In prior research, we found the way guppy life histories evolve in response to living in environments with a high or low risk of predation is consistent with life history theory that assumes no density-dependence. We later found that guppies from high predation environments experience higher mortality rates than those from low predation environments, but the increased risk was evenly distributed across all age/size classes. Life history theory that assumes density-independent population growth predicts that life histories will not evolve under such circumstances, yet we have shown with field introduction experiments that they do evolve. However, theory that incorporates density regulation predicts this pattern of mortality can result in the patterns of life history evolution we had observed. Here we report on density manipulation experiments performed in populations of guppies from low predation environments to ask whether natural populations normally experience density regulation and, if so, to characterize the short term demographic changes that underlie density regulation. Our experiments reveal that these populations are density regulated. Decreased density resulted in higher juvenile growth, decreased juvenile mortality rates and increased reproductive investment by adult females. Increased density causes reduced offspring size, increased fat storage by adult females and increased adult mortality.