In the beginning: egg–microbe interactions and consequences for animal hosts

Microorganisms are associated with the eggs of many animals. For some hosts, the egg serves as the ideal environment for the vertical transmission of beneficial symbionts between generations, while some bacteria use the egg to parasitize their hosts. In a number of animal groups, egg microbiomes often perform other essential functions. The eggs of aquatic and some terrestrial animals are especially susceptible to fouling and disease since they are exposed to high densities of microorganisms. To overcome this challenge, some hosts form beneficial associations with microorganisms, directly incorporating microbes and/or microbial products on or in their eggs to inhibit pathogens and biofouling. Other functional roles for egg-associated microbiomes are hypothesized to involve oxygen and nutrient acquisition. Although some egg-associated microbiomes are correlated with increased host fitness and are essential for successful development, the mechanisms that lead to such outcomes are often not well understood. This review article will discuss different functions of egg microbiomes and how these associations have influenced the biology and evolution of animal hosts. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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Optimal integration between host physiology and functions of the gut microbiome

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0594 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190594 ◽

Cited By ~ 4

Author(s):

Samantha S. Fontaine ◽

Kevin D. Kohl

Keyword(s):

Microbial Communities ◽

Physiological Function ◽

Biological Organization ◽

Theme Issue ◽

Microbe Interactions ◽

Host Physiology ◽

Host Microbe Interactions ◽

Host Evolution ◽

Physiological Systems

Host-associated microbial communities have profound impacts on animal physiological function, especially nutrition and metabolism. The hypothesis of ‘symmorphosis’, which posits that the physiological systems of animals are regulated precisely to meet, but not exceed, their imposed functional demands, has been used to understand the integration of physiological systems across levels of biological organization. Although this idea has been criticized, it is recognized as having important heuristic value, even as a null hypothesis, and may, therefore, be a useful tool in understanding how hosts evolve in response to the function of their microbiota. Here, through a hologenomic lens, we discuss how the idea of symmorphosis may be applied to host-microbe interactions. Specifically, we consider scenarios in which host physiology may have evolved to collaborate with the microbiota to perform important functions, and, on the other hand, situations in which services have been completely outsourced to the microbiota, resulting in relaxed selection on host pathways. Following this theoretical discussion, we finally suggest strategies by which these currently speculative ideas may be explicitly tested to further our understanding of host evolution in response to their associated microbial communities. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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The study of host–microbiome (co)evolution across levels of selection

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0604 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190604 ◽

Cited By ~ 2

Author(s):

Britt Koskella ◽

Joy Bergelson

Keyword(s):

Paradigm Shift ◽

Dynamic Nature ◽

Theme Issue ◽

Critical Question ◽

Microbiome Composition ◽

Single Host ◽

Host Evolution ◽

Existing Data ◽

Over Time

Microorganismal diversity can be explained in large part by selection imposed from both the abiotic and biotic environments, including—in the case of host-associated microbiomes—interactions with eukaryotes. As such, the diversity of host-associated microbiomes can be usefully studied across a variety of scales: within a single host over time, among host genotypes within a population, between populations and among host species. A plethora of recent studies across these scales and across diverse systems are: (i) exemplifying the importance of the host genetics in shaping microbiome composition; (ii) uncovering the role of the microbiome in shaping key host phenotypes; and (iii) highlighting the dynamic nature of the microbiome. They have also raised a critical question: do these complex associations fit within our existing understanding of evolution and coevolution, or do these often intimate and seemingly cross-generational interactions follow novel evolutionary rules from those previously identified? Herein, we describe the known importance of (co)evolution in host–microbiome systems, placing the existing data within extant frameworks that have been developed over decades of study, and ask whether there are unique properties of host–microbiome systems that require a paradigm shift. By examining when and how selection can act on the host and its microbiome as a unit (termed, the holobiont), we find that the existing conceptual framework, which focuses on individuals, as well as interactions among individuals and groups, is generally well suited for understanding (co)evolutionary change in these intimate assemblages. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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The evolution of paternal care: a role for microbes?

