Life history and eco-evolutionary dynamics in light of the gut microbiota

Article (PDF Available)inOikos 126(4):508-531 · April 2017with 577 Reads
DOI: 10.1111/oik.03900
Abstract
The recent emergence of powerful genomic tools, such as high-throughput genomics, transcriptomics and metabolomics, combined with the study of gnotobiotic animals, have revealed overwhelming impacts of gut microbiota on the host phenotype. In addition to provide their host with metabolic functions that are not encoded in its own genome, evidence is accumulating that gut symbionts affect host traits previously thought to be solely under host genetic control, such as development and behavior. Metagenomics and metatranscriptomics studies further revealed that gut microbial communities can rapidly respond to changes in host diet or environmental conditions through changes in their structural and functional profiles, thus representing an important source of metabolic flexibility and phenotypic plasticity for the host. Hence, gut microbes appear to be an important factor affecting host ecology and evolution which is, however, not accounted for in life-history theory, or in classic population genetics, ecological and eco-evolutionary models. In this forum, we shed new light on life history and eco-evolutionary dynamics by viewing these processes through the lens of host-microbiota interactions. We follow a three-level approach. First, current knowledge on the role of gut microbiota in host physiology and behavior points out that gut symbionts can be a crucial medium of life history strategies. Second, the particularity of the microbiota is based on its multilayered structure, composed of both a core microbiota, under host genetic and immune control, and a flexible pool of microbes modulated by the environment, which differ in constraints on their maintenance and in their contribution to host adaptation. Finally, gut symbionts can drive the ecological and evolutionary dynamics of their host through effects on individual, population, community and ecosystem levels. In conclusion, we highlight some future perspectives for integrative studies to test hypotheses on life history and eco-evolutionary dynamics in light of the gut microbiota. This article is protected by copyright. All rights reserved.
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Life history and eco-evolutionary dynamics in light of the gut
microbiota
Emilie Macke, Aurélie Tasiemski, François Massol, Martijn Callens and Ellen Decaestecker
E. Macke (http://orcid.org/0000-0002-5257-4968)(emilie.macke@kuleuven-kulak.be), M. Callens and E. Decaestecker, Laboratory Aquatic
Biology, KU Leuven (Kulak), Dept of Biology, E. Sabbelaan 53, BE-8500, Kortrijk, Belgium. – A. Tasiemski and F. Massol (http://orcid.
org/0000-0002-4098-955X), Univ. Lille, CNRS, UMR 8198 – Evo-Eco-Paleo, SPICI group, Lille, France.
e recent emergence of powerful genomic tools, such as high-throughput genomics, transcriptomics and metabolom-
ics, combined with the study of gnotobiotic animals, have revealed overwhelming impacts of gut microbiota on the host
phenotype. In addition to provide their host with metabolic functions that are not encoded in its own genome, evidence is
accumulating that gut symbionts affect host traits previously thought to be solely under host genetic control, such as devel-
opment and behavior. Metagenomics and metatranscriptomics studies further revealed that gut microbial communities
can rapidly respond to changes in host diet or environmental conditions through changes in their structural and functional
profiles, thus representing an important source of metabolic flexibility and phenotypic plasticity for the host. Hence, gut
microbes appear to be an important factor affecting host ecology and evolution which is, however, not accounted for in
life-history theory, or in classic population genetics, ecological and eco-evolutionary models. In this forum, we shed new
light on life history and eco-evolutionary dynamics by viewing these processes through the lens of host–microbiota inter-
actions. We follow a three-level approach. First, current knowledge on the role of gut microbiota in host physiology and
behavior points out that gut symbionts can be a crucial medium of life-history strategies. Second, the particularity of the
microbiota is based on its multilayered structure, composed of both a core microbiota, under host genetic and immune
control, and a flexible pool of microbes modulated by the environment, which differ in constraints on their maintenance
and in their contribution to host adaptation. Finally, gut symbionts can drive the ecological and evolutionary dynamics of
their host through effects on individual, population, community and ecosystem levels. In conclusion, we highlight some
future perspectives for integrative studies to test hypotheses on life history and eco-evolutionary dynamics in light of the
gut microbiota.
