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Arthropod-borne viruses (arboviruses), such as Zika virus, chikungunya virus, and West Nile virus (WNV), pose continuous threats to emerge and cause large epidemics. Often, these events are associated with novel virus variants optimized for local transmission that first arise as minorities within a host. Thus, the conditions that regulate the frequency of intrahost variants are important determinants of emergence. Here, we describe the dynamics of WNV genetic diversity during its transmission cycle. By temporally sampling saliva from individual mosquitoes, we demonstrate that virus populations expectorated by mosquitoes are highly diverse and unique to each feeding episode. After transmission to birds, however, most genetic diversity is removed by strong purifying selection. Further, transmission of potentially mosquito-adaptive WNV variants is strongly influenced by genetic drift in mosquitoes. These results highlight the complex evolutionary forces a novel virus variant must overcome to alter infection phenotypes at the population level.
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•Individual mosquitoes can transmit distinct virus populations during each bloodmeal•The distinct virus populations are largely shaped by genetic drift•Strong selection in birds purges most nonsynonymous mutations•West Nile virus evolution is characterized by cycles of diversification and selection
Grubaugh et al. describe how a single infected mosquito can transmit different virus populations during each blood feeding, highlighting the incredible amount of adaptive potential that exists in nature. This diversity, however, is rapidly removed during infection of a vertebrate host, which acts to maintain virus fitness.