Microcosm (12 page)

Short of time travel, Gould thought the best way a scientist could answer that question was by examining the fossil record, documenting the emergence and extinction of species. But experiments on
E. coli
can also address the question, at least on a scale of years. What makes experiments such as Lenski’s particularly powerful is that evolution unfolds many times over, not just once. From an identical ancestor, Lenski produced twelve lines, each of which went through its own natural selection. Lenski and his colleagues may not be able to rewind the tape of
E. coli’
s evolution, but they can create twelve identical copies of the same tape and watch what happens when they all play at the same time.

It turns out that the tapes are not identical, nor are they entirely different. In Lenski’s experiments all twelve lines grew faster than their ancestors, but some lines grew far faster than others. They all grew larger, but some became round while others remained rod-shaped. When scientists have taken a close look at the genomes of evolved bacteria, they have found many differences in their DNA. One reason evolution can take different paths is that mutations are not simple. A mutation may be beneficial in one microbe but downright harmful in another. That’s because a mutated gene’s effects depend in part on how it cooperates with other genes. In some cases the genes may work together well, but in other cases they may clash.

Despite those differences, natural selection can override many of the quirky details of history. While Lenski’s lines may not be identical, they have tended to evolve in the same direction. They have also converged on a molecular level. Lenski and his colleagues have found several cases in which the same gene has mutated in all their lines. Even genes that have not evolved a new sequence have changed in a similar way. Some genes now make more proteins, and some make fewer. Lenski and his colleagues took a close look at how the expression of genes changed in two lines of
E. coli.
They found fifty-nine genes, and in all fifty-nine cases, the genes had changed in the same direction in both lines. The evolutionary song remains the same.

THE TANGLED BANK

“It is interesting to contemplate a tangled bank,” Darwin wrote in
The Origin of Species,
“clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent upon each other in so complex a manner, have all been produced by laws acting around us.”

Darwin did not believe that he could see the production of life’s tangled bank as it happened. Life evolves into new species over vast stretches of time, he argued, changing as slowly as mountains rise and islands sink. He could only look at the results of evolution around him, such as the distribution of related species around the world, to reconstruct the tangled bank’s history. Today most scientists who study the diversity of plants and animals still follow Darwin’s lead. The evidence they’ve amassed indicates that new species generally take thousands of years or more to branch off from other species. For the most part, it’s a waste of time to sit around hoping to watch a new species emerge.

It turns out, however, that some of the same forces that drive the origin of species can be observed in a dish of
E. coli.
In the early 1990s, Julian Adams, a microbiologist at the University of Michigan, used a single microbe to found an
E. coli
population. Adams and his colleagues supplied the bacteria with a little glucose. Unlike Lenski, Adams replenished their sugar so that they never faced outright starvation. The bacteria began to evolve, adapting to the new conditions. But to Adams’s surprise, natural selection did not favor a single strategy. When he put the bacteria on petri dishes, they grew in two types of colonies: some formed big splotches, and others formed small ones.

Adams thought he might have contaminated his original colony with another strain, so he shut down the experiment and started over again. After the new colony had adapted to the low-glucose diet, Adams spread the microbes on plates again. And again he discovered the same big-and small-splotch makers. Adams ran the experiment a few more times, and he found that it took about 200 generations for the two types of microbes to emerge. He realized that a single clone was evolving time and again into two distinct types of
E. coli.

Those two types turned out to be ecological partners. The large colonies are inhabited by microbes that do a better job than their ancestors at feeding on glucose. One of the waste products they give off is acetate.
E. coli
can survive on acetate, although it grows more slowly on it than on glucose. Adams discovered that some of his
E. coli
were becoming more efficient at feeding on acetate than their ancestors were. The acetate feeders grow slowly, but they aren’t driven to extinction because they are taking advantage of a food that the faster-growing bacteria aren’t eating. A food chain had emerged spontaneously in Adams’s lab as organisms began to depend on one another for survival.

Other scientists have confirmed Adams’s findings with experiments of their own. And they’ve created new kinds of ecological diversity from a single
E. coli
ancestor. Instead of a glucose-only diet, Michael Doebeli and his colleagues at the University of British Columbia supplied
E. coli
with both glucose and acetate. After a thousand generations, Doebeli found that the bacteria had evolved into big and small colonies. But they were different from the big and small colonies that Adams had produced. Both colonies in Doebeli’s experiment fed on glucose and acetate. The difference between them was a matter of timing. The big colonies fed on glucose until it ran out, and then they turned to acetate. The small colonies switched over sooner, so that they had a head start.

