The drivers of squirrelpox virus dynamics in its grey squirrel reservoir host

Many pathogens of conservation concern circulate endemically within natural wildlife reservoir hosts and it is imperative to understand the individual and ecological drivers of natural transmission dynamics, if any threat to a related endangered species is to be assessed. Our study highlights the key drivers of infection and shedding dynamics of squirrelpox virus (SQPV) in its reservoir grey squirrel (Sciurus carolinensis) population. To clarify SQPV dynamics in this population, longitudinal data from a 16-month mark-recapture study were analysed, combining serology with real-time quantitative PCR to identify periods of acute viraemia and chronic viral shedding. At the population level, we found SQPV infection prevalence, viral load and shedding varied seasonally, peaking in autumn and early spring. Individually, SQPV was shown to be a chronic infection in >80% of grey squirrels, with viral loads persisting over time and bouts of potential recrudescence or reinfection occurring. A key recurring factor significantly associated with SQPV infection risk was the presence of co-infecting squirrel adenovirus (ADV). In dual infected squirrels, longitudinal analysis showed that prior ADV viraemia increased the subsequent SQPV load in the blood. However, there was a strong, negative association between prior ADV viraemia and subsequent SQPV shedding from the forearm, probably caused by ADV prolonging the SQPV acute viraemic phase, so delaying onset of the chronic shedding phase, and thereby altering viral shedding patterns over the time scales examined here. Hence, co-circulating ADV infection may be involved in mediating both the quantitative levels of SQPV infection and the timing and degree of subsequent infectiousness of grey squirrels.