Douglas H. Cornwall, James S. Ruff, Elizabeth R. Zachary, Chloe P. Young, Kathleen M. Maguire, Rachel J. Painter, Sophie M. Trujillo, Wayne K. Potts

Semi‐natural enclosure and population design. (a) Semi‐natural enclosure set up with six territories, four optimal territories (large bins) and two suboptimal territories (open nest boxes and feeder stations). (b) Study design showing three different population design groups: female only index (left), male only index (centre) and female and male index (right)

Pathogen life history is complex and consists of many challenges. One key challenge is transmitting from one host to another. The mode of transmission, or how a pathogen moves between hosts, helps determine both the likelihood of successful infection and the resulting harm experienced by the new host. Often a given pathogen can be transmitted by several modes (for example, vertically from a host’s mother or horizontally through fluid transfer from unrelated individuals); however, which mode is most common in nature is difficult to assess in simple laboratory experiments. In addition, host characteristics (such as sex, social status, and age) may influence, which transmission mode is more likely to occur.

The close association between house mice and human buildings provides a unique opportunity emulate their habitat and experimentally manipulate variables to determine how their pathogens move through a population. Here we use house mouse populations living under semi-natural conditions to evaluate the transmission dynamics of a mouse retrovirus—Friend Virus Complex—which is a well-established model for understanding various aspects of viral life history and immunity. Specifically, we test 1) whether horizontal or vertical is the dominant mode of transmission; 2) which sex, if either, drives horizontal transmission; 3) if one sex is harmed more by the virus; and 4) if the harm resulting from natural transmission vs. directly infecting a mouse with an injection differ.

This study demonstrates that horizontal transmission (not vertical) is the primary method Friend Virus Complex uses to spread among hosts and is driven primarily by male mice (likely while fighting over territories). In addition, our study highlights that males harbour more viral particles than do females despite experiencing similar levels of harm and that natural transmission results in less harmful infection than direct experimenter inoculation. These results upset the prevailing understanding of how this virus transmits, as previous work showed chiefly vertical transmission with some horizontal transmission occurring during sex; however, these studies did not consider all modes of transmission simultaneously to determine their relative contribution to viral spreading in a natural context.

Understating the natural transmission dynamics of model pathogens, like Friend Virus Complex, will lead to better interpretations of the results of laboratory experiments by framing them in an ecological context. Future studies with semi-natural host-pathogen systems promise to bridge the gap between laboratory and field studies and shed light on the complex interactions of sociality and disease ecology. Characterizations of the transmission dynamics of various pathogens under natural conditions will provide insight into better combating emerging infectious disease, and established pathogens of wildlife and humans

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