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.