Host-pathogen-vector continuum in a changing landscape: Drivers of Bartonella prevalence and evidence of historic spillover in a multi-host community

Abstract

Small mammals and their ectoparasites present a unique system to investigate the eco-epidemiology of multi-host vector-borne pathogens and identify specific bacterial spillover determinants. We applied ecological and evolutionary analyses in a rainforest-human-use mosaic to investigate Bartonella spp. across small mammal and ectoparasite communities. We observed substantial overlap among small mammal communities in different habitat types, predominantly driven by habitat generalists. Most ectoparasites were generalists, infecting multiple hosts. We observed high Bartonella prevalence at both study sites -a forest-plantation mosaic (47.4%) and a protected area (28.8%). Seven of the ten ectoparasite species sampled were also positive for Bartonella, following prevalence trends in their hosts. A generalised linear model revealed an independent association between aggregated ectoparasite load in hosts and Bartonella prevalence, implicating ectoparasites in transmission. Bartonella lineages from small mammals were host-specific, while ectoparasites carried Bartonella associated with other small mammal hosts, indicating the potential for cross-species transmission. Phylogenetic ancestral trait reconstruction of Bartonella haplotypes suggest historic spillover events in the small mammal community, validating the potential for contemporary spillover events. These results highlight the necessity to disentangle the complex relationship between hosts, ectoparasites, and pathogens to understand the zoonotic implications of undetected spillover events in such multi-host communities.