Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli

Abstract

The causes and mechanisms of evolutionary diversification are central issues in biology. Geographic isolation is the traditional explanation for diversification, but recent theoretical and empirical studies have shown that frequency-dependent selection can drive diversification without isolation and that adaptive diversification occurring in sympatry may be an important source of biological diversity. However, there are no empirical examples in which sympatric lineage splits have been understood at the genetic level, and it is unknown how predictable this process is—that is, whether similar ecological settings lead to parallel evolutionary dynamics of diversification. We documented the genetic basis and the evolutionary dynamics of adaptive diversification in three replicate evolution experiments, in which competition for two carbon sources caused initially isogenic populations of the bacterium Escherichia coli to diversify into two coexisting ecotypes representing different physiological adaptations in the central carbohydrate metabolism. Whole-genome sequencing of clones of each ecotype from different populations revealed many parallel and some unique genetic changes underlying the derived phenotypes, including changes to the same genes and sometimes to the same nucleotide. Timelines of allele frequencies extracted from the frozen “fossil” record of the three evolving populations suggest parallel evolutionary dynamics driven at least in part by a co-evolutionary process in which mutations causing one type of physiology changed the ecological environment, allowing the invasion of mutations causing an alternate physiology. This process closely corresponds to the evolutionary dynamics seen in mathematical models of adaptive diversification due to frequency-dependent ecological interactions. The parallel genetic changes underlying similar phenotypes in independently evolved lineages provide empirical evidence of adaptive diversification as a predictable evolutionary process. The causes and mechanisms of evolutionary diversification are central issues in biology. There is well-established theory that predicts that adaptive diversification can arise because of ecological interactions between individuals, such as competition or predation, but there are no empirical examples in which this process has been observed at the genetic level. We documented the genetic basis of adaptive diversification resulting from competition for resources in populations of the bacterium Escherichia coli. The populations diversified into two coexisting ecotypes representing different physiological adaptations. We found that similar but independently evolved phenotypes often shared mutations in the same gene and, in four cases, shared identical mutations at the same nucleotide position. Timelines of allele frequencies extracted from the frozen “fossil record” of three evolving populations showed parallel evolutionary dynamics, suggesting that mutations causing one type of physiology changed the ecological environment and allowed invasion of mutations causing an alternate physiology. The results provide empirical evidence of adaptive diversification as a predictable evolutionary process.