Abstract
A growing number of studies report that viruses can spread in groups in so-called collective infectious units. By increasing the cellular multiplicity of infection, collective dispersal may allow for social-like interactions, such as cooperation or cheating. Yet, little is known about how such interactions evolve. In previous work with vesicular stomatitis virus, we showed that virion aggregation accelerates early infection stages in most cell types, providing a short-term fitness benefit to the virus. Here, we examine the effects of virion aggregation over several infection cycles. Flow cytometry, deep sequencing, infectivity assays, reverse transcription-quantitative PCR, and electron microscopy revealed that virion aggregation rapidly promotes the emergence of defective interfering particles. Therefore, virion aggregation provides immediate fitness benefits to the virus but incurs fitness costs after a few viral generations. This suggests that an optimal strategy for the virus is to undergo virion aggregation only episodically, for instance, during interhost transmission.IMPORTANCE Recent insights have revealed that viruses use a highly diverse set of strategies to release multiple viral genomes into the same target cells, allowing the emergence of beneficial, but also detrimental, interactions among viruses inside infected cells. This has prompted interest among microbial ecologists and evolutionary biologists in studying how collective dispersal impacts the outcome of viral infections. Here, we have used vesicular stomatitis virus as a model system to study the evolutionary implications of collective dissemination mediated by viral aggregates, since this virus can spontaneously aggregate in the presence of saliva. We find that saliva-driven aggregation has a dual effect on viral fitness; whereas aggregation tends to increase infectivity in the very short term, virion aggregates are highly susceptible to invasion by noncooperative defective variants after a few viral generations.
Highlights
A growing number of studies report that viruses can spread in groups in so-called collective infectious units
A common feature among collective dispersal strategies is that they increase the cellular multiplicity of infection, defined as the average number of viral genomes that initiates the infection of a cell [16]
The evolution was initiated with a 1:1 mix of vesicular stomatitis virus (VSV)-green fluorescent protein (VSV-GFP) and VSV-mCherry to track the formation of aggregates, since these tend to produce doubly fluorescent cells
Summary
A growing number of studies report that viruses can spread in groups in so-called collective infectious units. IMPORTANCE Recent insights have revealed that viruses use a highly diverse set of strategies to release multiple viral genomes into the same target cells, allowing the emergence of beneficial, and detrimental, interactions among viruses inside infected cells. This has prompted interest among microbial ecologists and evolutionary biologists in studying how collective dispersal impacts the outcome of viral infections. Elevating the cMOI could reduce the chances of abortive infections due to stochastic processes occurring during the earliest stages of infection, when low transcription or translation levels, dilution, or degradation of essential components could limit establishment of the infection These or other possible infection barriers produce an Allee effect at the cellular level, defined as a positive correlation between the per-capita viral progeny production and the cMOI. A previous study with HIV-1 supported the idea that high cMOIs help overcome early barriers to infection [18], and at least three additional studies with influenza A virus [19, 20] and vaccinia virus [21] are consistent with the notion that increasing the cMOI improves infectivity
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