Host-Microbiome Interactions as Moderators of Host Quality and Biodiversity-Disease Relationships

Biodiversity-disease studies typically focus on how changes in community composition (e.g., species richness, abundance, and functional or phylogenetic metrics of biodiversity) affect disease risk. In doing so, these studies tend to overlook intraspecific variation in the organisms comprising the community. Yet, intraspecific variation, which occurs to varying degrees both within and between communities, could also modulate biodiversity-disease relationships. One important driver of intraspecific variation is the microbiome. By directly and indirectly influencing health and susceptibility to infection and disease, microbiomes are integral to organismal functioning. Thus, the microbiome plays a crucial role in host quality. We define host quality as an integration of host traits related to parasite exposure, establishment, growth, and infectivity, which ultimately shape parasite fitness. The microbiome can impact host quality via a variety of mechanisms including host size and developmental stage, immune function, reproduction, nutrient acquisition, and behavior. However, the potential for such microbiome-driven changes in host quality to trigger cascading effects on community-level processes, specifically by altering parasite transmission dynamics and community competence, has not been well explored. Here, we examine and illustrate a pathway by which the microbiome may influence variation in organismal biology (i.e., host quality) of hosts in communities. Furthermore, we consider how major anthropogenic drivers of microbiome shifts, such as climate change, pollution, land use change, and domestication, might influence this pathway and thereby alter outcomes. Future studies bridging microbiome and disease ecology research will provide opportunities to unify these concepts across scales and between the plant and animal domains. To date, most microbiome research has focused on humans, crops, and laboratory animals. However, to better understand the potential for knock-on ecological effects of microbiomes, more attention must be paid to the microbiomes of wild plants and animals. Ultimately, more experimental and theoretical data are needed to clarify how the microbiome impacts host quality and disease dynamics, as well as how anthropogenic factors continuously reshape these relationships.