Doebeli and his colleagues then looked closely at how the genes in each colony had evolved. Typically, when
E. coli
is feeding on glucose, it keeps the genes for digesting acetate tightly repressed. If it made both sets of enzymes at the same time, they would get snared in a metabolic traffic jam. When the time comes to switch sugars, the bacteria must first destroy the enzymes for glucose and then build enzymes that can break down acetate. Doebeli found that in the small colonies, natural selection had favored mutants that stopped repressing their acetate genes. When glucose and acetate were available, these mutants fed on both kinds of sugar but did a lousy job of it compared with the glucose specialists in the large colonies. They got a reward for this sacrifice, however: they could leap quickly to take advantage of acetate while the big colony slowly retooled itself.

These experiments on
E. coli
may shed light on how new species form. Nature has formed its own petri dishes in Nicaragua, where dead volcanoes have filled with rainwater. These crater lakes are completely isolated from neighboring lakes and rivers, but on rare occasion a hurricane can sweep fish into them. In Lake Apoyo, which formed about 23,000 years ago, two species of cichlids live together. One of the fish, known as the Midas cichlid, is a big creature that roots around in the muck and crushes snails. The other fish, the arrow cichlid, is a thin, quick-darting creature that hunts for insect larvae in the open water. Their DNA indicates that the Midas cichlid was swept into the lake after it formed and that the arrow cichlid evolved from it. The split may have taken only a few thousand years.

Whether scientists study cichlids or
E. coli
or any other organism, they face the same question: Why specialize? Why don’t organisms evolve to become jacks-of-all-trades instead? There may simply be limits to how well one organism can do many things. Sooner or later they encounter a trade-off. A mutation that helps
E. coli
feed on acetate may interfere with its ability to feed on glucose. By trying to do everything, generalists may lose out to specialists, which do one thing far better than anything else. Cichlids may face similar trade-offs. A hybrid cichlid may not be particularly well adapted to eating snails or hunting for larvae, and it will have less reproductive success than the fish at the two ends of the spectrum. As more species emerge in an ecosystem, they create more opportunities for specialists to find a new way to make a living. And so over time, Darwin’s bank tangles itself.

Six

DEATH AND KINDNESS

THE ANARCHIST PRINCE

         
CHARLES DARWIN WAS BURIED DURING
a grand funeral in Westminster Abbey in 1882. Biologists were soon fighting over his legacy. In 1888, the British zoologist Thomas Huxley published a shocking essay, “Struggle for Existence and Its Bearing upon Man.” In it he summoned up an ugly picture of nature as a combat of all against all. “The animal world is on about the same level as the gladiator’s show,” he wrote. “The creatures are fairly well-treated, and set to fight—whereby the strongest, the swiftest, and the cunningest live to fight another day. The spectator has no need to turn his thumbs down, as no quarter is given.” In order to be moral, Huxley believed, humans had to work against nature.

Huxley’s essay drew a stinging attack from an anarchist prince. Pyotr Alekseyevich Kropotkin was born in 1842 to a wealthy Russian nobleman. In his teenage years he served as a page to Tsar Alexander II, but he became disillusioned with the court and went to Siberia to serve in the army. There he worked as the secretary of a prison-reform committee, and the horrors he witnessed in the labor camps turned him into a radical anarchist. At the same time, he was developing into a first-rate scientist. Kropotkin joined a geographic survey in 1864 and spent the next eight years studying the Siberian landscape.

On his return from Siberia, Kropotkin soon ended up in jail for his politics. He escaped and fled to Europe, where he wrote pamphlets that earned him fame and more time in jail. Huxley’s essay appeared just as Kropotkin had emerged from a three-year stint in a French prison. He settled in England, where he immediately set about writing a series of essays attacking what he saw as Huxley’s distortion of both man and nature. His essays were eventually published as the best-selling book
Mutual Aid.

Human morality is not artificial, Kropotkin argued, but in fact profoundly natural. “Sociability is as much a law of nature as mutual struggle,” he wrote. Cooperation has evolved thanks to the advantages it offers over selfish behavior. Animals do not abandon one another but instead show care and concern. He recounted example after example of kindness in the animal kingdom, from horses that helped one another escape a grassland fire to horseshoe crabs righting overturned friends.