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0599 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190599 ◽

Cited By ~ 4

Author(s):

Yael Gurevich ◽

Ohad Lewin-Epstein ◽

Lilach Hadany

Keyword(s):

Natural Selection ◽

Computational Models ◽

Paternal Care ◽

Genetic Models ◽

Theme Issue ◽

Factors Affecting ◽

Host Evolution ◽

Uncertain Paternity ◽

Limited Accuracy

Paternal care, particularly in cases of uncertain paternity, carries significant costs. Extensive research, both theoretical and experimental, has explored the conditions in which paternal care behaviour would be favoured. Common explanations include an adjustment of care with uncertainty in paternity and limited accuracy in parentage assessment. Here, we propose a new explanation that microbes may play a role in the evolution of paternal care among their hosts. Using computational models, we demonstrate that microbes associated with increased paternal care could be favoured by natural selection. We find that microbe-induced paternal care could evolve under wider conditions than suggested by genetic models. Moreover, we show that microbe-induced paternal care is more likely to evolve when considering paternal care interactions that increase microbial transmission, such as feeding and grooming. Our results imply that factors affecting the composition of host microbiome may also alter paternal behaviour. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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Symbiosis and stress: how plant microbiomes affect host evolution

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0590 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190590 ◽

Cited By ~ 1

Author(s):

Christine V. Hawkes ◽

James J. Bull ◽

Jennifer A. Lau

Keyword(s):

Plant Stress ◽

Partner Choice ◽

Microbial Populations ◽

Ecological Understanding ◽

Microbial Responses ◽

Microbe Interactions ◽

Plant Stress Tolerance ◽

Host Evolution ◽

Plant Microbiome

Existing paradigms for plant microevolution rarely acknowledge the potential impacts of diverse microbiomes on evolutionary processes. Many plant-associated microorganisms benefit the host via access to resources, protection from pathogens, or amelioration of abiotic stress. In doing so, they alter the plant's perception of the environment, potentially reducing the strength of selection acting on plant stress tolerance or defence traits or altering the traits that are the target of selection. We posit that the microbiome can affect plant microevolution via (1) manipulation of plant phenotypes in ways that increase plant fitness under stress and (2) direct microbial responses to the environment that benefit the plant. Both mechanisms might favour plant genotypes that attract or stimulate growth of the most responsive microbial populations or communities. We provide support for these scenarios using infectious disease and quantitative genetics models. Finally, we discuss how beneficial plant–microbiome associations can evolve if traditional mechanisms maintaining cooperation in pairwise symbioses, namely partner fidelity, partner choice and fitness alignment, also apply to the interactions between plants and diverse foliar and soil microbiomes. To understand the role of the plant microbiome in host evolution will require a broad ecological understanding of plant–microbe interactions across both space and time. This article is part of the theme issue ‘The role of the microbiome in host evolution'.

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Pathogen resistance may be the principal evolutionary advantage provided by the microbiome

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0592 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190592 ◽

Cited By ~ 5

Author(s):

Michael R. McLaren ◽

Benjamin J. Callahan

Keyword(s):

Natural Selection ◽

Adaptive Evolution ◽

Pathogen Resistance ◽

Tree Of Life ◽

Direct Inhibition ◽

Theme Issue ◽

Evolutionary Advantage ◽

Pathogenic Microbes ◽

Host Evolution

To survive, plants and animals must continually defend against pathogenic microbes that would invade and disrupt their tissues. Yet they do not attempt to extirpate all microbes. Instead, they tolerate and even encourage the growth of commensal microbes, which compete with pathogens for resources and via direct inhibition. We argue that hosts have evolved to cooperate with commensals in order to enhance the pathogen resistance this competition provides. We briefly describe competition between commensals and pathogens within the host, consider how natural selection might favour hosts that tilt this competition in favour of commensals, and describe examples of extant host traits that may serve this purpose. Finally, we consider ways that this cooperative immunity may have facilitated the adaptive evolution of non-pathogen-related host traits. On the basis of these observations, we argue that pathogen resistance vies with other commensal-provided benefits for being the principal evolutionary advantage provided by the microbiome to host lineages across the tree of life. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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The role of the microbiome in host evolution

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0588 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190588 ◽

Cited By ~ 1

Author(s):

Oren Kolodny ◽

Benjamin J. Callahan ◽

Angela E. Douglas

Keyword(s):

Paradigm Shift ◽

Nutritional Quality ◽

Animal Health ◽

Life Sciences ◽

Theme Issue ◽

Microbiome Composition ◽

Sequencing Technologies ◽

Host Evolution ◽

The Relationship

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'.

