Typically, systems biology focuses on the form and function of networks of biochemical interactions. Questions inevitably arise as to the evolutionary origin of those networks' properties. Such questions are of interest to a growing number of systems biologists, and several groups have published studies shown how varying environments can affect network topology and lead to increased evolvability. For decades, evolutionary biologists have also investigated the evolution of evolvability and its relationship to the interactions between genotype and phenotype. While the perspectives of systems and evolutionary biologists sometimes differ, their interests in patterns of interactions and evolvability have much in common. This thesis attempts to bring together the perspectives of systems and evolutionary theory to investigate the evolutionary effects of fluctuating environments. Chapter 1 introduces the necessary themes, terminology and literature from these fields. Chapter 2 explores how rapid environmental fluctuations, or "noise", affects network size and robustness. In Chapter 3, we use the Avida platform to investigate the relationship between genetic architecture, fluctuating environments and population biology. Chapter 4 examines contingency loci as a physical basis for evolvability, while chapter 5 presents a 500-generation laboratory evolution experiment which exposes E. coli to varying environments. The final discussion, concludes that the evolution of generalism can lead to genetic architectures which confer evolvability, which may arise in rapidly fluctuating environments as a by-product of generalism rather than as a selected trait.