Tick Microbiomes in Neotropical Forest Fragments Are Best Explained by Tick-Associated and Environmental Factors Rather Than Host Blood Source

ABSTRACT

The composition of tick microbiomes varies both within and among tick species. Whether this variation is intrinsic (related to tick characteristics), or extrinsic (related to vertebrate host and habitat) is poorly understood but important, as microbiota can influence the reproductive success and vector competence of ticks. We aimed to uncover what intrinsic and extrinsic factors best explain the microbial composition and taxon richness of 11 species of Neotropical ticks, collected from eight species of small mammals in 18 forest fragments across central Panama. Microbial richness varied among tick species, life stages, and collection sites, but was not related to host blood source. Microbiome composition was best explained by tick life stage, with bacterial assemblages of larvae being a subset of those of nymphs. Collection site explained most of the bacterial taxa with differential abundance across intrinsic and extrinsic factors. Francisella and Rickettsia were highly prevalent, but their proportional abundance differed greatly among tick species and we found both positive and negative co-occurrence between members of these two genera. Other tick endosymbionts (e.g. Coxiella, Rickettsiella) were associated with specific tick species. In addition, we detected Anaplasma and Bartonella in several tick species. Our results indicate that the microbial composition and richness of Neotropical ticks are principally related to intrinsic factors (tick species, life stage) and collection site. Taken together, our analysis informs how tick microbiomes are structured and can help anchor our understanding of tick microbiomes from tropical environments more broadly.

Importance: Blood feeding insect microbiomes often play important roles in disease transmission, yet the factors that structure tick microbial communities in the Neotropics are unknown. Utilizing ticks collected from live animals in Neotropical Forest Fragments, this study teases apart the contributions of intrinsic and extrinsic tick-associated factors on tick microbial composition, as well as which specific microbes contribute to differences across tick species, tick lifestages, mammals they fed on, and the locations from where they were sampled. Furthermore, this study provides revelations of how notable tick-associated bacterial genera are interacting with other tick-associated microbes, as well as and the forest animals they encounter.