Host specificity, pathogen exposure, and superinfections impact the distribution of Anaplasma phagocytophilum genotypes in ticks, roe deer, and livestock in a fragmented agricultural landscape

Anaplasma phagocytophilum is a bacterial pathogen mainly transmitted by Ixodes ricinus ticks in Europe. It infects wild mammals, livestock, and, occasionally, humans. Roe deer are considered to be the major reservoir, but the genotypes they carry differ from those that are found in livestock and humans. Here, we investigated whether roe deer were the main source of the A. phagocytophilum genotypes circulating in questing I. ricinus nymphs in a fragmented agricultural landscape in France. First, we assessed pathogen prevalence in 1837 I. ricinus nymphs (sampled along georeferenced transects) and 79 roe deer. Prevalence was dramatically different between ticks and roe deer: 1.9% versus 76%, respectively. Second, using high-throughput amplicon sequencing, we characterized the diversity of the A. phagocytophilum genotypes found in 22 infected ticks and 60 infected roe deer; the aim was to determine the frequency of co-infections. Only 22.7% of infected ticks carried genotypes associated with roe deer. This finding fits with others suggesting that cattle density is the major factor explaining infected tick density. To explore epidemiological scenarios capable of explaining these patterns, we constructed compartmental models that focused on how A. phagocytophilum exposure and infection dynamics affected pathogen prevalence in roe deer. At the exposure levels predicted by the results of this study and the literature, the high prevalence in roe deer was only seen in the model in which superinfections could occur during all infection phases and when the probability of infection post exposure was above 0.43. We then interpreted these results from the perspective of livestock and human health.