Roles of the gut microbiota in the adaptive evolution of mammalian species

Abstract

Every mammalian species harbours a gut microbiota, and variation in the gut microbiota within mammalian species can have profound effects on host phenotypes. In this review, we summarize recent evidence that gut microbiotas have influenced the course of mammalian adaptation and diversification. Associations with gut microbiotas have: (i) promoted the diversification of mammalian species by enabling dietary transitions onto difficult-to-digest carbon sources and toxic food items; (ii) shaped the evolution of adaptive phenotypic plasticity in mammalian species through the amplification of signals from the external environment and from postnatal developmental processes; and (iii) generated selection for host mechanisms, including innate and adaptive immune mechanisms, to control the gut microbiota for the benefit of host fitness. The stability of specific gut microbiotas within host species lineages varies substantially across the mammalian phylogeny, and this variation may alter the ultimate evolutionary outcomes of relationships with gut microbiotas in different mammalian clades. In some mammalian species, including humans, relationships with host species-specific gut microbiotas appear to have led to the evolution of host dependence on the gut microbiota for certain functions. These studies implicate the gut microbiota as a significant environmental factor and selective agent shaping the adaptive evolution of mammalian diet, phenotypic plasticity, gastrointestinal morphology and immunity. This article is part of the theme issue 'The role of the microbiome in host evolution'.

Keywords: holobiont; host–microbe interactions; metagenome; microbiome; population genetics.

Figure 1.

Dietary niche expansions mediated by the gut microbiota. The presence of a gut microbiota during mammalian evolution has had profound effects on mammalian dietary diversification. As herbivory has evolved multiple times independently throughout mammalian evolution, distantly related mammalian lineages have converged on gut microbiota compositions required for digesting complex plant polysaccharides (left). Dietary specialization on plants that produce toxic secondary metabolites, such as koala specialization on eucalyptus and woodrat specialization on creosote, has probably been facilitated by gut microbiota plasticity (centre). Gut microbiota-mediated metabolism of lactose in adulthood may have potentiated the recent evolution of lactase persistence phenotype in some human populations (right).

Figure 2.

Gut microbes as potentiators of host dietary shifts. Graphs depict fitness surfaces, or the fitness outcomes of hosts (vertical axis) as a function of variation in a host phenotype value (horizontal axis), in this case, the degree of milk consumption as an adult. Presume that acquisition and consumption of milk has increasing fitness costs to the host, and fitness rewards that plateau at a certain point. Presume also that ability to digest lactose, either through secretion of endogenous host enzymes or via Bifidobacterium, increases the point at which that fitness reward plateaus. In a background population without adult production of lactase (LCT_wt allele; (a)), a change in phenotype that increased milk acquisition and consumption (P_low → P_high) might lead to a fitness decrease in the absence of Bifidobacterium in the gut, but a fitness increase in its presence. After fixation of the lactase-production allele (LCT_mut) in the population (b), the host may no longer be sensitive to the presence of the lactose-degrading bacterium in the gut. In this way, the evolution of the host diet could be potentiated by gut bacteria, even without ultimately depending on the bacteria.

Figure 3.

The gut microbiota as an amplifier of environmental signals for adaptive phenotypic plasticity in mammals. (a) An environmental gradient (coloured triangle) affects hosts (mouse cartoons), which in turn affects the gut microbiota (coloured circles). The shifts in the microbiota induced by host responses to the environmental gradient feed back to further affect host responses. (b) The combined direct and microbiota-mediated effects of the environmental gradient in (a) generate a host reaction norm (dashed line) that closely matches the fitness optimal reaction norm (solid line). (c) An environmental gradient (coloured triangle) affects hosts (mouse cartoons) and their microbiota (coloured circles), but the host does not respond to the shifts in the microbiota. (d) Under this scenario, the slope of the host reaction norm (dashed line) is less than the fitness optimal reaction norm (solid line). By serving as a signal amplification mechanism in this way, the microbiota could speed up adaptation during host transition to a new environmental gradient by allowing natural selection to act on host genetic variation in both direct and microbiota-mediated host phenotypic responses to the environmental gradient, rather than on direct host phenotypic responses alone. Alternatively, hosts may come to rely on the microbiota as a signal amplification mechanism through neutral processes, even if the host has previously evolved the optimal reaction norm through direct responses to the environmental gradient alone. Specifically, genetic drift may lead to the replacement of host direct responses to the environmental gradient by host responses to shifts in the microbiota caused by the gradient.

Figure 4.

Potential pathways towards evolutionary dependence on a specific gut microbiota. Initial variation in gut microbiota composition within a species, denoted by coloured capsules (a), may generate differential fitness of lineages within the species in the presence of different food resources, denoted by coloured moths and acorns (b). Selection to retain ecological benefits of microbial associations may lead to the evolution of adaptive host mechanisms designed to maintain specific microbiotas, denoted by matching colours of host outlines and capsules (c). As the associations persist over evolutionary time, postnatal developmental processes may evolve to integrate signals from the specific microbiotas (d). Alternatively, host-lineage specific gut microbiotas can be evolutionarily integrated into host development even if the gut microbiotas have no effect on host fitness originally (e,f). Both pathways (a–d) and (a,e,f) can lead to deleterious effects on hosts if the symbiotic associations are disrupted.