One can only wonder what Kropotkin would have thought of
E. coli.
Perhaps he would have been pleased to watch billions of microbes working together to build biofilms, to follow their swarming flocks traveling with intertwined flagella. He might have been startled by the selfless sacrifice of bacteria exploding with colicins that kill other strains. Or perhaps he would not have been startled at all.
E. coli’
s spirit of cooperation came as something of a surprise to scientists at the end of the twentieth century, but Kropotkin had written prophetic words a hundred years earlier: “Mutual aid is met with even amidst the lowest animals,” he wrote, “and we must be prepared to learn some day, from the students of microscopic pond-life, facts of unconscious mutual support, even from the life of micro-organisms.”

Kropotkin belonged to the same scientific era as Darwin. He was an observant nineteenth-century naturalist with no understanding of DNA and its mutations. It was not until the mid-1900s that scientists recognized how mutations arise in individuals and help them outcompete other members of their species. But when this view of evolution first emerged, many biologists recoiled from it much as Kropotkin had recoiled from Huxley’s gladiatorial spectacle.

Kropotkin’s intellectual grandchildren asked how competition among individuals could give rise to behavior that benefits entire groups. Fish join together into giant schools that move like a single organism. Sterile ants tend the offspring of their queen. A meerkat will stand guard so that its companions can nose around for food. If a meerkat acquired a mutation that made it stand high to keep watch over its companions, it would become easier prey. Even if natural selection could produce these selfless behaviors, biologists wondered, how could it prevent individuals from exploiting the altruism of others?

For
E. coli
the evolution of cheating is no mere thought experiment. When a colony runs out of food, the bacteria engage in a complicated cooperative dance as they enter a stationary phase. The microbes send signals to one another to synchronize their actions as they collapse their DNA and halt their production of proteins. By entering the stationary phase together, the bacteria improve the chances that at least some of them will survive until conditions improve, even though many of them may die along the way. Yet Roberto Kolter of Harvard and a former student, Marin Vulíc, discovered that some bacteria do not dance to the same dying tune.

Vulíc and Kolter discovered that mutants arose in their
E. coli
colony that could rouse themselves from the limbo of the stationary phase and start to feed. They fed not on sugar but on the amino acids excreted by their dormant companions. As some of the stationary bacteria died, they burst open. The mutants then fed on their proteins and DNA. The diet of the mutants was meager, but it was enough to allow them to reproduce. Over the course of several weeks the cheaters’ descendants came to dominate the entire population.

This betrayal was not a rare fluke. Time and again when Vulíc and Kolter starved
E. coli,
cheaters evolved and thrived. They did so according to the fundamental rules of modern evolutionary biology: through random mutations and the competition among individuals for reproductive success. One has to wonder: If it is so easy for cheaters to triumph, how can cooperation survive at all?

STRENGTH IN NUMBERS

In the 1950s, some scientists explained cooperation in animals with an idea that came to be known as group selection. They argued that a large group of unrelated animals could outcompete another group, just as individuals outcompete other individuals. The adaptations that allow some groups to outreproduce other groups should become more common over time. Group selection could produce traits and behaviors that benefit the many, not the few. In some bird colonies, for example, only a third of the adults might reproduce in a year. Group selectionists argued that the birds are restraining themselves so that the colony will not get too big and destroy its food supply. They even saw death as resulting from group selection, clearing away old individuals so that young ones can get enough food to reproduce.

Group selection was popular for a time. People began to speak of behavior that was for the good of the species. But by the 1960s, critics were beginning to demolish the theory. They pointed out that group selection can produce benefits only slowly—far more slowly than the changes created by natural selection acting on individuals, as with the rise of cheaters. George Williams, an evolutionary biologist at the State University of New York, Stony Brook, distilled many of these arguments into a devastating assault. In his 1966 book,
Adaptation and Natural Selection,
Williams argued that the group-selection arguments were often the result of lazy thinking. If scientists couldn’t see how natural selection produced an adaptation, it was likely they had simply failed to think seriously enough about the question.

Williams declared that most aspects of biology, no matter how puzzling, were the result of strict natural selection working on individuals. Take the school of fish swimming like a superorganism. It might seem as if every individual cooperates for the good of the group, working with others to avoid predators, even if that means an individual gets devoured in the process. Williams argued that the schooling behavior could emerge as each fish tries to boost its personal chances of survival, either by trying to get in the middle of the school or by watching other fish for signs of approaching predators.

Meanwhile, in England, another young biologist, William Hamilton, realized that something important had been ignored in the debate over natural selection and group selection: family. Natural selection favors mutations that spread genes through a population, and one way to spread those genes is by having a lot of healthy children. Hamilton demonstrated, however, that an individual can spread its genes by helping its relatives breed.

