Adaptive and pleiotropic effects of evolution in synonymous sugar environments

Abstract Adaptation to an environment is enabled by the accumulation of beneficial mutations. When adapted populations are shifted to other environments, the byproduct or pleiotropic fitness effects of these mutations can be wide-ranged. Since there exists no molecular framework to quantify relatedness of environments, predicting pleiotropic effects based on adaptation has been challenging. In this work, we ask if evolution in highly similar environments elicits correlated adaptive and pleiotropic responses. We evolve replicate populations of Escherichia coli in non-stressful environments that contain either a mixture of glucose and galactose, lactose, or melibiose as the source of carbon. We term these similar sugars as “synonymous”, since lactose and melibiose are disaccharides made up of glucose and galactose. Therefore, the evolution environments differed only in the way carbon was presented to the bacterial population. After 300 generations of evolution, we see that the adaptive responses of these populations are not predictable. We investigate the pleiotropic effects of adaptation in a range of non-synonymous environments, and show that despite uncorrelated adaptive changes, the nature of pleiotropic effects is largely predictable based on the fitness of the ancestor in the non-home environments. Overall, our results highlight how subtle changes in the environment can alter adaptation, but despite sequence-level variations, pleiotropy is qualitatively predictable. Lay Summary In nature, evolution in “similar” environments is believed to elicit identical responses. For example, the arctic fox and ptarmigan, which are two unrelated species living in the arctic, have evolved to turn white in the winters. They did not evolve this ability because they from the common ancestor, but because the environment favoured this trait. In this work, we ask what happens to evolving populations if there are minute changes in the environment, and what are the consequences of adapting in these environments that are “almost identical”, or as we call them, “synonymous”. We evolve replicate populations of the bacteria E. coli in three synonymous environments, and quantify their ability to grow in both synonymous and non-synonymous environments. We see that evolution does not proceed in an identical fashion in these populations, and that each environment favours a different trait. However, interestingly, in non-synonymous environments, these three sets of populations perform almost identically, and their growth is qualitatively predictable. Our results show that even simple and subtle changes in the environment can act as drivers of biodiversity.