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Experimental evolution has become an increasingly common approach for studying evolutionary phenomena, as well as uncovering physiological connections in a manner complementary to traditional genetics. Here I describe the development of Methylobacterium as a model system for using experimental evolution to study questions at the intersection of metabolism and evolution. Each experiment was initiated to address a particular question inspired by patterns in natural methylotrophs, such as tradeoffs between single-carbon and multi-carbon growth, or the challenges involved in incorporating novel metabolic pathways or genes with poor codon usage that are acquired via horizontal gene transfer. What I could not have appreciated initially, however, was just how many fortuitous surprise findings would emerge. These have ranged from the repeatability of evolution, complex dynamics within populations, epistasis between beneficial mutations, and even the ability to use simple mathematical models to generate testable, quantitative hypotheses about the fitness landscape.