Abstract
Viruses frequently spread among cells or hosts in groups, with multiple viral genomes inside the same infectious unit. These collective infectious units can consist of multiple viral genomes inside the same virion, or multiple virions inside a larger structure such as a vesicle. Collective infectious units deliver multiple viral genomes to the same cell simultaneously, which can have important implications for viral pathogenesis, antiviral resistance, and social evolution. However, little is known about why some viruses transmit in collective infectious units, whereas others do not. We used a simple evolutionary approach to model the potential costs and benefits of transmitting in a collective infectious unit. We found that collective infectious units could be favoured if cells infected by multiple viral genomes were significantly more productive than cells infected by just one viral genome, and especially if there were also efficiency benefits to packaging multiple viral genomes inside the same infectious unit. We also found that if some viral sequences are defective, then collective infectious units could evolve to become very large, but that if these defective sequences interfered with wild-type virus replication, then collective infectious units were disfavoured.
Highlights
Viruses disperse from host cells in many different ways
We model the theoretical plausibility of these three types of hypothesis: (i) if cells infected by multiple viral genomes are more productive; (ii) if packaging multiple genomes into the same unit is more efficient; (iii) if there is a high likelihood that genomes are defective
We found that collective infectious units (CIUs) were more likely to evolve when: (i) infections initiated by a single viral genome are relatively unsuccessful (Fig. 1c–d); (ii) a small number of initial infecting genomes can reach the maximal infection efficiency; (iii) additional genomes have a greater influence on infection success when there are fewer genomes infecting a cell; (iv) additional genomes result in a diminishing relationship with infection success (Fig. 1b–d)
Summary
Viruses disperse from host cells in many different ways. Some viruses disperse in single virions which each contain one genome. Other viruses can disperse in groups, with multiple genomes in the same virion, or multiple virions inside a larger structure These are called collective infectious units (CIUs), and are characterised by multiple viral genomes transmitting as part of the same infective structure (Sanjuán, 2017). Multiple virions can collectively disperse from the same host cell, for example inside extra-cellular vesicles formed of sections of host cell membrane, or inside protein-coated occlusion bodies (Altan-Bonnet and Chen, 2015; Chen et al, 2015; Santiana et al, 2018; Slack and Arif, 2007) These various kinds of collective infectious units appear to have evolved independently many times, since they exist in many different viral families and take a range of structural forms. Our aim is to generate testable predictions across a range of different CIUs and to encourage interplay between theory and data in the study of collective infectious units
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