Drastic bottleneck events have been reproduced with laboratory populations of viruses in the form of plaque-to-plaque transfers. This design served to verify experimentally the operation of Müller’s ratchet, or fitness decrease by the irreversible incorporation of mutations in asexual organisms in absence of compensatory mechanisms. The serial bottleneck transfers unveiled the presence rare mutations, not seen in standard laboratory or natural viral populations. In absence of forced bottleneck events, such rare mutations would be lost by negative selection because of their fitness cost. The investigation of how FMDV clones debilitated by Müller’s ratchet regained replicative fitness revealed several alternative molecular pathways for fitness recovery. The implications of this observation went largely unnoticed until recent results with hepatitis C virus (HCV) have also suggested the accessibility of multiple pathways for fitness gain. Also, extensive passage of a biological clone of FMDV in BHK-21 cells conferred the capacity to infect several human cell lines in addition to the expected fitness increase for multiplication in BHK-21 cells. Thus, several lines of evidence suggest that fitness gain in a specific environment may paradoxically broaden the phenotypic potential of a virus. It will be interesting to investigate whether focused adaptation of other viruses to a specific environment may also entail a broadening of diversity, with many phenotypic variants attaining similar fitness levels. If generalized, this broadening of phenotypic space would provide a new interpretation of the molecular basis of adaptation, and explain why adaptation to alternative environments may not lead to attenuation.