Genotypic but not phenotypic historical contingency revealed by viral experimental evolution

Abstract

BACKGROUND: The importance of historical contingency in determining the potential of viral populations to evolve has been largely unappreciated. Identifying the constraints imposed by past adaptations is, however, of importance for understanding many questions in evolutionary biology, such as the evolution of host usage dynamics by multi-host viruses or the emergence of escape mutants that persist in the absence of antiviral treatments. To address this issue, we undertook an experimental approach in which sixty lineages of Tobacco etch potyvirus that differ in their past evolutionary history and degree of adaptation to Nicotiana tabacum were allowed to adapt to this host for 15 rounds of within host multiplication and transfer. We thereafter evaluated the degree of adaptation to the new host as well as to the original ones and characterized the consensus sequence of each lineage. RESULTS: We found that past evolutionary history did not determine the phenotypic outcome of this common host evolution phase, and that the signal of local adaptation to past hosts had largely disappeared. By contrast, evolutionary history left footprints at the genotypic level, since the majority of host-specific mutations present at the beginning of this experiment were retained in the end-point populations and may have affected which new mutations were consequently fixed. This resulted in further divergence between the sequences despite a shared selective environment. CONCLUSIONS: The present experiment reinforces the idea that the answer to the question "How important is historical contingency in evolution?" strongly depends on the level of integration of the traits studied. A strong historical contingency was found for TEV genotype, whereas a weak effect of on phenotypic evolution was revealed. In an applied context, our results imply that viruses are not easily trapped into suboptimal phenotypes and that (re)emergence is not evolutionarily constrained.