Spiteful Suicide

Persister cells make a sacrifice for their companions, giving up the chance to multiply quickly. But when E. coli produce colicins, the chemical weapons for killing rival strains, they pay a far bigger price. In order to let their kin thrive, they explode in a suicidal blast.

The chemical warfare practiced by E. coli is the dark side of altruism. William Hamilton originally argued that natural selection could favor sacrifice if it meant an individual could help its relatives reproduce more. In 1970, he recognized that natural selection could also favor sacrifice if it meant that nonrelatives suffered—a nasty sort of altruism he called spite. Hamilton always argued that spite was rare and inconsequential, because his equations suggested it would be favored only when populations were very small. But in 2004, Andy Gardner and Stuart West at the University of Edinburgh demonstrated that if unrelated individuals compete fiercely with their immediate neighbors spite can also evolve.

E. coli meets these spiteful standards. It competes in the crowded confines of the intestines for a limited supply of sugar. An individual microbe sacrifices its own reproductive future by committing suicide, but its colicins destroy many competitors, allowing the microbe's own close relatives to thrive. As with persistence, becoming a colicin maker is a matter of chance. The noisy production of proteins determines which few individuals will respond to starvation by switching on their colicin-producing genes. The burden is shared by all.

Spite, some experiments now suggest, may also drive E. coli to become more diverse. Margaret Riley, a biologist at the University of Massachusetts, Amherst, and her colleagues have observed the evolution of this arms race in experiments on E. coli in both petri dishes and the guts of lab mice. Once in a rare while, an antidote gene may mutate into a more powerful form. Instead of just defending E. coli against its own colicin, it can also defend against the colicins made by other strains. This mutation gives a microbe an evolutionary edge, because it can survive enemy attacks that kill other members of its strain.

This powerful antidote opens the way for another advance. A second mutation strikes the colicin-producing gene, causing it to make a new colicin. Its relatives, which still carry an antidote for the old colicin, are killed off by the mutant toxin. But thanks to its powerful antidote, the microbe that makes the new colicin can survive while its relatives die. Its spite becomes intimate.

The emergence of new colicins drives the evolution of new antidotes in other strains. Likewise, new antidotes drive the evolution of new colicins. But E. coli has to pay a price for this weaponry. It has to use energy to make colicins and antidotes, which are particularly big as bacterial molecules go. A new colicin may be even deadlier than its predecessor, but it may also become a drain on a microbe. If a mutation leaves a microbe unable to make colicins—but still able to resist them—it may be able to channel the extra energy into reproducing. A colicin-free strain will spread, outcompeting the colicin makers.

If colicin makers are driven to extinction, their colicins no longer pose a threat to neighboring bacteria. Now antidotes become a waste of effort, since there is nothing for them to protect E. coli against. Natural selection can begin to favor pacifists—microbes that make neither colicins nor antidotes. Once the pacifists come to dominate the population, colicin producers can invade the population once more, killing off the vulnerable strains and getting the food for themselves. And so the journey comes full circle.

These sorts of cycles emerge spontaneously from evolution. You can think of them as games in which players use different kinds of strategies to compete with other players. In the case of E. coli, a strategy might be to make a particular colicin or to do without colicins and antidotes altogether. In the case of a male elephant seal, strategies might include fighting with other males for the opportunity to mate with females or sneaking off with a female without the big male on the beach noticing. In some cases, one strategy may prove superior to all the others. In other cases, two strategies may coexist. Fighting males and sneaker males can coexist in many species, for example. In still other cases, the success of strategies goes up and down over time.

Scientists sometimes call this cycling evolution a rock-scissors-paper game. In the game, each player can make a fist for a rock, extend two fingers for scissors, or hold the hand flat for paper. A player wins or loses depending on what the other players do. Rock beats scissors, but scissors beats paper, and paper beats rock. If a population of organisms is dominated by one strategy—call it paper—then natural selection will favor scissors. But once scissors takes over, rock is favored, then paper, and so on.

The common side-blotched lizard of coastal California plays a colorful version of rock-scissors-paper. The male lizards have colored throats, which may be orange, yellow, or blue. The orange-throated lizards are big fighters; they establish large territories with several females. The blue-throated lizards are medium sized; they defend small territories, holding just a few females, which they can guard carefully. The yellow-throated males are small and sneak around for mates, taking advantage of the fact that they look like females. Each type of male can outcompete one type but not the other. The yellow-throated males can sneak past the orange-throated males because the territories of the orange-throated males are so big. The yellow-throated males cannot use the same strategy against the blue-throated males because the blue-throated males stay close to their females and are bigger than the yellow-throated males. But the blue-throated males lose against the orange-throated males because the orange-throated males are bigger.

Over a period of six years, each type of male goes through a population cycle. When the orange-throated males become common, natural selection favors yellow-throated males, which can sneak off with their females. But once yellow-throated males become common, the biggest benefits go to blue-throated males, which can fight off the yellow-throated males and father lots of baby lizards with their few females. And in time, natural selection favors the orange-throated males again.

When scientists at Stanford and Yale discovered the E. coli version of the rock-scissors-paper game in 2003, they suggested that it may turn out to be particularly common. Chemical warfare is a frequent strategy in nature, particularly among organisms that are too small or too immobile to use other sorts of weapons. Trees poison their insect visitors, corals ward off grazers, and humans and other animals produce antibodies to fight off pathogens. The race to develop better poisons and defenses, as well as the added dimension of the rock-scissors-paper game, can foster the evolution of diversity. Scientists have long known that a single strain of E. coli may dominate the gut for a few months, only to later shrink away, making way for a rarer strain. The colicin war may be one force behind this cycle.

E. coli may be able to spontaneously evolve a harmonious food web. But when it comes to weaving Darwin's tangled bank, war may be just as good as peace.

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