History restricts and guides the evolution of innovations
The role of history in evolution is a hotly debated topic. The late Stephen Jay Gould was a firm believer in its importance and held the view that innocuous historical events can have massive repercussions, often making the difference between survival and extinction. To him, every genetic change is an “accident of history” that makes some subsequent changes more likely and others less so. Evolution, as a result, is “fundamentally quirky and unpredictable”. In his book Wonderful Life, Gould imagined that if we replayed life’s tape from some point in the past, evolution would go down very different paths than the ones it has currently taken.
Another eminent palaeontologist, Simon Conway Morris, disagreed. He argued that life can weave its way down any number of evolutionary routes, but that its “destinations are limited”. He saw the fact that living things often converge on the same adaptations as evidence that history has very little pull on evolution. In his mind, replaying life’s tape would lead to more or less the same result, with historical contingency only altering minor details.
Of course, it’s impossible to replay life’s tape on a planetary scale but some experiments allow us the chance to do so at a more modest level. The aptly named “long-term evolution experiment” (or LTEE) is one of these. It’s the longest-running experiment in evolution ever undertaken and began in 1988, when Richard Lenski at Michigan State University bred 12 lines of the gut bacteria Escherichia coli from a single ancestor. Since then, the bacteria have been grown in twelve separate vials of sugary broth and plopped into fresh solution every day.
Every 500 generations, samples are frozen to act as a ‘fossil record’, and since the experiment’s humble beginnings, over 44,000 generations have passed. In this time, the bacteria have changed greatly. All of them are now bigger, grow faster on sugar, and take less time to establish new colonies. But recently, Lenski noticed that one lineage of bacteria have developed an extremely rare adaptation that in the entire history of the experiment has turned up only once. Why?
One in ten trillion
The bacteria are grown in broth that is low in sugar, and they usually run out by the afternoon.The broth is also rich in citrate ions but in general, E.coli cannot use these as fuel when oxygen is around. Any bacterium that evolves this ability would suddenly find itself amid a vast and exclusive energy source. But in 20 years of evolution, only one population of E.coli has managed to do this, even though all 12 strains have evolved under exactly the same conditions and all 12 have been exposed to citrate from the beginning.
Blount first discovered the citrate adaptation, when he noticed that one vial of bacteria (known as Ara-3) was much cloudier than usual, a sign that the cells that been growing on a fuel other than sugar. Unlike almost all other E.coli, some of the cells from Ara-3 were able to grow solely on citrate. To prove that these unique cells didn’t come from a contaminating strain, Blount showed that their DNA carried certain giveaway mutations that characterised earlier generations of Ara-3.
During the experiment, each population of bacteria experienced billions of mutations, and given the size of E.coli‘s genome, it’s likely that each lineage tried every typical genetic change several times. And yet, the citrate adaptation turned up only once in all of this tinkering. Based on the experiment, the odds of a bacterium developing the adaptation in any generation is just one in ten trillion! There are two possible explanations for this: it’s the result of an extremely rare mutation; or it depended on the particular history of that specific population.
Replaying the tape
To work out which, Zachary Blount from Lenski’s lab used the frozen fossil record to replay evolution from different points from this population’s past. In three separate replays, Blount cultured bacteria from the entire length of the experiment, from the original ancestor to the most recent generation. In all cases, he found that citrate users evolved much more often in samples from later generations than those from earlier ones.
These results strongly suggest that the citrate innovation was not simply the consequence of an extremely rare mutation. If that was the case, it would be equally likely to crop up at any point throughout the experiment’s history. To Blount, the fact that it happened more frequently in later generations suggests that it depended on one or more mutations that the bacteria had previously picked up, which unlocked the potential for the later innovation.
It’s possible that the ability to use citrate depends on teamwork between several genes. Any one of these could pick up the right mutation, but it would be meaningless if earlier mutations hadn’t provided the right partners. Alternatively, earlier mutations could have been directly responsible for later ones. Blount speculates that the clinching mutation might have happened in a piece of mobile DNA that had previously jumped into the right spot. Without this insertion, the critical change would never have happened. Blount and Lenski are now trying to discover this sequence of genetic events, and how they affected the bacterial cells.
One change to rule them all…
Whatever the route, one lineage of bacteria had managed to make use of citrate after about 31,000 generations. Their numbers grew quickly and by 32,500 generations, they made up 20% of the population. But 500 generations later, they had fallen back down to just 1%.
Blount believes that the first bacteria to use citrate just weren’t very good at it and reaped only marginal benefits from their innovation. As a result, they initially prospered but were soon outcompeted by other bacteria that couldn’t use citrate but had become much better at metabolising sugar. Only later did they regain their initial foothold, with further mutations that improved their unique ability and allowed them to switch seamlessly from sugar to citrate when the first fuel ran out. Eventually, these advances catapulted the citrate users to dominance. Their sugar-only peers still eke out a minority existence because they are still better at using sugar as an energy source.
So a single innovation – citrate exploitation – was enough to split a united population of bacteria into a community of two members: a specialist that focuses on sugar; and a generalist that uses both sugar and citrate.
In the team’s own words, the study clearly shows that “historical contingency can have a profound and lasting impact under the simplest conditions, in which initially identical populations evolve in identical environments. Even from so simple a beginning, small happenstances of history may lead populations along different evolutionary paths. A potentiated cell took the one less travelled by, and that has made all the difference.”
Reference: PNAS doi:10.1073/pnas.0803151105
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