Abstract

To date, few studies of parasite epidemiology have investigated ‘who acquires infection from whom’ in wildlife populations. Nonetheless, identifying routes of disease transmission within a population, and determining the key groups of individuals that drive parasite transmission and maintenance, are fundamental to understanding disease dynamics. Gammaherpesviruses are a widespread group of DNA viruses that infect many vertebrate species, and murine gammaherpesviruses (i.e. MuHV-4) are a standard lab model for studying human herpesviruses, for which much about the pathology and immune response elicited to infection is well understood. However, despite this extensive research effort, primarily in the lab, the transmission route of murine gammaherpesviruses within their natural host populations is not well understood. Here, we aimed to understand wood mouse herpesvirus (WMHV) transmission, by fitting a series of population dynamic models to field data on wood mice naturally infected with WMHV and then estimating transmission parameters within and between demographic groups of the host population. Different models accounted for different combinations of host sex (male/female), age (subadult/adult) and transmission functions (density/frequency-dependent). We found that a density-dependent transmission model incorporating explicit sex groups fitted the data better than all other proposed models. Male-to-male transmission was the highest among all possible combinations of between- and within-sex transmission classes, suggesting that male behaviour is a key factor driving WMHV transmission. Our models also suggest that transmission between sexes, although important, wasn’t symmetrical, with infected males playing a significant role in infecting naïve females but not vice versa. Overall this work shows the power of coupling population dynamic models with long-term field data to elucidate otherwise unobservable transmission processes in wild disease systems.

Highlights

  • Understanding ‘who acquires infection from whom’ is a key chal­ lenge in epidemiology, population biology and disease ecology (Webster et al, 2017)

  • 15.4% animals were seropositive for wood mouse herpesvirus (WMHV), with a significant difference in WMHV incidence between the sexes (0.1 of female captures were seropositive, compared to 0.19 of male captures; X2 = 19.79, p < 0.001)

  • One way to identify and quantify potential transmission routes is through the fitting of mechanistic models to epidemiological data, where we can estimate the magnitude of possible transmission-relevant parameters in the process (Baguelin et al, 2020)

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Summary

Introduction

Understanding ‘who acquires infection from whom’ is a key chal­ lenge in epidemiology, population biology and disease ecology (Webster et al, 2017). For managing parasite species (defined here generally to include both macroparasites (i.e. helminths, ectoparasites) and micro­ parasites/pathogens (i.e. viruses, bacteria, protozoans)) that can infect multiple host species, it is clearly important to establish both which host species play an important role in transmission (Fenton et al, 2015; Streicker et al, 2013), and why and how they contribute more to transmission than other species. While it is clearly important to understand transmission between different groups of species for gener­ alist parasites, it is true for specialist parasites that infect only a single host species that it can be important to distinguish the contribu­ tion of different host population categories, such as age and sex classes, to determine which behaviours and groups are driving infection (Anderson and May, 1991). It can be notoriously difficult to identify routes of disease transmission and the key individuals or groups driving transmission in natural populations, which has limited our knowledge about who acquires infection from whom for many wildlife diseases

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