The Hologenome Concept: Helpful or Hollow?

Abstract

With the increasing appreciation for the crucial roles that microbial symbionts play in the development and fitness of plant and animal hosts, there has been a recent push to interpret evolution through the lens of the "hologenome"--the collective genomic content of a host and its microbiome. But how symbionts evolve and, particularly, whether they undergo natural selection to benefit hosts are complex issues that are associated with several misconceptions about evolutionary processes in host-associated microbial communities. Microorganisms can have intimate, ancient, and/or mutualistic associations with hosts without having undergone natural selection to benefit hosts. Likewise, observing host-specific microbial community composition or greater community similarity among more closely related hosts does not imply that symbionts have coevolved with hosts, let alone that they have evolved for the benefit of the host. Although selection at the level of the symbiotic community, or hologenome, occurs in some cases, it should not be accepted as the null hypothesis for explaining features of host-symbiont associations.

Fig 1. Alternative evolutionary processes can result in related host species harboring similar symbiont communities.

Left panel: Individual symbiont lineages retain fidelity to evolving host lineages, through co-inheritance or other mechanisms, with some gain and loss of symbiont lineages over evolutionary time. Right panel: As host lineages evolve, they shift their selectivity of environmental microbes, which are not evolving in response and which may not even have been present during host diversification. In both cases, measures of community divergence will likely be smaller for more closely related hosts, but they reflect processes with very different implications for hologenome evolution. Image credit: Nancy Moran and Kim Hammond, University of Texas at Austin.