Richard Lenski (of the University of Michigan) and his colleagues have published a new paper in Nature (Blount et al., 2012) entitled “Genomic analysis of a key innovation in an experimental Escherichia coli population.” Lenski, as most readers will be aware, is famed for his long-term E. coli evolution experiment. The abstract of the new paper reads,
Evolutionary novelties have been important in the history of life, but their origins are usually difficult to examine in detail. We previously described the evolution of a novel trait, aerobic citrate utilization (Cit+), in an experimental population of Escherichia coli. Here we analyse genome sequences to investigate the history and genetic basis of this trait. At least three distinct clades coexisted for more than 10,000 generations before its emergence. The Cit+ trait originated in one clade by a tandem duplication that captured an aerobically expressed promoter for the expression of a previously silent citrate transporter. The clades varied in their propensity to evolve this novel trait, although genotypes able to do so existed in all three clades, implying that multiple potentiating mutations arose during the population’s history. Our findings illustrate the importance of promoter capture and altered gene regulation in mediating the exaptation events that often underlie evolutionary innovations.
Those who have read Richard Dawkins’s 2009 book The Greatest Show on Earth will remember that this particular example of evolutionary “innovation” was used as a flagship demonstration of evolution’s power. Richard Dawkins explains,
The broth contained plenty of citrate, but E. coli normally can’t use it, at least not where there is oxygen in the water, as there was in Lenski’s flasks. But if only a mutant could ‘discover’ how to deal with citrate, a bonanza would open up for it. This is exactly what happened with Ara-3. This tribe, and this tribe alone, suddenly acquired the ability to eat citrate as well as glucose, rather than only glucose. The amount of available food in each successive flask in the lineage therefore shot up. And so did the plateau at which the population in each successive flask daily stabilized.
Our own Michael Behe, in a 2010 peer-reviewed article in the Quarterly Review of Biology, pointed out that citrate can already be utilised by E. coli under low-oxygen conditions, and hypothesized that a simple modification of gene-regulation was likely responsible for the observed phenotype.
With this new paper in Nature (which was also picked up by Carl Zimmer), the mechanistic basis for this apparent evolutionary innovation has now been identified. Ann Gauger reports on the new paper at the Biologic Institute’s blog. She reports,
After an enormous amount of work, having sequenced the genomes of many clones along the lineages that led to the ability to use citrate, as well as lineages that never did, and testing the phenotypes of identified mutations, Blount et al. have now reported that Behe was largely right. The key innovation was a shift in regulation of the citrate operon, caused by a rearrangement that brought it close to a new promoter.
The new trait additionally required one or two pre-adaptive steps that could not be definitively identified, perhaps because of variable or weak phenotypic effects, perhaps because of epistatic interactions. Once in place though, those mutations enabled the next step, a duplication of the citrate operon that moved it next to another promoter, enabling the aerobic transport of citrate and its metabolism.
The total number of mutations postulated for this adaptation is two or three, within the limits proposed for complex adaptations by Axe  and Behe in Edge of Evolution. Because the enabling pre-adaptive mutations could not be identified, though, we don’t know whether this was one mutation, a simple step-wise series of adaptive mutations, or a complex adaptation requiring one or two pre-adaptations before the big event.
But does this adaptation constitute a genuine innovation? That depends on the definition of innovation you use. It certainly is an example of reusing existing information in a new context, thus producing a new niche for E coli in lab cultures. But if the definition of innovation is something genuinely new, such as a new transport molecule or a new enzyme, then no, this adaptation falls short as an innovation. And no one should be surprised.