Microbial prions facilitate a variety of phenotypic switches. Recently-developed tools that can directly interrogate, in the living cell, the aggregation state of a protein have enabled a wider range of experiments for prion-mediated behaviors. With such tools, the roles of the yeast prion [SWI+] in migration and mating were studied. Although [SWI+] cells were consistently less fit than their [swi-] counterparts under traditional laboratory conditions, in these new phenotypic paradigms [SWI+] cells demonstrated a distinct advantage. [SWI+] cells dispersed over a larger area under conditions resembling rainfall and outcrossed more frequently. We postulate that many behaviors in microorganisms may be modulated by stochastic prion switching. In diverse and changing natural environments, prion switching at low frequency may promote greater fitness of the population by specializing a small number of individuals with altered responses to their environments.