Rethinking “mutualism” in diverse host‐symbiont communities

Abstract

While examples of bacteria benefiting eukaryotes are increasingly documented, studies examining effects of eukaryote hosts on microbial fitness are rare. Beneficial bacteria are often called "mutualistic" even if mutual reciprocity of benefits has not been demonstrated and despite the plausibility of other explanations for these microbes' beneficial effects on host fitness. Furthermore, beneficial bacteria often occur in diverse communities, making mutualism both empirically and conceptually difficult to demonstrate. We suggest reserving the terms "mutualism" and "parasitism" for pairwise interactions where the relationship is largely independent of other species and can be verified by measuring the fitness effect experienced by both partners. In hosts with diverse microbial communities, we propose re-formulating some of the essential questions of symbiosis research - e.g. concerning specificity, transmission mode, and common evolutionary fates - as questions of community ecology and ecosystem function, allowing important biological interactions to be investigated without making assumptions about reciprocity. Understanding the fitness of host-associated bacteria is a crucial component of investigations into the role of microbes in eukaryote evolution.

Invasions of Host-Associated Microbiome Networks

“…Overall, then, we do not have the full picture of this commensal-pathogenic continuum. As such, we echo the suggestion by Mushegian and Ebert (2016) that the term "mutualism" be used more sparingly, i.e. only when there is a clear pairwise interaction or when mutual reciprocity has been directly investigated and demonstrated.…”

Holobionts and the ecology of organisms: Multi-species communities or integrated individuals?

“…Such processes can lead to interdependent communities without requiring selection or functional integration at the holobiont level (Sachs and Hollowell 2012;Douglas and Werren 2016). Mushegian and Ebert (2016) give plausible examples that include protective symbioses based on secondary metabolic functions, such as detoxification of heavy metals or plant toxins, or production of defensive compounds against other microbes, which are likely to be beneficial regardless of whether the microbe is in a host or non-host environment. Perhaps a more compelling example of the independence of metabolic dependency and functional integration is the mammalian gut.…”

“…No, because ecological communities can have reproducible dynamics and predictable outcomes for their members without being the result of selection, integration or coevolution at the level of the community (Mushegian and Ebert 2016). Something further is needed to bind individuals into a whole.…”

The evolution of the host microbiome as an ecosystem on a leash

“…Interactions between hosts and their microbiota appear to include many examples of biological mutualism: interactions that provide fitness benefits to all the species involved 18 . However, a degree of caution is required; although benefits to the host have been well documented, it is difficult to show that microbes benefit, because we typically do not know if better alternatives exist for microbes outside of the host 19 . If microbes do not benefit, the prediction is that natural selection will favour strategies to escape from the microbiome, or adaptions that increase within-host fitness, even if this harms the host.…”