The tortoise or the hare? Impacts of within-host dynamics on transmission success of arthropod-borne viruses

Abstract

Arthropod-borne viruses (arboviruses) are maintained in a cycle of alternating transmission between vertebrate hosts and arthropod vectors. Arboviruses possess RNA genomes capable of rapid diversification and adaptation, and the between-host trade-offs inherent to host alternation impose well-documented constraints on arbovirus evolution. Here, we investigate the less well-studied within-host trade-offs that shape arbovirus replication dynamics and transmission. Arboviruses generally establish lifelong infection in vectors but transient infection of variable magnitude (i.e. peak virus concentration) and duration in vertebrate hosts. In the majority of experimental infections of vertebrate hosts, both the magnitude and duration of arbovirus replication depended upon the dose of virus administered, with increasing dose resulting in greater magnitude but shorter duration of viraemia. This pattern suggests that the vertebrate immune response imposes a trade-off between the height and breadth of the virus replication curve. To investigate the impact of this trade-off on transmission, we used a simple modelling approach to contrast the effect of ‘tortoise’ (low magnitude, long duration viraemia) and ‘hare’ (high magnitude, short duration viraemia) arbovirus replication strategies on transmission. This model revealed that, counter to previous theory, arboviruses that adopt a tortoise strategy have higher rates of persistence in both host and vector populations.