The role of the microbiome in host evolution

Abstract

In the last decade, we have witnessed a major paradigm shift in the life sciences: the recognition that the microbiome, i.e. the set of microorganisms associated with healthy animals (including humans) and plants, plays a crucial role in the sustained health and fitness of its host. Enabled by rapid advances in sequencing technologies and analytical methods, substantial advances have been achieved in both identifying the microbial taxa and understanding the relationship between microbiome composition and host phenotype. These breakthroughs are leading to novel strategies for improved human and animal health, enhanced crop yield and nutritional quality, and the control of various pests and disease agents.

This article is part of the theme issue ‘The role of the microbiome in host evolution'.

1. Introduction

Increasingly, the research community is starting to ask different—and more difficult—questions about the fundamentals of host–microbiome interactions and their evolutionary consequences. This has brought into focus a major gap in our understanding: the role of the microbiome in host evolution. There is genuine confusion in the research community, including concerns that traditional evolutionary theory may be inadequate to explain evolutionary processes involving microbiomes, and uncertainty about the best choice of system and approach to investigate pattern and process from an evolutionary perspective. Opinions are diverse and often polarized.

Our goal for this theme issue is twofold: to provide an overview of the current status of the field for the researcher, teacher and student alike; and to spark new ideas and research, including much-needed interdisciplinary collaborations to solve the many outstanding problems. Our rationale is that an evolutionary perspective promotes understanding of biological mechanisms of host–microbial interactions, providing explanations for patterns discovered via different disciplinary approaches, such as genetic, physiological, behavioural or ecological. Such a perspective may explain, for example, why some types of interactions occur and recur, while others are rare or apparently absent globally, in specific host taxa or under particular ecological conditions. For example, microbiome-mediated protection against pathogens is very widespread in both animals and plants, while Archaea other than methanogens are apparently rarely associated with eukaryotes, and beneficial intracellular bacteria are largely unknown in vertebrates but widespread in many invertebrate animal groups. Of equal importance, evolutionary understanding can help make microbiome science more predictive: meticulous studies that demonstrate how change or elimination of the microbiome influences host traits, for example, call for eco-evolutionary frameworks that will explain these findings in a broader context and will aid in inference of mechanisms and processes. Considering, for instance, how hosts have adapted to accommodate or to rely on the microbiome and the consequences for the phenotype and evolutionary trajectory of the host may explain otherwise-puzzling phenomena, from coral bleaching to the effects of antibiotics. As our science becomes more predictive, its application to solve real-world problems will become more reliable. Some important discoveries have already been made, including the resolution of Clostridium difficile infections in human patients by certain gut bacteria, the suppression of Aedes mosquito-transmitted dengue virus by Wolbachia bacteria, and plant tolerance of high temperatures conferred by fungal endophytes. These can best be understood in an eco-evolutionary context: the systematic application of evolutionary principles to microbiome science has the potential to enable transformative advances in medicine, agriculture and public health.

This volume containing 15 reviews and opinion pieces brings together the insights and expertise of 36 authors from six countries. Conceptually, the articles can be assigned to two broad themes. The first theme concerns how the microbiome influences host traits and fitness, revealing both the pervasive role of the microbiome as a selective force on their hosts, and as a modality of host adaptation to environmental challenges. The second theme explores the evolutionary process at scales from micro-evolution in host populations to macro-evolutionary phylogenies. Cutting across these two themes, some articles focus on specific systems, e.g. humans, corals, fish, while others draw on the literature for many animal and plant systems or explore general evolutionary principles without reference to specific taxa.

The issue starts with two articles that highlight fundamental evolutionary processes. First, Kolodny & Schulenberg [1] treat the microbiome as a source of adaptive phenotypic plasticity. They suggest that hosts, faced with a novel environmental challenge, may adapt to the challenge via changes in the composition of their microbiome. Such adaptation is analogous to the well-known Baldwin effect, but in addition involves feedback loops and eco-evolutionary dynamics that play out on a range of time scales, portraying a rich picture of adaptive processes. The following review by Moeller & Sanders [2] develops this theme, focusing particularly on how microbiome effects have shaped, and arguably continue to shape, mammalian evolution.

