The macroecology and evolution of avian competence for Borrelia burgdorferi

Aim: Predicting novel reservoirs of zoonotic pathogens would be improved by identifying inter-specific drivers of host competence, the ability to transmit pathogens to new hosts or vectors. Tick-borne pathogens can provide a useful model system, as larvae become infected only when feeding on a competent host during their first bloodmeal. For tick-borne diseases, competence has been best studied for Borrelia burgdorferi sensu lato (Bbsl), which causes Lyme borreliosis. Major reservoirs include several small mammal species, but birds may play an underrecognized role in human risk given their ability to disperse infected ticks across large spatial scales. Here, we provide a global synthesis of the ecological and evolutionary factors that determine the ability of bird species to infect larval ticks with Bbsl. Location: Global. Time period: 1983 to 2019. Major taxa studied: Birds. Methods: We compiled a dataset of Bbsl competence across 183 bird species and applied meta-analysis, phylogenetic factorization, and boosted regression trees to describe spatial and temporal patterns in competence, characterize its phylogenetic distribution across birds, reconstruct its evolution, and evaluate the trait profiles associated with competent avian species. Results: Half of sampled bird species show evidence of competence for Bbsl. Competence displays moderate phylogenetic signal, has evolved multiple times across bird species, and is pronounced in the genus Turdus. Trait-based analyses distinguished competent birds with 80% accuracy and show that such species have low baseline corticosterone, exist on both ends of the pace-of-life continuum, breed and winter at high latitudes, and have broad migratory movements into their breeding range. We use these trait profiles to predict various likely but unsampled competent species, including novel concentrations of avian reservoirs within the Neotropics. Main conclusion: Our results can generate new hypotheses for how birds contribute to the dynamics of tick-borne pathogens and help prioritize surveillance of likely but unsampled competent birds. Our findings further emphasize that birds display underrecognized variation in their contributions to enzootic cycles of Bbsl and the broader need to better consider competence in ecological and predictive studies of multi-host pathogens.