Modeling the effects of phenological mismatch in tick questing and host demographic turnover on Lyme disease hazard

Climate change is altering the seasonal abundance and activity patterns of ecologically interacting species. It is not yet known how changes in phenological alignment between ticks and their hosts will impact tick feeding, survival, and the timing and probability of pathogen transmission during feeding. It has been observed that the seasonal timing of human Lyme disease cases has shifted earlier, accompanying an increased incidence, which may reflect changes in tick questing phenology. We present a mathematical model framework for exploring the seasonal dynamics of a tick-borne pathogen. The model extends a recently developed seasonal population matrix model for ixodid ticks feeding on a small and a large host, to i) incorporate the transmission of a pathogen, based on the causative agent of Lyme disease, Borrelia burgdorferi sensu lato, between ticks and a reservoir-competent small mammal host, and ii) include seasonal demographic turnover in the small mammal host. Through modification of model parameters, we explored the effects of alternative scenarios for tick questing phenology, tick host selection, and seasonality of host reproduction on disease dynamics. Our model predicts that due to differences in their life history, seasonal infection prevalence is much more variable in the small mammalian host than in the tick vector. The rapid pace of host demographic turnover is important for clearing infection in the small mammal population. The alignment between the seasonal timing of host reproduction and tick questing phenology is a critical feature in the model, as it determines pathogen transmission and infection prevalence in host and vector populations. The model predicts that increased asynchrony between larval tick feeding and small host reproduction can increase the number of infected questing nymphs, a common metric for Lyme disease hazard. When larval tick feeding is misaligned with small host reproduction, the larvae feed predominantly on older hosts, which are more likely to be infected. Our model presents an adaptable framework for exploring seasonal relationships between pathogen dynamics, host demography, and vector life history traits in an emergent tick-borne disease system.