With this conceptual framework, the volume explores the adaptive response of hosts to the microbiome from a variety of perspectives. Three articles consider host physiological systems that interact directly with the microbiome. Centre-stage in any consideration of host–microbiome interactions is the host immune system, which both controls and is influenced by the microbial partners. Gerardo, Hoang & Stoy [3] review the ways in which the immune system interacts with microbial symbionts, and how immunological processes can constrain the evolution of the participating organisms. The complementary opinion article of McLaren & Callahan [4] argues that hosts are adapted to promote microbial taxa that confer pathogen resistance, generating what the authors aptly term ‘cooperative immunity'. The interaction between host metabolism and the microbiome is considered by Fontaine & Kohl [5], who explore the value of optimality thinking, specifically symmorphosis which hypothesizes that host metabolism is structured by natural selection to match the functional demand of the association. Founded on current understanding of nutritional interactions between various animals and their microbiome, these authors predict specific testable patterns in selection pressures for microbiome-dependent regulation of host metabolic function. These considerations segue directly to the article of Grieneisen, Muehlbauer & Blekhman [6], which reviews the patterns of microbial control over gene expression in primates and its implications for primate and human evolution.

There is growing evidence for developmental orchestration of the composition and function of the microbiome, reflecting the variation in selection pressures and evolutionary constraints at different host life stages. Linking to the emerging interest in the interface between microbiomes and life-history theory, two articles in this issue focus on the microbiome associated with two key life stages. Nyholm [7] reviews the incidence and consequences of egg–microbiome interactions in animals. Until recently, most egg-associated microorganisms were described as a biologically ‘silent' transmission stage ensuring the colonization of newly hatched offspring with maternal microbes. Nyholm calls for a radical reassessment of the adaptive evolution of eggs in the light of growing evidence that egg-associated microorganisms can protect the egg against abiotic stresses and natural enemies (both predators and pathogens). At the other end of the animal lifespan, Popkes & Valenzano [8] summarize findings about the influence of the microbiome on survival as organisms age, using in particular insights from recent studies of vertebrates and their microbiomes, and discuss the mechanisms involved and the ways in which this may have affected host evolution and host–microbiome coevolutionary dynamics. Developmental orchestration of the host–microbiome relationship also involves the localization of the microbiome, including host adaptations that restrict microorganisms to specific organs or sites in the body. Chomicki, Werner, West & Kiers [9] review various modes of microbiome compartmentalization in plants, insects and vertebrates, and they discuss how this allows the host to control resource flow, to discriminate cooperative from defecting microbial partners, and to manipulate the microbiome composition. Weighing costs and benefits of compartmentalization, they explore the different selection pressures that may have determined which hosts evolved compartmentalization and which have not. One form of compartmentalization involves symbiotic organs, i.e. organs whose sole function is to house and maintain the microbial partners. Douglas [10] adopts an evolutionary developmental (evo–devo) approach to explore how the developmental biology of symbiotic organs can provide insights into their evolutionary origins, and advocates for the greater use of genetic technologies to test whether conserved genetic circuitry might underlie the apparently convergent evolution of symbiotic organs in different host lineages.

The possible effects of the microbiome on behaviour has attracted much attention and, until recently, more speculation than data. As the evidence for behavioural correlates of the presence and composition of the microbiome accumulates, an evolutionary perspective becomes imperative. Fortunately, a robust conceptual framework is provided by the well-established discipline of behavioural ecology. This issue includes two stimulating and provocative opinion articles that illustrate the opportunities of interdisciplinary synthesis between microbiome research and behavioural ecology. Gurevich, Lewin-Epstein & Hadany [11] lay out a theoretical model of microbiome effects on paternal care, including the consequences of microbiome-mediated manipulation of host behaviour on the mating and parenting strategies of male hosts. Natan, Fitak, Werber & Vortman [12] suggest that information that hosts derive from magnetotactic bacteria in their microbiomes may be the answer to a long-standing puzzle: how do animals, from protists to birds, sense magnetic fields? They lay out supporting evidence for this suggestion, and they discuss various specific mechanisms by which hosts might incorporate information from resident magnetotactic microbes.

