By forcing bacteria to evolve in ever-changing conditions, scientists have induced a behavior in which colonies formed by microbes with identical genes take radically different forms, as if one sibling in a set of identical quadruplets could sprout gills.

Technically known as "stochastic switching between phenotypic states" — or, more conversationally, hedging your bets — the ability may have been critical to the success of primitive forms of life.

Bet hedging "may have been among the earliest evolutionary solutions to life in variable environments," even preceding the ability to turn genes on and off, wrote researchers in a study published Wednesday in Nature.

Scientists have known for decades about bet hedging, which is widespread in the natural world. One well-known example comes from disease-causing bacteria, which randomly produce different surface proteins, a few of which are bound to escape immune system detection. For all its ubiquity, however, bet-hedging behavior was at first considered counter-intuitive, even baffling. After all, in any given instance, it's better to have the right surface protein.

But it's not always possible to know what's right in advance, especially in highly variable environments. In the 1960s, evolutionary biologists made mathematical models suggesting that bet hedging made sense over the long run. Some researchers even speculated that it was a basic component in the toolbox of early life, allowing primitive microbes to adapt rapidly, without being able to sense their environments or adjust gene activity — a sophisticated ability that probably took hundreds of millions of years to emerge.

But for all this theorizing, the evolution of bet-hedging had until now never been directly observed.

"Almost every biologist knows about this and is fascinated by it," said study co-author Hubertus Beaumont, a Leiden University biologist. "We go one step further, and see this evolving in real time."

Beaumont started the experiment with a population of genetically identical Pseudomonas fluorescens, a common bacterium that divides every 45 minutes and has a relatively small genome, making it easy to study.

From that strain, they seeded 12 different bacterial lines, each growing in a tube of undisturbed, nutrient-rich broth. After three days, a sample was taken and spread on agar plates to see what type of colonies formed. The bacteria divided and spread across each plate. The researchers then took a single sample of the healthiest colony and transferred it to a tube of shaken broth. After another three days of growth, the P. fluorescens in that tube were again sampled, spread on agar, and the healthiest put back into unshaken broth.

From a human perspective, it was as if tribes that thrived in a forest were suddenly tossed in a desert, then thrown back as soon as they'd started to adjust. The switch was performed a total of 16 times, with the researchers sequencing the survivors' genomes at each step.

Earlier research by Paul Rainey, a Massey University evolutionary geneticist and co-author of the study, showed that different types of broth drove the evolution of different colony types. Shaken broth favored colonies that, in their aggregates of millions of microbes, had a smooth, rounded appearance. Unshaken conditions favored the evolution of wrinkled, fast-spreading colonies. As the rounds of selection continued, some P. fluorescens lines evolved back and forth between wrinkly and smooth types.

But in two of the lines, something special happened: In the very same tube, sharing the very same genetic inheritance, were cells that formed completely different types of colonies. Some were wrinkled, and others were smooth. It was as if those P. fluorescens strains had planned for an unpredictable future.

When the researchers looked at the genomic histories, they found that bet hedging required nine genetic mutations. The first eight were linked to traits that helped microbes survive in shaken and static tubes. The ninth, involving a gene important in metabolism, triggered the ability to produce multiple colony forms. The researchers ran the experiment multiple times, with similar results. An average of one line in twelve would evolve bet hedging, always as a result of the same accumulation of mutations.

This ability "could reasonably—one might think—take tens of thousands of generations to evolve," wrote the researchers. Instead, it took a few months. That it emerged so rapidly hints at the role it may have played for microbes that hadn't yet evolved ability to to sense changes in temperature or nutrient availability, much less respond to them.

"For them, the world was completely unpredictable," said Beaumont. "I suspect that if you go back in time, you'd find organisms with one genotype that could express a wide range of strategies."

Richard Lenski, a Michigan State University evolutionary biologist known for his decades-long studies of evolutionary dynamics in E. coli colonies, said that it's difficult to know exactly what happened early in life's history. "But their results do show that such adaptations evolve pretty easily, so it's certainly possible," said Lenski, who was not involved in the study.

As for what caused colonies to take radically different forms from their genetically identical neighbors, or why that ninth mutation in particular was so critical, Beaumont doesn't yet know. Although we know the mutations, the details of the mechanisms underlying evolution, even in simple bacteria, are often "still hidden in a black box," he said.

"We want to know what's going on in that box," said Beaumont. "We're going beyond theory. We're doing experiments with evolution itself."

Image: Hubertus Beaumont

See Also:

Citation: "Experimental evolution of bet hedging." Hubertus J. E. Beaumont, Jenna Gallie, Christian Kost, Gayle C. Ferguson & Paul B. Rainey. Nature, Vol. 461 No. 7269, November 4, 2009.

Brandon Keim's Twitter stream and reportorial outtakes; Wired Science on Twitter. Brandon is currently working on a book about ecosystem and planetary tipping points.