Multiscale ecological boundaries and microbial community coalescence in host-associated microbiota

Ecological boundaries between different environments are important for generating and maintaining biodiversity and for understanding community assembly. Classic examples include temperature gradients between upland and lowland habitats and estuaries (brackish) between fresh- and saltwater. While numerous studies have examined community assembly of free-living organisms across ecological boundaries, few studies have considered community assembly of host-associated (HA) organisms, including HA microbiota, across similar ecological boundaries. This is likely because it is unclear what constitutes an ecological boundary for organisms that reside on a host. We identify hybrid hosts (i.e., hosts derived from breeding events between two different genetic lineages) as ecological boundaries for HA organisms. More specifically, we argue that the intermediate genetic compositions of hybrid organisms, often accompanied by traits that are either intermediate to or else combinations of progenitor traits, create transition zones between the environments experienced by microbes on or in progenitor host lineages. This, in turn, paves the way for microbial community coalescence (i.e., mixing of microbial communities) that is directly analogous to community assembly in classic ecological boundaries. Further, because many hybrid hosts reside along ecological boundaries themselves, hybrid microbiota often experience simultaneous boundaries of both their hosts and their hosts' environment-an underexplored phenomenon that we term a "multiscale ecological boundary." By introducing ecological boundaries into HA microbiota literature, our goals are to further understanding of HA microbiota assembly and to propose a framework for studying the effects of ecological boundaries at multiple scales.IMPORTANCEBoundaries between environments provide important insight into how ecological communities are structured across broader landscapes. Of particular interest is how communities assemble within the transition zone constituting the boundary (i.e., where the transition in environmental variables occurs) and whether transitions in community composition parallel transitions in environmental variables. While ecological boundaries have a long history in classic ecology, similar concepts have recently emerged in microbiota literature. Currently, however, most studies of microbial ecological boundaries focus on environmental microbiota, rather than host-associated (HA) microbiota. This is likely because it is unclear what constitutes an ecological boundary in HA microbiota systems. We propose hybrid hosts as an HA analog for environmental ecological boundaries. Specifically, we outline how different types of hybrid hosts serve as models for different types of ecological boundaries. We then outline how the ecological boundary framework can be used to interpret HA microbial community coalescence (i.e., mixing) across host species. Finally, we suggest that many hybrid hosts reside within the transition zones of larger scale ecological boundaries. When this happens, hybrid hosts can be used to examine a novel phenomenon that we term a "multiscale ecological boundary."