Getting the hologenome concept right: An eco-evolutionary framework for hosts and their microbiomes

Over the past couple of years, there has been numerous discussion pro and against the significance of the concepts of holobionts and hologenomes. It states that all organisms, including humans, plants, corals or even parasites, may be associated with microbes (bacteria, viruses, fungi, protists etc.) that participates in the phenotype of their host. The community of biologists and philosophers recognizing the importance of considering the role of holobionts at the ecological and evolutionary level is rapidly growing. In most cases, it appears that the arguments against it result from of a misunderstanding of the definitions and constructs that constitute the basic of this concept and resulting theories. Recently, some of us have attempted to clarify some recent misconceptions in order to allow more constructive discussion on the significance of this underestimated level of biological organization.

The preprint is available on bioRxiv http://biorxiv.org/content/early/2016/02/02/038596.article-metrics

Abstract

Given the recently appreciated complexity of symbioses among hosts and their microbes, significant rethinking in biology is occurring today. Scientists and philosophers are asking questions at new biological levels of hierarchical organization – What is a holobiont and hologenome? When should this vocabulary and associated concepts apply? Are these points of view a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Legitimate questions, advancements and revisions are warranted at this nascent stage of the field. However, a productive and meaningful discourse can only commence when skeptics and proponents alike use the same definitions and constructs. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not necessarily the primary unit of selection is not synonymous with arguing that it is not a unit of selection in general. Here, we succinctly deconstruct and clarify these recent misconceptions. Holobionts (hosts and their microbes) and hologenomes (all genomes of the holobiont) are multipartite entities that result from ecological, evolutionary and genetic processes. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome. We invite the community to consider these new perspectives in biology.