The holobiont is not a useful model for most host-microbiome interactions

Gavin M Douglas , S. Andrew Inkpen

The holobiont concept refers to a host and associated microbes. It has been critiqued over the last decade, primarily based on the argument that individual holobionts are not an appropriate level for analyzing multi-generation host dynamics, as most microbes are acquired from the environment. Several responses were given to this and other criticisms. The main response has been that the holobiont concept, even from its initial conception, allows for a more holistic, and realistic, model of host biology. This is regardless of one’s evolutionary concerns, since hosts are always in association with microbes and phenotypes change in response to these associations. Taken further, it has been argued that allele frequencies shifting across host populations and microbes shifting in composition across hosts exist on the same conceptual continuum. We highlight that this analogy equally applies to entire communities of macro-organisms, and that there is no principled reason to privilege hosts and microbiota specifically as a holobiont. We also highlight the conceptual confusion surrounding host genetic variance when the holobiont concept is employed, and how this relates to the “missing heritability” debate. More generally, we discuss the social and practical impacts of this model, particularly in terms of its implicature and how it relies on interest-relativity. We argue that while biological categories are often fuzzy, we should strive for categories that are both informative and unambiguous. An individual host represents such a category, while a holobiont does not.