Replaying evolution reveals the benefits of being slow and steady

By Ed Yong | March 17, 2011 2:00 pm

Video game players are used to replaying history. They can load up any saved game and start afresh, sometimes making different choices that lead to alternative endings. Life, sadly, is no game and it’s far more difficult to reload and start again… difficult, but not impossible. In a laboratory in Michigan State University, Richard Lenski repeatedly replays evolution from saved files.

Lenski’s aptly named “long-term evolution experiment” is the longest-running in history, and one of the most important. It looks deceptively simple – just twelve gently shaking flasks of sugary solution, each containing a strain of the gut bacterium Escherichia coli. Lenski bred the dozen strains from a common ancestor in 1998. Every day since then, his team has transferred one per cent of the cells into a fresh flask to grow anew. Last month, the bacteria passed their 50,000th generation.

Every 500 generations, the team takes a sample from each of the dozen strains and freezes them. These stocks are the experiment’s “fossil record” – its living save-files. By thawing them out and growing them afresh, the team can compare their fates to that of the original dozen. As the late Stephen Jay Gould once said, they can “replay life’s tape”.

Using the bacteria, Robert Woods and Jeffrey Barrick (both now working in different labs) have shown that slow and steady can often win the evolutionary race. “Hare” bacteria, which initially take the lead and outperform their peers, might eventually lose out to strains with hidden potential – “tortoise” strains that were better at evolving.

Woods and Barrick knew that by the 1500th generation, many of the bacteria had genetic changes (mutations) in two important genes, which allowed them to outcompete their peers. These changes weren’t new – many of the microbes already had them by the 500th generation. To understand how these “eventual winners” rose to power, Woods and Barrick cloned two strains of bacteria which had the right mutations from the 500th generation stocks. They also cloned two “eventual losers” that lacked these important mutations.

All of these strains were superior to the ancestral one – the 0th generation bug that started the whole experiment. But to everyone’s surprise, the eventual losers were better adapted than the eventual winners. When pitted against each other, the so-called losers came out on top. In direct battle, with no further changes, the “winners” would have been driven to extinction within another 350 generations. How did they survive, let alone triumph?

Did they just get lucky? To find out, Woods and Barrick replayed the experiment… repeatedly. They made ten clones of each of their four chosen strains at the 500 generation mark, and grew them for almost 900 more. You can see the results in the colourful graphs below (see footnote). The vertical axis in either direction is a measure of evolution – it represents how much the strains had changed from the originals. The eventual winners (right) started changing about a hundred generations earlier than the eventual losers (left) and they did so more quickly and more dramatically.

By 800 generations, the winners had more than made up for the losers’ headstart. When pitted against each other, on average, they were the superior strains.

What gave the winners their eventual edge? They weren’t evolving any faster, for they ended up with the same number of extra mutations as the losers. Instead, Woods and Barrack found that the eventual winners started off with the right backgrounds.

The winners eventually gained a mutation in a gene called spoT, while none of the losers did. The gene affects the way in which DNA is packaged. Mutations that alter spoT can set off sweeping changes across the entire genome, radically changing which genes are switched on or off. And this particular mutation turned out to be very beneficial to the bacteria that picked it up.

The losers, unfortunately, never did. They had a mutation in a different gene called topA (which also controls the packaging of DNA) that cancelled out the benefits of the spoT one. Their version of topA prevented them from ever picking up the valuable spoT mutation – after all, what would be the point? The winners had no such problems – the critical spoT mutation could live in perfect harmony with their version of topA.

So the eventual winners were able to pick up, and benefit from, a new genetic innovation that the eventual losers weren’t in a position to appreciate. As Woods and Barrack write, the losers “shut the door on at least one important avenue for further improvement.” While they snoozed in their comfortable lead, their tortoise peers overtook them.

