Role of the Gut Microbiome in Vertebrate Evolution

Abstract

Darwin referred to life as a struggle. Organisms compete for limited resources in nature, and their traits influence the outcome. Victory carries great weight as winners survive, reproduce, and progenate subsequent generations. Consequently, organismal traits that influence fitness drive adaptation and their discovery clarifies evolution. Recent research implicates the vertebrate gut microbiome as an agent of fitness, selection, and evolution. Going forward, we must define the functional effects of the gut microbiome to determine how it impacts evolution. Specifically, we must quantify how gut microbiome function diversifies in concert with vertebrate radiation and resolve specific functions that influence natural selection. In so doing, we can discover and potentially capitalize upon the mechanisms by which our gut microbiomes impact our physiology and fitness. Ultimately, we may come to find that while life involves struggle, it also depends upon cooperation.

Keywords: coevolution; evolution; metabolome; metagenome; microbiome; vertebrates.

FIG 1

Conceptual illustrations of how microbiome function can be studied as an evolutionary trait. (A) Quantification of how gut microbiome functions (colored boxes) distribute across vertebrate species can reveal which functions manifest phylogenetic signal and are potential vertebrate evolutionary traits. (B) Population-level analyses of microbiome function can demonstrate how specific functions vary among individuals and associate with fitness. Microbiome functions that correlate with fitness can be further investigated to validate their contribution to host fitness and discover the demographic processes that impact their population-level distribution. (C) Observations of microbiome functions in extant lineages (boxed in blue) and neutral models of how microbiomes change throughout host evolution can theoretically predict ancestral microbiome functions (boxed in black). Moreover, neutral models can consider the distribution of microbiome functions among extant lineages to quantify rates of microbiome functional conservation and diversification and identify specific functions that putatively affect host fitness (e.g., deleterious effects from loss of conserved functions [boxed in red]). (D) Ultimately, studies must validate microbiome function fitness effects. Validation can come in many forms, including transplantation of microbiomes that encoded a fitness-associated function (purple ellipse) from wild individuals (black mice) into gnotobiotic animals (gray mice). Comparison of the physiological effects of transplantation across a donor population that varies in the abundance of the microbiome function (hashed purple ellipse) can provide additional insight.