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Review
. 2015 Aug 19;370(1675):20140299.
doi: 10.1098/rstb.2014.0299.

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

Benjamin M Althouse  1 , Kathryn A Hanley  2
Affiliations
Review

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

Benjamin M Althouse et al. Philos Trans R Soc Lond B Biol Sci. .

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.

Keywords: arthropod-borne virus; dynamics; host; trade-off; transmission; vector.

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Figures

Figure 1.
Figure 1.
Figure produced by Sean Vidal Edgerton Science Illustration (http://www.theillustration.co/).
Figure 2.
Figure 2.
Variation in viral replication curves across viruses and hosts. Figure shows viral replication (log10 PFU by day) of different strains of dengue 1, 2 and 3 in rhesus macaques ((a), (c) and (e), respectively; data from Althouse et al. [24]), and of two strains of Japanese encephalitis virus (Indian and Vietnamese) in three species of bird ((b,d,f), data from Nemeth et al. [25]). Lines are mean log10 PFU and shaded regions are mean ±1 s.d. Clear differences in the lag to viraemia, magnitude of viraemia and duration of viraemia are evident. (Online version in colour.)
Figure 3.
Figure 3.
Results of the stochastic arbovirus transmission model. (a) The infectivity curves used in model runs for a steady viraemia titre over the course of infection (constant transmission probability across infection), and (b) the curves for viral titre correlated with peaks in the infectious duration (higher viraemia leading to higher transmission). Lines indicate a mean duration 4 days with variance either 4 days (dark solid curve) or 1.6 days (dark dashed curve), and mean duration 25 days with variance either 25 days (light solid curve) or 12.5 days (light dashed curve). (c,d) Virus incidence in vertebrate hosts for the steady and correlated titre scenarios, respectively, and (e,f) the proportion of infected vectors in each scenario. Colours and line type correspond to distributions in (a,b). Lines are means of 50 stochastic simulations and shaded regions are mean ±1 s.d. Model parameters: transmissibility (probability of infection per infectious bite) = 0.3, amplitude of seasonality = 0.1; 0.5 bites per vertebrate host per day, vector birthrate = 1/7 d−1, vertebrate host birthrate = 1/60 yr−1, initial number of vectors = 15 000, initial number of vertebrate hosts = 10 000.
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