Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts

The advent of relatively inexpensive tools for characterizing microbial communities has led to an explosion of research exploring the diversity, ecology, and evolution of microbe-host systems. Some now question whether existing conceptual frameworks are adequate to explain microbe-host systems. One popular paradigm is the "holobiont-hologenome," which argues that a host and its microbiome evolve as a single cooperative unit of selection (i.e., a superorganism). We argue that the hologenome is based on overly restrictive assumptions which render it an approach of little research utility. A host plus its microbiome is more effectively viewed as an ecological community of organisms that encompasses a broad range of interactions (parasitic to mutualistic), patterns of transmission (horizontal to vertical), and levels of fidelity among partners. The hologenome requires high partner fidelity if it is to evolve as a unit. However, even when this is achieved by particular host-microbe pairs, it is unlikely to hold for the entire host microbiome, and therefore the community is unlikely to evolve as a hologenome. Both mutualistic and antagonistic (fitness conflict) evolution can occur among constituent members of the community, not just adaptations at the "hologenome" level, and there is abundant empirical evidence for such divergence of selective interests among members of host-microbiome communities. We believe that the concepts and methods of ecology, genetics, and evolutionary biology will continue to provide a well-grounded intellectual framework for researching host-microbiome communities, without recourse to the limiting assumption that selection acts predominantly at the holobiont level.