Hamilton made his point mainly with social insects, such as ants and bees. A sterile female worker ant may have no hope of reproducing, but that does not mean the genes she carries have no chance of getting into the next generation. Every female worker in an anthill is the offspring of the queen, as are the eggs she helps to raise. That means the worker is helping to rear ants that share some of the same genes she carries. In fact, thanks to a quirk in insect genetics, a worker ant shares more genes with the eggs of the queen than she would with her own offspring. Hamilton put together a mathematical model of genes passing from one generation to the next. If altruism is more likely to pass a set of genes to the next generation than is reproducing oneself, it could be favored by natural selection. Group selection is indeed possible, Hamilton argued, if the group is an extended family.

Williams and Hamilton had a staggering impact on biology. It’s as if they had passed out decoder rings that allowed scientists to decipher many mysterious patterns in nature—why some animals dote on their offspring while others abandon them at birth, for example. They could make predictions about the intimate details of species with mathematical precision. As zoologists, Williams and Hamilton didn’t have much to say about the evolution of a microbe such as
E. coli.
But it turns out that in many ways
E. coli
supports their view of life as well.

There may be nothing terribly mysterious, for example, about why cheating
E. coli
haven’t completely taken over. Cheaters can exploit their fellow bacteria in the stationary phase, but only at a cost. The mutation that turns ordinary
E. coli
into cheaters occurs on a gene called rpoS. Normally rpoS acts as a master control gene, responding to signs of stress by turning on hundreds of other genes. Starvation and other kinds of stress cause rpoS to put
E. coli
into the stationary phase. If a mutation disables rpoS, the microbe will not shut down its metabolism but instead will begin to feed and grow.

Like many other genes, rpoS has many roles to play in
E. coli’
s life. When the microbe enters our stomachs and senses that it has entered an acid bath, rpoS responds by switching on acid-resistance genes. Cheaters cannot marshal these defenses, and so they are more likely to die before they can pass through the stomach. Although cheaters may thrive in one state, they lose out over
E. coli’
s entire life cycle.

Even
E. coli’
s biofilms, those lovely cooperative ventures built on self-sacrifice, may not be quite the models of altruism they seem to be. Joao Xavier and Kevin Foster, two biologists at Harvard, have found evidence that conflict can help produce biofilms. Xavier and Foster built a complex mathematical model of a biofilm to compare how well two kinds of bacteria would fare: one kind produced a biofilm glue (technically known as extracellular polymeric substances), and the other did not. Xavier and Foster seeded an empty surface with both kinds of bacteria and let them grow by eating glucose and consuming oxygen.

At first, Xavier and Foster found, the glue-making bacteria lost out to the others because they were diverting energy from their growth. But soon the balance tipped. As the bacteria multiplied, they used up the oxygen around them and could not grow as quickly. The glue makers could escape suffocation because they created a rising mound on which their offspring could grow. They could reach higher concentrations of oxygen, which allowed them to grow faster, which in turn allowed them to build their mounds of glue even higher. As a mound grew, it suffocated the older bacteria underneath while their descendants—and thus their genes—lived on. Meanwhile, the bacteria that did not make glue, trapped in the biofilm with no way to escape, were buried by their competitors. In some ways a biofilm may be less like a city and more like a forest, in which trees become wooden towers in order to reach the sunlight and avoid the shade of their rivals.

Conflict and cooperation strike an uneasy balance whenever many cells come together, whether they are
E. coli
or the cells of our own bodies. We descend from single-celled ancestors that probably looked a lot like amoebas. At some point our ancestors began to form colonies, which gradually evolved into vast collectives, otherwise known as animals. They communicated with one another as they had before, but now their signals caused them to differentiate into different types of cells, forming tissues and organs. Each time a new animal took shape, most of the cells of its body had to make the ultimate evolutionary sacrifice. They would become part of the body, and in that body they would die. Only sperm and eggs had the slightest chance of their genes surviving.

This is not a simple way to exist. In order to form a full-grown body, most cells must divide many times and then stop. Some kinds of cells must not lose the ability to regenerate themselves, but they must multiply only as much as necessary to heal a wound or build a new intestinal lining. Unfortunately, a dividing cell can mutate, just like a dividing
E. coli.
In some cases, the mutations will turn the cell into a rebel. It will reproduce rapidly, ignoring the signals that tell it to stop. It will produce a mass of insurgent cells, and within that mass new mutations will arise, producing even more rebellious cells. They will develop new tricks for evading the body’s defenses and for manipulating the body so that it brings them new blood vessels in order to supply them with extra oxygen and nutrients. They become cheaters, just like the cheaters that exploit
E. coli’
s cooperation. We call their success cancer.