Evolutionary Genomics of Host Adaptation in Vesicular Stomatitis Virus

Abstract

Populations experiencing similar selection pressures can sometimes diverge in the genetic architectures underlying evolved complex traits. We used RNA virus populations of large size and high mutation rate to study the impact of historical environment on genome evolution, thus increasing our ability to detect repeatable patterns in the evolution of genetic architecture. Experimental vesicular stomatitis virus populations were evolved on HeLa cells, on MDCK cells, or on alternating hosts. Turner and Elena (2000. Cost of host radiation in an RNA virus. Genetics. 156:1465-1470.) previously showed that virus populations evolved in single-host environments achieved high fitness on their selected hosts but failed to increase in fitness relative to their ancestor on the unselected host and that alternating-host-evolved populations had high fitness on both hosts. Here we determined the complete consensus sequence for each evolved population after 95 generations to gauge whether the parallel phenotypic changes were associated with parallel genomic changes. We also analyzed the patterns of allele substitutions to discern whether differences in fitness across hosts arose through true pleiotropy or the presence of not only a mutation that is beneficial in both hosts but also 1 or more mutations at other loci that are costly in the unselected environment (mutation accumulation [MA]). We found that ecological history may influence to what extent pleiotropy and MA contribute to fitness asymmetries across environments. We discuss the degree to which current genetic architecture is expected to constrain future evolution of complex traits, such as host use by RNA viruses.

Genomic Evolution of Vesicular Stomatitis Virus Strains with Differences in Adaptability

“…5). All three substitutions have appeared in additional independent experiments during MARM U and/or wt adaptation (4,27,36). These results are consistent with previous work that demonstrated that viruses evolving under regimens of strict positive selection do not necessarily accumulate an excess of nonsynonymous mutations (31).…”

Effect of Host Species on Topography of the Fitness Landscape for a Plant RNA Virus

“…Not all potential hosts in the host range (different species or different genotypes of the same species) of a virus are equally susceptible to infection, and it is generally assumed that a tight match may exist between host genotypes and virus genotypes to allow a virus to successfully infect a host (6). Indeed, a substantial amount of data supports the idea that by evolving in a single host species or genotype, viruses become specialists (7)(8)(9)(10), whereas by evolving in multiple host species, the result may be no-cost generalists (7,(11)(12)(13).…”

Predicting Virus Evolution: The Relationship between Genetic Robustness and Evolvability of Thermotolerance

“…Resource generalization is often assumed to be costly, fostering arguments that natural species biodiversity can be explained by a tendency for niche specialists to be favored over niche generalists (Finke and Snyder 2008). However, many experimental evolution studies in microbes such as RNA viruses have shown that genotypes that evolve to use multiple hosts are not necessarily fitness disadvantaged relative to their more specialized counterparts (Novella et al 1999;Turner and Elena 2000;Remold et al 2008). These collections of microbes could be harnessed to conduct studies examining whether an evolved broad host range is superior to a narrow host range, when avoidance of extinction is the selective challenge.…”