Speaker
Description
Evolution can be viewed as a game where the object is to keep playing. From this perspective, focus is brought to the properties of lineages that enable their success over long spans of evolutionary time, rather than the phenotypes and performance of individuals in the contemporary environment. One property required for long-term evolutionary success is the ability of a lineage to translate genetic mutation into adaptive phenotypic variation so as to meet the demands imposed by changing selection pressures. That is, a lineage must be sufficiently evolvable. Competition between lineages that vary in evolvability can generate natural selection dynamics and in theory optimize evolvability in a manner akin to the optimization of fitness. However, addressing the evolution of such long-term phenomena is experimentally challenging. Here, we achieve this through a bacterial evolution experiment that explicitly rewards evolvable lineages. Specifically, lineages are challenged to repeatedly activate and then inactivate a single focal phenotype that is in turn beneficial then deleterious across time. Failure to reach the target phenotypic state at any one point results in extinction (death) of that lineage and replacement (birth) by a contemporary extant lineage from the population. This lineage-level death-birth process allows natural selection to operate on an entity reproducing beyond the generation time of individual cells and therefore over a timescale where variation in evolvability is visible to selection. We identify each mutation that occurs along the trajectory of the evolving lineages, revealing how the genotype-phenotype map and mutational biases both shape and are shaped by evolution, as well as how this influences the success or failure of a given lineage. Moreover, we show that the most successful lineages increase in evolvability through the establishment of mutational biases that facilitate rapid switching between the target phenotypic states. Remarkably, due to the increased speed with which the target phenotype is generated in these lineages, an additional adaptive step becomes possible that optimizes cell fitness with respect to other aspects of the environment – a possibility that is stalled in lineages not possessing the rapid-switching ability. These results demonstrate the power of lineage selection in shaping evolvability and represent the clearest experimental evidence yet for the capacity of evolution to act in a self-facilitating manner.