Reference: Woods, Barrick, Cooper, Shrestha, Kauth & Lenski. 2011. Second-Order Selection for Evolvability in a Large Escherichia coli Population. Science http://dx.doi.org/10.1126/science.1198914If the citation link isn’t working, read why here

More on the long-term evolution experiment: History restricts and guides the evolution of innovations

Footnote: Woods and Barrick used a really elegant method to monitor the evolution of their forty cloned strains. In each culture, they mixed two versions of the same strain in equal proportions – one that could eat a sugar called arabinose and one that couldn’t. Aside from this difference, the two versions were genetically identical. There wasn’t any arabinose in their surroundings, so this ability didn’t matter to the bacteria. It did however matter to Woods and Barrack – it gave them an easy way to track the evolution of their strains. Over time, new mutations turned up that gave specific cells an advantage and soon edged out their weaker siblings. If these mutations turned up in arabinose-eating cells, then the population as a whole became better at consuming the sugar; otherwise, they became worse. The change in arabinose-eating ability – in either direction – showed how far the bacteria had changed from their original forms.

CATEGORIZED UNDER: Bacteria, Evolution

Comments (11)

  1. Lenski’s experiment never ceases to amaze me *_*

  2. “Last month, the bacteria passed their 50,000th generation.”

    Last year I guess – February 2010 ;-) .

    Regards.

  3. amphiox

    In the picture, is the strain in flask A-3 (the one with the uniquely cloudier fluid in the flask) the famous citrate strain?

  4. amphiox

    Interestingly, this seems to parallel, at least in broad strokes, patterns observed in the fossil record. The most successful and dominant lineages at any given time (the hares) often end up going extinct and very rarely end up being the ancestors of the most successful and dominant lineages of later time periods, which most often descend from rarer, less conspicuous ancestors (the turtles).

  5. Were they randomly exposed to DDT?

  6. These e. coli haven’t learned to read, obviously.

    “There are no limits. There are plateaus, and you must not stay there; you must go beyond them. If it kills you, it kills you.” – Bruce Lee

  7. DavidB

    I’m not sure what the significance of this is supposed to be. If the 12 evolving strains are isolated from each other, they are not in competition, the ‘tortoises’ are able to go at their own pace, and may eventually speed up and pass the ‘hares’. It is interesting if they do (and to understand the mechanisms), but does this have any relevance to the course of evolution in nature, where the ‘tortoises’ would just go extinct?

    I notice that in the earlier post there was a rather different account of the experiment – or maybe a different version of it. In that version the ‘tortoises’ survived because they were able to exploit a different nutrient from the one favoured by the ‘hares’. This meant they were able to survive in low concentrations despite their competitive disadvantage.

  8. @Amphiox – Yep, it’s the citrate-using one. Neat, huh?

    @DavidB – The tortoises and hares didn’t come from separate flasks. They were competing strains within the same cultures. The earlier post refers to a different paper coming out of the same experiment and it’s irrelevant to this story. The events described in that post happened after 30,000+ generations; the events in this one started happening after just 500-1500.

  9. amphiox

    One question that interests me is how the EWs managed to survive those first 350 generations or so before they overtook the ELs in relative fitness. Was it simply a question of hanging on as a minority population in head-to-head competition until they turned the competitive tables?

    Or was it something more complicated that that? Presumably, in the original experiment, at generation 500, there were other variants in the population besides the EW and EL strains tested. Could there have been interactions between the EWs and other, untested variants, within the ‘ecosystems’ of the flasks that provided a sheltered niche for the EWs that perhaps protected them to some degree from direct competition with the ELs, giving them the opportunity to survive until they accrued to additional mutations that ultimately allowed their relative fitness to overtake the ELs?

  10. amphiox

    Yep, it’s the citrate-using one. Neat, huh?

    Mondo neat indeed. That picture is “evolution before our eyes”. 12 initially identical strains, from one common ancestor, and now 20 years later, there is a difference between them so obvious that we can see it with the naked eye. So obvious that someone with no training whatsoever in microbiology can recognize that it is there.

  11. JSmith

    Lenski bred the dozen strains from a common ancestor in ***1988.***

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