Can the microbiome influence host evolutionary trajectories?

Abstract

The microbiome shapes many traits in hosts, but we still do not understand how it influences host evolution. To impact host evolution, the microbiome must be heritable and have phenotypic effects on the host. However, the complex inheritance and context-dependence of the microbiome challenges traditional models of organismal evolution. Here, we take a multifaceted approach to identify conditions in which the microbiome influences host evolutionary trajectories. We explore quantitative genetic models to highlight how microbial inheritance and phenotypic effects can modulate host evolutionary responses to selection. We synthesize the literature across diverse taxa to find common scenarios of microbiome driven host evolution. First, hosts may leverage locally adapted microbes, increasing survivorship in stressful environments. Second, microbial variation may increase host phenotypic variation, enabling exploration of novel fitness landscapes. We further illustrate these effects by performing a meta-analysis of artificial selection in Drosophila, finding that bacterial diversity also frequently responds to host selection. We conclude by outlining key avenues of research and experimental procedures to improve our understanding of the complex interplay between hosts and microbiomes. By synthesizing perspectives through multiple conceptual and analytical approaches, we show how microbiomes can influence the evolutionary trajectories of hosts.

Host evolutionary history and ecological context modulate the adaptive potential of the microbiome

“…First, our work contributes to the growing body of literature that environmentally acquired microbes are important in stressful environments. Stressful environments are predicted to increase the relative importance of mutualisms [26][27][28], though how often the microbiome behaves evolutionarily like a traditional mutualism remains contentious [4,5,72]. In plants, stress-adapted soil microbiomes improve germination and seedling survival in stressful environments [73,74], highlighting the importance of early life traits like we also observed for development.…”

“…Many have predicted that the microbiome could accelerate local adaptation in the host, facilitating phenotypic changes to buffer local stressors [6,[70][71][72]. If so, transplanting the locally adaptive microbiomes should confer adaptive phenotypes to naive individuals.…”

“…To shape adaptive potential, the microbiome must contribute to host phenotype, not unlike traditional (host) additive genetic variance [72]. For development, the microbiome conferred an adaptive phenotype--HS Acetobacter accelerated development similarly for both the naive C and adapted HS fly in the HS diet (Fig.…”

Disentangling the relative roles of vertical transmission, subsequent colonizations and diet on cockroach microbiome assembly

“…Although the relative roles of all potential factors shaping community structure will conceivably vary with hosts and diets, our findings suggest that environmental microbial sources have a stronger filtering effect on the microbiota composition than do diet, ecological relationships between early-life microbiota, or future gut colonizers. This, in turn, may lead to consistent microbial communities with host adaptations maximizing the extended phenotype that the microbiota provides (11,78), particularly if microbes spend most of their lives in host-associated environments and, in turn, can co-evolve with hosts (2).…”

“…These microbial symbionts facilitate a multitude of functions associated with host nutrient management, immunity and development (1,3), and ultimately impact host adaptation and diversification across environments and dietary niches (e.g., [4][5][6][7][8]. When hosts traits select for specific microbial functions, these can be considered the extended phenotype of the host (9)(10)(11)(12). Selection should optimally involve getting a microbiota that is both flexible (i.e., containing environment-specific strains that are likely to enable degradation of environment-specific nutrients and toxins) and consistent (i.e., similar under a defined set of circumstances) rather than subject to random fluctuations (3,(13)(14)(15).…”