Evolving as a holobiont
Venue: PLoS biology

Some of the most exciting recent advances in biology have been in our understanding of how the microbiome—the community of bacteria, fungi, and other single-celled microorganisms— influences host functions and behaviors. From the way we eat, to the way we think, to our susceptibility to diseases (just to name a few), the microbiome has a huge impact on human physiology. But microbiomes aren’t just for humans, or even just for mammals. The composition and function of microbiomes are critical for most animals and plants, so much so that many scientists believe that hosts and their microbiomes should be considered as single ecological unit—the holobiont. Given their ubiquity and importance, researchers are now investigating how this symbiotic relationship between hosts and microbes has evolved over time. In a paper recently published in PLOS Biology, the authors investigate whether the composition of a microbiome changes in parallel with the evolution of its host species . To do this, they characterized the microbiota of 24 carefully reared animal species from four different groups (Peromyscus deer mice, Drosophila flies, Anopheles/Aedes/Culex mosquitoes, and Nasonia wasps), and they also re-analyzed data from seven species of wild hominid. By comparing the composition of the microbiomes to how closelyor distantly-related these 24 species are, they determined that the more closely-related two host species are evolutionarily, the more similar their microbiota, and inversely, the more distantly-related, the more distinct . Thus, the microbiome isn’t a random assembly of microbes derived from the environment, but rather there has been a selection on maintaining specific host–microbiota interactions over time. The authors term this relationship between the microbiome and host evolution “phylosymbiosis”. To test this, they performed interspecific microbiome transplants in both mice and wasp species, and found that the microbiome of even closely related species was less functional than the endogenous microbiome, indicating that each host is ideally suited for its own microbiome. To further understand the process of phylosymbiosis, researchers can mimic it in the lab via artificial selection. In work published in the journal Frontiers in Microbiology, researchers performed a 15-generation selection experiment on bank voles (Myodes glareolus) and found that voles bred for the ability to maintain body mass on a high-fiber, herbivorous diet had a distinct microbiome compared to control lines . Similarly, chickens bred for either high weight or low weight (while maintaining the same diet and husbandry) have altered gut microbiota; in a PLOS ONE study, researchers characterized the composition of the microbiome of chickens that had been bred for>50 generations for these specific phenotypes . They identified families of bacteria that were moderately heritable, and found that some interactions among gut microbiota members are mediated by the host genes. These studies demonstrate that the make-up of the microbiome is not dictated solely by diet and environment, but that rather it changes in conjunction with the demands of the host. One important technique needed to understand holobionts is a computational framework for modeling host-microbiota interactions.