Abstract
The trillions of microbes living in the gut—the gut microbiota—play an important role in human biology and disease. While much has been done to explore its diversity, a full understanding of our microbiomes demands an evolutionary perspective. In this review, we compare microbiomes from human populations, placing them in the context of microbes from humanity’s near and distant animal relatives. We discuss potential mechanisms to generate host-specific microbiome configurations and the consequences of disrupting those configurations. Finally, we propose that this broader phylogenetic perspective is useful for understanding the mechanisms underlying human–microbiome interactions.
The microbiome in the context of evolution
We are in the midst of a revolution in our understanding of the human microbiome (Box 1). A decade ago, very little was known of the inventory of microbes that inhabit different parts of the human body, how they assemble into communities of varying levels of complexity, and how they relate to microbiomes in other species. Recent improvements in technology for collecting and analyzing DNA sequence data make these questions accessible for the first time. Various aspects of the microbiome have been correlated to a surprising number of human diseases [1], and some microbiome-centric interventions have shown extraordinary efficacy in treatment of specific disorders like recurrent Clostridium difficile infection [2]. More broadly, this wealth of additional data has drawn attention to the connections between microbes and foundational elements of organismal biology and ecology [3]. Given the rush to apply knowledge of the human microbiome in fields ranging from medicine to forensics, there has been a heavy emphasis on practical applications of microbiome sequencing, largely from North American and European populations. However, as in many other areas of biology, a true understanding of these patterns and processes requires an evolutionary perspective.
In this review, we focus on the gut microbiome, as surprisingly little comparative data are available for other body sites across human populations or other species. We place the human gut microbiome into its evolutionary context across different modern populations with varying diets, lifestyles, and environmental exposures, and relate evolutionary patterns in the gut microbiome across the mammals to address several key questions. How do human microbiomes compare with our evolutionary ancestors? Are those patterns consistent with a common assumption that the microbiome evolves with the host? If so, what exactly is evolving in a microbiome and how? Does evolutionary history in the microbiome matter to human health and fitness? If so, how can we use evolutionary history to better understand the assembly and effects of the microbiome to the benefit of human health?
To address these questions, we first describe the human gut microbiome and its contents. We then place this information in the context of our closest relatives, the primates, and more distant relatives, mammals. Then we discuss the consequences of modifying species-specific microbiomes, and some of the mechanisms underlying this process. Finally, we point the way to microbiome studies that can better take into account the evolutionary properties of hosts, microbes, and their symbioses to improve our knowledge both of the underlying biology and for practical applications in human and animal health.
Global diversity of the human microbiome