a link between a spiteful self-destructive microbe and a suicide bomber, the analogy is both disgusting and stupid. Yet the same evolutionary calculus keeps playing out in the behavior of bacteria and people alike.

(Update 6.27.04: Did I say siderophiles? I meant siderophores...)