Persistent phylogeographic structure of an emerging virus on a homogeneous landscape

Landscape composition and structure influence animal movement, which in turn can affect transmission of their diseases. Spatio-temporal variation in host diffusion, caused by landscape heterogeneity, is thus expected to generate corresponding phylogeographic patterns in the pathogen. However, establishing causative links between genetic structure in pathogen populations and environmental variation does require appropriate null models. Here, we present an empirical example of the emergence and multi-decade persistence of phylogeographic structure on a homogeneous landscape in a rapidly diversifying pathogen in the absence of any apparent landscape heterogeneity. By applying phylogeographic inference to 173 sequences of a raccoon-specific strain of rabies virus, we reconstruct patterns of the virus’ evolution and diffusion on the Florida peninsula, USA, from its first emergence in the 1940’s to the present. Consistent with a lack of significant landscape heterogeneity relevant to raccoon movement in Florida, we found that the speed of rabies virus diffusion was spatially homogeneous across the peninsula. In contrast, we document the emergence of strong phylogeographic structure in the virus, in the form of five monophyletic lineages that diverged during the early years of colonization and now each occupy a distinct sub-region of Florida. Based on samples taken over multiple decades, we show that the spatial distribution of these lineages has changed little over the past four decades. This phylogeographic stability allowed us to retrospectively identify a small set of counties within Florida as the likely source of the virus strain that seeded a much larger rabies outbreak in the northeastern USA in the 1970s. Our results provide a rare empirical demonstration that spatial genetic structure can arise and be maintained in the absence of landscape heterogeneity, which has wider implications for the interpretation of phylogeographic data and the reconstruction of historical colonization patterns from molecular data.