OF GERMS AND BUGS: ECOLOGICAL AND GENETIC APPROACHES TO DISENTANGLING SYMBIOSES IN A HONEY BEE PARASITE SYSTEM

Abstract

Complex communities of microorganisms reside within and impact the health of their hosts along a dynamic continuum of interactions that fall under the blanket term symbiosis. Host-microbe associations are a fundamental feature of animal life, where they shape digestion, development, immunity, reproduction, and behavior—but nowhere is this more apparent than in the relationship between hosts, their resident microbiota, and the parasites and pathogens that share the same ecological niche. These relationships are likely to shift over time and are the product of complex interactions between hosts, symbionts, and the environments that they inhabit, yet we have done little to characterize these relationships in the context of the ecological factors that drive them. Of these ecological factors, temperature is one of the most influential—often altering immunity, metabolism, and parasite replication rates. Utilizing the well-characterized and highly conserved core gut symbionts found in honey bees (Apis mellifera), and their niche-sharing trypanosomatid gut parasite, Lotmaria passim, I leveraged both cell cultures and a gnotobiotic infection model to assess the potential for temperature to shape parasite-symbiont interactions. In vitro, I found that symbionts demonstrated greater heat tolerance than parasites and reduced parasite growth in a temperature-dependent, acidity-driven manner, and in vivo, these protective effects held true. Building from this work, I integrated U.S. honey bee disease survey data in a multi-year analysis, confirming that even across vast spatiotemporal scales, temperature—alongside the influence of co-occurring pests and pathogens—is likely an integral driver of parasite distributions. Lastly, I describe the updated reference genome for Lotmaria passim, which reveals this parasite’s unique chromosome-level plasticity, thereby generating an invaluable resource for future work in this system. Together, these results integrate ecology, epidemiology, genomics, and controlled infection assays to assess the drivers of microbiome-mediated resistance to infection across a vast, seldomly achievable range of spatial scales. I demonstrate that temperature is an integral aspect of host-symbiont-parasite interactions—underscoring the importance of considering ecological drivers of infection in diverse, cross-phyla systems.