Evolutionary trade-offs and adaptive phenotypic plasticity under multidimensional selective pressure

The structure and function of biological systems at all levels of organization are the product of evolutionary change. However, predicting how phenotypes respond to selective pressure via a quantitative theory of evolution remains challenging due to a number of factors complicating the genotype to phenotype map. Genetic architecture presents an internal source of complexity, constraining adaptive responses by imposing trade-offs between beneficial traits. This is of particular consequence in natural environments, where selective pressure almost always acts on multiple traits simultaneously. Meanwhile, we must also consider environmental influence as a source of external complexity for the genotype-phenotype map. The environment determines the selective pressure by defining the fitness function, influences the adaptive capacity of mutations and shapes traits directly through phenotypic plasticity. Moreover, the ability of plasticity to allow a single genotype to thrive in multiple environmental conditions could provide an important mechanism for the evolution of generalists. Predicting evolutionary dynamics will require careful consideration of the interplay between complex selection pressures, adaptability under genetic constraints as well as non-genetic means of phenotypic diversification. To this end, we study the evolution of bacterial migration through a porous environment as a model system. We show that repeated selection at the edge of expanding colonies dramatically enhances the speed at which Escherichia coli populations spread through soft agar. Because this process depends on both motility and growth, it provides a unique opportunity to study adaptation under multidimensional selective pressure of traits with thoroughly-characterized molecular bases. In the first part of the work, we performed selection in both rich and minimal media and found that a trade-off between swimming speed and growth rate constrains the evolution of faster migration. Fast migration in rich medium was evolved by enhancing swimming despite slower growth, while fast migration in minimal medium was evolved by enhancing growth despite slower swimming. Sequencing and genetic engineering revealed the trade-off to be caused by antagonistic pleiotropy of mutations in negative regulatory elements. A model of constrained evolution showed that an organism's genetic capacity to vary traits can depend on its environment, coupling with the selective pressure to ultimately determine the direction of evolution. In the second part of the work, we performed selection in four different minimal media environments and found that strains evolved in any one condition exhibited fast migration in all conditions. To investigate this generality, we measured the swimming and growth phenotypes of all evolved strains in all environments. We found that strains measured in each environment exhibited a distinct growth and motility phenotype regardless of their evolutionary history. Therefore, we concluded that the evolution of migration rate generality in these conditions was achieved by phenotypic plasticity. Plasticity allowed evolved strains to optimize their phenotype for different environments without needing to select for particular genetic variants, demonstrating a powerful strategy for the evolution of generalist organisms