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Compartmentalization drives the evolution of symbiotic cooperation

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0602 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190602 ◽

Cited By ~ 2

Author(s):

Guillaume Chomicki ◽

Gijsbert D. A. Werner ◽

Stuart A. West ◽

E. Toby Kiers

Keyword(s):

Human Microbiome ◽

Tree Of Life ◽

Common Mechanism ◽

Theme Issue ◽

Single Host ◽

Nutrient Provisioning ◽

Host Evolution ◽

And Control

Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with symbiotic partners. We suggest that the evolution of physical structures that allow hosts to spatially separate symbionts, termed compartmentalization, is a common mechanism used by hosts. Such compartmentalization allows hosts to: (i) isolate symbionts and control their reproduction; (ii) reward cooperative symbionts and punish or stop interactions with non-cooperative symbionts; and (iii) reduce direct conflict among different symbionts strains in a single host. Compartmentalization has allowed hosts to increase the benefits that they obtain from symbiotic partners across a diversity of interactions, including legumes and rhizobia, plants and fungi, squid and Vibrio , insects and nutrient provisioning bacteria, plants and insects, and the human microbiome. In cases where compartmentalization has not evolved, we ask why not. We argue that when partners interact in a competitive hierarchy, or when hosts engage in partnerships which are less costly, compartmentalization is less likely to evolve. We conclude that compartmentalization is key to understanding the evolution of symbiotic cooperation. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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Microbiome-mediated plasticity directs host evolution along several distinct time scales

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0589 ◽

2020 ◽

Vol 375 (1808) ◽

pp. 20190589 ◽

Cited By ~ 3

Author(s):

Oren Kolodny ◽

Hinrich Schulenburg

Keyword(s):

Phenotypic Plasticity ◽

Time Scales ◽

Generation Time ◽

Experimental Tests ◽

Theme Issue ◽

Baldwin Effect ◽

Host Genetic ◽

Host Evolution ◽

The Baldwin Effect

Host-associated microbiomes influence their host's fitness in myriad ways and can be viewed as a source of phenotypic plasticity. This plasticity may allow the host to accommodate novel environmental challenges and thus influence the host's evolutionary adaptation. As with other modalities of phenotypic plasticity in phenomena such as the Baldwin effect and genetic assimilation, the microbiome-mediated plasticity may influence host genetic adaptation by facilitating and accelerating it, by slowing it down, or even by preventing it. The dynamics involved are likely more complex than those of previously studied phenomena related to phenotypic plasticity, and involve different processes on each time scale, such as acquired recognition of newly associated microbes by the host's immune system on single- and multiple-generation time scales, or selection on transmission dynamics of microbes between hosts, acting on longer time scales. To date, it is unclear if and how any of these processes shape host evolution. This opinion piece article provides a conceptual framework for considering the processes by which microbiome-mediated plasticity directs host evolution and concludes with suggestions for key experimental tests of the presented ideas. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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Neurotropic enteroviruses co-opt “fair-weather-friend” commensal gut microbiota to drive host infection and central nervous system disturbances

Behavioral and Brain Sciences ◽

10.1017/s0140525x18002741 ◽

2019 ◽

Vol 42 ◽

Author(s):

Kevin B. Clark

Keyword(s):

Central Nervous System ◽

Nervous System ◽

Gut Bacteria ◽

Infection Cycle ◽

Fair Weather ◽

Host Health ◽

Microbe Interactions ◽

Animal Hosts ◽

Host Infection ◽

Neuropsychiatric Conditions

Abstract Some neurotropic enteroviruses hijack Trojan horse/raft commensal gut bacteria to render devastating biomimicking cryptic attacks on human/animal hosts. Such virus-microbe interactions manipulate hosts’ gut-brain axes with accompanying infection-cycle-optimizing central nervous system (CNS) disturbances, including severe neurodevelopmental, neuromotor, and neuropsychiatric conditions. Co-opted bacteria thus indirectly influence host health, development, behavior, and mind as possible “fair-weather-friend” symbionts, switching from commensal to context-dependent pathogen-like strategies benefiting gut-bacteria fitness.

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