The microbiome extends host evolutionary potential

Abstract

The microbiome shapes many host traits, yet the biology of microbiomes challenges traditional evolutionary models. Here, we illustrate how integrating the microbiome into quantitative genetics can help untangle complexities of host-microbiome evolution. We describe two general ways in which the microbiome may affect host evolutionary potential: by shifting the mean host phenotype and by changing the variance in host phenotype in the population. We synthesize the literature across diverse taxa and discuss how these scenarios could shape the host response to selection. We conclude by outlining key avenues of research to improve our understanding of the complex interplay between hosts and microbiomes.

Fig. 1. Microbial influence on host phenotypic variation.

The microbiome encodes many more genes than the host genome alone. Interactions with variation in the microbiome may alter the host genotype-phenotype map, shaping host phenotypic variance within populations. A First, some host phenotypes will not be affected by the microbiome (visualized in gray) and it is worth noting that not all microbes will influence host phenotypes. B The microbiome may shift the mean host phenotypes. The blue distribution is suggestive of when hosts leverage locally adaptive microbiomes to match local selective pressures. C Alternatively, the microbiome may also alter phenotypic variance (conceptualized in purple). D Finally, both the phenotypic mean and variance may be affected by the microbiome (in green). We note here that these scenarios are not mutually exclusive. Expanding host phenotypic variation through the microbiome may allow hosts to explore novel regions of fitness landscapes. These are conceptualized phenotypic distributions, and more experimental work is necessary to confirm how the microbiome affects host phenotypic distributions.

Fig. 2. Microbiome responds to host experimental evolution.

Experimental evolution is a powerful tool to understand the genetic basis of adaptation. A Hypothesized schematic of the microbial response during adaptation in flies. B Microbial diversity is frequently reduced in evolved populations during experimental evolution in flies. Data is reproduced from Henry & Ayroles. Here, each point represents Shannon diversity of metagenomes from a pool of sequenced flies. Asterisks denote the experiments where microbial diversity is significantly different between control and evolved populations.

Fig. 3. Partitioning microbial effects on host adaptation.

Experimental approaches developed for variance partitioning in quantitative genetics can be a powerful way to assess the influence of the microbiome on host evolution. A Experimental evolution will provide critical insights into how hosts and microbiomes respond to stressful environments. By including the microbiome (visualized as different colored circles) in experimental evolution, then genetic responses in both host and microbiome can be measured following selection. At the end of experimental evolution, we expect both host and microbiome to adapt - visualized as blue fly and blue/purple microbes. Microbial evolution may occur at the strain level (e.g., when beneficial mutations in particular genes drive adaptation to the novel selective pressure). Alternatively, selection may increase the frequency of a particular microbial taxon, leading to loss of microbial taxa in the adapted microbiome. To test how the microbiome interacts with the host genome to influence host phenotypes, one can perform fully factorial, reciprocal transplants between host, microbiome, and environment. B Key insights will be gained from examining the evolutionary trajectory of alleles that emerge or change in frequency during experimental evolution. C To test how microbial variation influences host phenotype, hosts can be inoculated with different levels of microbial variation. Removing the microbiome through antibiotics (or other manipulations) will show how hosts respond to perturbation to their microbiomes. D Finally, diallel crosses can be used to show how host and microbial genetic variation interact. Diallel crosses are performed by crossing all possible combinations between inbred lines to each other in a common environment (represented by fly colors). Rearing F1s in different microbial environments will enable partitioning of the additive and nonlinear, epistatic components between host and microbial genetic variation.