Pathogen resistance may be the principal evolutionary advantage provided by the microbiome

Abstract

To survive, plants and animals must continually defend against pathogenic microbes that would invade and disrupt their tissues. Yet they do not attempt to extirpate all microbes. Instead, they tolerate and even encourage the growth of commensal microbes, which compete with pathogens for resources and via direct inhibition. We argue that hosts have evolved to cooperate with commensals in order to enhance the pathogen resistance this competition provides. We briefly describe competition between commensals and pathogens within the host, consider how natural selection might favour hosts that tilt this competition in favour of commensals, and describe examples of extant host traits that may serve this purpose. Finally, we consider ways that this cooperative immunity may have facilitated the adaptive evolution of non-pathogen-related host traits. On the basis of these observations, we argue that pathogen resistance vies with other commensal-provided benefits for being the principal evolutionary advantage provided by the microbiome to host lineages across the tree of life. This article is part of the theme issue 'The role of the microbiome in host evolution'.

Keywords: colonization resistance; commensal bacteria; defensive symbionts; evolution of immunity; host–microbiome interactions; microbiome.

Figure 1.

Competition between commensal and pathogenic microbes affects the survival and evolution of their hosts. (a,b) All plants and animals encounter pathogenic microbes (pictured here as red flagellated bacilli), which seek to damage the host’s epithelial and other protective tissues in order to extract the nutrients within, and commensal microbes (yellow non-flagellated bacilli), which can live on hosts while causing minimal damage. Commensals restrict the nutrients (orange hexagons) and physical access to vulnerable host tissues available to pathogens and also directly harm pathogens with secretion systems and other microbial weapons. (c,d) Under strong pathogen pressure, hosts that acquire and maintain commensal microbiomes that are more effective at resisting a broad range of pathogens will tend to survive and leave more offspring than their competitors.

Figure 2.

A conceptual model of selection for cooperative immunity. Hosts encounter random pathogens with varied innate infectivities, which we represent by a distribution of exponential growth rate across pathogens. Encountered pathogens with positive growth rates successfully infect the host and those with negative growth rates are resisted. Host fitness increases when the fraction of unresisted pathogen encounters (dark red area under the curve) is reduced. Each row illustrates a different host defence strategy, illustrated by the arrow diagrams, in which red arrows denote direct harm and blue arrows denote direct help between host (H), commensal (C) and pathogen (P). Grey arrows indicate the shift in the peak of the distribution of pathogen growth rates from baseline caused by the given strategy. Row 1: As a baseline, we consider a host that is colonized by commensals that compete with its pathogens. Row 2: A host strategy that harms commensals and pathogens equally reduces the competition experienced by pathogens and so has a limited net impact on pathogen growth rates. Row 3: Selectively harming pathogens maintains competition from commensals and so provides a greater reduction in pathogen growth rates than harming all microbes. Row 4: Additionally helping commensals increases the competition from commensals and thus further decreases pathogen growth rates. The host may also have a fixed set of baseline antimicrobial defences common to all strategies, which we do not represent in the arrow diagrams.