The closing articles of the issue return to the theme of how the microbiome affects pattern and process in host evolution. Two articles focus on specific systems. Hawkes, Bull & Lau [13] reinforce and build on the several articles that address the evolutionary consequences of microbiomes with defensive function. Focusing on plants, they explore the micro-evolutionary consequences of microbiomes that confer protection against both pathogens and abiotic stress, including an analysis of the impact of host–microbial partner fidelity on the evolutionary trajectory of these relationships. The article by van Oppen & Medina [14] on scleractinian corals illustrates how genome sequence data can shed light on the genetic basis of interactions with bacterial and algal partners and the ecological success of these associations. Finally, Koskella & Bergelson [15] address a pressing question facing the study of microbiome effects on host evolution: can these complex and dynamic associations be accommodated within current understanding of evolutionary and coevolutionary processes? This article reviews current understanding of (co)evolution between hosts and microbiomes, including the patterns of selection on the partners, as individuals and a group, and provides a fresh and informed perspective on this hotly debated issue.

Together, the articles in this issue demonstrate the key opportunities and challenges that an evolutionary perspective can offer to researchers in the discipline of microbiome science. Evolutionary thinking provides the basis for rational explanation and prediction in biology, and it is most powerful when combined with explicit formulation of testable hypotheses. Our discipline is most fortunate to have access to a broad range of genetic, phylogenetic, physiological, behavioural and ecological methodologies. These tools and an evolutionary mindset offer the strongest route for scientific advance in our understanding and application of host–microbiome interactions.

Biographies

Editor biographies

Oren Kolodny is a senior lecturer in the Department of Ecology, Evolution, and Behavior in the Institute for Life Sciences in The Hebrew University of Jerusalem. He received his BSc degree in Physics and Humanities and his MSc degree in evolutionary biology in the Hebrew University and did his PhD in the department of Zoology in Tel Aviv University. Oren studied a broad range of eco-evolutionary questions during his post-doc at Stanford, and his lab now explores a diverse set of topics, from the influence of the microbiome on its host's ecology and evolution, through questions in conservation of endangered species and the dynamics of invasive species, to studies of cultural evolution and human prehistory.

Benjamin Callahan is an assistant professor in the Population Health and Pathobiology department of the North Carolina State University College of Veterinary Medicine. He received a BSc degree in physics and mathematics from Iowa State University and a PhD degree in Physics from the University of California, Santa Barbara. His current research focuses on the accuracy, precision and reproducibility of measurements of the microbiome, and on the application of measurement and analysis methods to various microbiome-related topics including preterm birth, foodborne pathogen detection and antimicrobial resistance. Ben has become a great admirer of the field of software engineering through his experiences developing and maintaining software packages used by microbiome researchers, such as DADA2 and decontam, and maintains an abiding interest from his PhD and post-doc days in the evolutionary process and its role in so many important biological phenomena.

Angela Douglas is the Daljit S. and Elaine Sarkaria Professor of Insect Physiology and Toxicology at Cornell University. She received a BA degree in zoology at the University of Oxford and PhD at Aberdeen University. Her research focuses on interactions between animals and beneficial microorganisms, with particular emphasis on the gut microbiome of Drosophila and intracellular bacteria in plant sap-feeding insects. Her research has demonstrated multiple effects of the microbiome on host nutrition, including energy storage, protein growth and the dynamics of host metabolism, offering opportunities for microbiome-based strategies for improved metabolic health and novel insect pest control strategies.

Data accessibility

This article has no additional data.

Authors' contributions

The authors contributed equally to this article.

Competing interests

We declare that we have no competing interests.

Funding

O.K. is partially funded by the Gordon and Betty Moore Foundation, GBMF9341, https://doi.org/10.37807/GBMF9341.