The evolution of microbial populations in simple environments such as chemostats is still not fully understood. The classical interpretation of adaptation involves a process of successive substitution whereby a new dominant genotype arises by mutation from the genotype previously dominant and spreads more or less rapidly through the population until it is nearly fixed. The population is, thus, nearly uniform most of the time. Some observations suggest that the process may be more complicated, but it remains formidably difficult to assemble the phylogeny of an evolving culture in sufficient detail to be sure. We report experiments with an electronic microcosm inhabited by self-replicating computer programs whose phylogeny can be rendered completely transparent. The physiology of these programs is different in many respects from that of organic creatures, but their population biology has many features in common, including a very extensive, if not unbounded, range of variation. Experimental populations evolved through point mutations (many of which were quasi-neutral when they were viable) and through rearrangements that led to a change in genome size and often had large effects on fitness. As a general rule, smaller genomes execute fewer instructions in order to replicate, the rate of replication increases as the number of instructions executed declines, and the rate of replication in pure culture is a good predictor of success in mixture. When cultured with CPU (central processing unit) time as the sole limiting resource, smaller genomes, therefore, evolve as a correlated response to natural selection for faster replication. The genetic basis of adaptation was highly contingent and always differed in replicate experiments. The pattern of evolution depends on mutation rate. At low mutation rates of 0.01 per genome per generation or less, we observed classic periodic selection, with each dominant genotype descending from the previous dominant and rising to a frequency of 0.8 or more. At higher mutation rates of about 0.1 per genome per generation, the most abundant genotypes rarely exceeded a frequency of about 0.4, and rare genotypes present in a few copies comprised a large part of the population. New dominant genotypes did not usually descend directly from previous dominants but, instead, from one of the many rare or moderately abundant genotypes. We suggest that the conventional chemostat paradigm may hold only as a special case at very low mutation rates and that the dynamics and diversity of evolving populations, even in the simplest conditions, may be more complex than is usually recognized. Artificial genetic autoadaptive systems are likely to be useful in constructing theory for situations that lie beyond the boundary of conventional population genetics.