Evolution of Microbiota–Host Associations: The Microbe’s Perspective

Microbiota–host associations are ubiquitous in nature. They are often studied using a host-centered view, while microbes are assumed to have coevolved with hosts or colonize hosts as nonadapted entities. Both assumptions are often incorrect. Instead, many host-associated microbes are adapted to a biphasic life cycle in which they alternate between noncoadapted hosts and a free-living phase. Full appreciation of microbiota–host symbiosis thus needs to consider how microbes optimize fitness across this life cycle. Here, we evaluate the key stages of the biphasic life cycle and propose a new conceptual framework for microbiota–host interactions which includes an integrative measure of microbial fitness, related to the parasite fitness parameter R0, and which will help in-depth assessment of the evolution of these widespread associations. A microbial perspective is needed for a full understanding of microbiota–host symbiosis.A biphasic life cycle likely shapes the origin of a microbe’s association with the host.Microbes must thus succeed in the host, the environment, and reciprocal transmission.Symbiosis is driven by microbial fitness integrated across the entire life cycle.A new formalized integrative fitness measure can guide novel research on symbiosis.