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We propose a general barrier theory as an evolutionary framework for understanding coevolutionary effects of conflicts of interest in natural and human systems. It is generalized from the barrier theory of cancer, which describes how cancer develops through the evasion of mechanisms, that block unregulated cellular reproduction and survival. Barriers are naturally evolved or artificially implemented mechanisms for blocking exploitation; restraints are mechanisms that impede but do not block exploitation. When conflicts of interest arise, selection will favor exploiters that are capable of overcoming barriers and restraints. When barriers are in place, they halt, at least temporarily, coevolutionary arms races (the Red Queen can stop running). Barriers occur in a broad spectrum of interactions characterized by conflicts of interest: barriers to cellular survival (apoptosis) and reproduction (cell cycle arrest) may block a virus from replicating its genome through reproduction of its host cell. Vaccines may completely protect against targeted pathogens. A plant may escape herbivory by evolving defensive chemicals that block herbivory. Obligate mutualisms may evolve when barriers to horizontal transmission favor symbionts that increasingly lose mechanisms that contribute to horizontal transmission. Here, we show how the barrier theory applies across a spectrum of natural and social systems.

The microbiome is composed of hundreds of interacting species that have co-evolved with the host and alterations in microbiome composition have been associated with health and disease. Insights from evolutionary ecology may aid efforts to ameliorate microbiome-associated diseases. One step toward this goal involves recognition that the idea of commensalism has been applied too broadly to human/microbe symbioses. Commensalism is most accurately viewed on a symbiosis continuum as a dividing line that separates a spectrum of mutualisms of decreasing positive interdependence from parasitisms of increasing severity. Insights into the evolution of the gut microbial symbiosis continuum will help distinguish between human actions that will advance or hinder health. Theory and research indicate that a major benefit of mutualistic microbes will be protection against pathogens. Mismatches between current and ancestral diets may disfavor mutualists, resulting in microbiome effects on health problems, including obesity, diabetes, autism, and childhood allergy. Evolutionary theory indicates that mutualisms will be favored when symbionts depend on resources that are not used by the host. These resources, which are referred to as human-inaccessible microbiota-accessible carbohydrates (HIMACs), can be supplied naturally through diet. Public health interventions need to consider the position of gut microbes on the mutualist-parasite continuum and the specific associations between prebiotics, such as HIMACs, and the mutualists they support. Otherwise interventions may fail to restore the match between human adaptations, diet, and microbiome function and may thereby fail to improve health and even inadvertently promote illness.