Why do hosts malfunction without microbes? Missing benefits versus evolutionary addiction

• Published in: Trends in microbiology (Regular ed.) 2024-02, Vol.32 (2), p.132-141
• Main Author: Hammer, Tobin J.
• Format: Article
• Language: English
• Subjects: Biological Evolution; evolved dependence; Host Microbial Interactions; host–microbe interactions; microbiome; Microbiota; mutualism; Symbiosis
• ISSN: 0966-842X; 1878-4380
• DOI: 10.1016/j.tim.2023.07.012

A large and increasing body of evidence has demonstrated that hosts often need microbial symbionts to perform essential functions.Deficiencies of microbe-free hosts are usually attributed to the lack of microbial benefits, but the field has neglected evolutionary addiction, where dependencies evolve without benefits.Evolutionary addiction is a general process that could operate in any host system evolving in the continual presence of symbionts, from the human gut to plant roots to microbial hosts of other microbes.Evolutionary addiction helps explain the broad extent to which microbes impact host biology. Microbes are widely recognized to be vital to host health. This new consensus rests, in part, on experiments showing how hosts malfunction when microbes are removed. More and more microbial dependencies are being discovered, even in fundamental processes such as development, immunity, physiology, and behavior. But why do they exist? The default explanation is that microbes are beneficial; when hosts lose microbes, they also lose benefits. Here I call attention to evolutionary addiction, whereby a host trait evolves a need for microbes without having been improved by them. Evolutionary addiction should be considered when interpreting microbe-removal experiments, as it is a distinct and potentially common process. Further, it may have unique implications for the evolution and stability of host–microbe interactions. Microbes are widely recognized to be vital to host health. This new consensus rests, in part, on experiments showing how hosts malfunction when microbes are removed. More and more microbial dependencies are being discovered, even in fundamental processes such as development, immunity, physiology, and behavior. But why do they exist? The default explanation is that microbes are beneficial; when hosts lose microbes, they also lose benefits. Here I call attention to evolutionary addiction, whereby a host trait evolves a need for microbes without having been improved by them. Evolutionary addiction should be considered when interpreting microbe-removal experiments, as it is a distinct and potentially common process. Further, it may have unique implications for the evolution and stability of host–microbe interactions.