All animals live in intimate association with communities of
microorganisms, known as microbiota, composed of bacte-
ria, archaea, anaerobic fungi, protozoa and viruses. e vast
majority of these microbes reside in the gut, where they are in
continuous and intimate contact with host tissues, and where
they can outnumber the surrounding host cells by at least an
order of magnitude (Bäckhed et al. 2005, Amato 2016). e
existence of these microbes has first been reported several
centuries ago, but until recently they remained largely under-
studied, and thus unknown, essentially because they are dif-
ficult to extract and to cultivate in the laboratory. A decade
ago, the advent of sequencing technologies finally opened up
this frontier (Gilbert et al. 2015). e emergence of power-
ful genomic tools, such as high-throughput transcriptomics
and metabolomics, applied to the older technology of gno-
tobiotics, have led to a detailed understanding of how micro-
biota shapes many aspects of host physiology (Hooper et al.
2012). Combined to whole-genome shotgun metagenomics
and metatranscriptomics, which allow precisely determin-
ing the taxonomic composition and functional profiles of
gut microbial communities, it is now possible to estimate
how variations in gut microbiota can affect the host and be
affected by various environmental and dietary conditions
(Rampelli et al. 2015).
Evidence has accumulated that the gut microbiota is not
just a random set of microorganisms, but rather a complex
community that plays a critical role in host physiology and
behavior (Engel and Moran 2013, Douglas 2015, Amato
2016; Fig. 1). In particular, gut symbionts provide their host
with metabolic capabilities not directly encoded in the host
genome, such as digestion of plant polysaccharides (David
et al. 2014) or detoxification of food-borne toxins (Kikuchi
et al. 2012, Kohl et al. 2014), and contribute to the normal
development of the host, e.g. by fostering the maturation of
the immune system (Belkaid and Hand 2014). Dysbioses
in the gut microbial community have recently been associ-
ated with diseases such as obesity, diabetes or inflammatory
bowel disease, and new therapies based on fecal transplants
are progressively emerging to prevent or cure such diseases
(Belkaid and Hand 2014). Consequently, the gut microbiota
has started to be studied intensively and is a burgeoning field
of scientific research. So far, most studies have focused on
© 2016 e Authors. Oikos © 2016 Nordic Society Oikos
Subject Editor: Dries Bonte. Editor-in-Chief: Dustin Marshall. Accepted 11 November 2016
Oikos 000: 001–024, 2017
doi: 10.1111/oik.03900
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the bacterial component of the microbiota, while there is a
relative lack of research on other gut microorganisms, such
as archaea, fungi or viruses (Ogilvie and Jones 2015). In this
review, the term ‘gut microbiota’ thus mainly refers to the
bacterial gut microbiota.
Despite its impact on host physiology and behavior, the
gut microbiota is rarely accounted for in life-history theory,
as well as in classic population genetics-, ecological- and
eco-evolutionary models. Contrary to the genome, which
is largely static, the microbiome is highly flexible, and can
respond rapidly to changes in host diet or environmental
conditions, e.g. through changes in the taxonomic compo-
sition of the community (David et al. 2014). It may thus
represent an important source of metabolic flexibility for the
host. As such, the gut microbiome is sometimes referred as
“the third malleable genome” (Carroll et al. 2009), and is
increasingly hypothesized to play a role in host ecology and
evolution (Bordenstein and eis 2015, Gilbert et al. 2015).
An emerging theory suggests that animals should no longer
be seen as autonomous entities, but rather as a biomolecular
network composed of the host plus its associated microbes,
i.e. the ‘holobiont’, the collective genome of which being
referred to as “hologenome” (Bordenstein and eis 2015).
Animals may therefore be considered as polygenomic
entities, in which variation in the hologenome can lead to
variation in phenotypes upon which natural selection, and
genetic drift, can operate. is theory, however, is still highly
debated. While most biologists agree that microorganisms
likely play an important role in host evolution, the idea that
hosts and its associated microorganisms form a primary
unit of natural selection, and represent two components of
a unified genome, is more controversial (Moran and Sloan
2015). Especially, how gut symbionts evolve, and whether
they undergo natural selection to benefit their host, is still
far from being evident (Moran and Sloan 2015). Indeed,
the gut microbiota is a complex, heterogeneous and variable
community of microbes, which is assembled anew in each
host generation through different transmission routes. At
one extreme, gut symbionts can be directly transferred from
mother to offspring, but most of the time they are randomly
picked up from the environment (Moran and Sloan 2015,
Shapira 2016). Hence, contrary to endosymbionts, vertical
transmission of gut microbiota is rare and imperfect. e
symbiotic part of the hologenome within the host–symbiont
association is thus “labile”, i.e. it can be lost between genera-
tions (Shapira 2016). As such, the evolutionary interests of
hosts and symbionts are not necessarily aligned, and micro-
organisms may tend to evolve selfish traits, at the expense
of the holobiont (Moran and Sloan 2015, Wasielewski et al.
2016). Gut microbes are also not mutualistic in the truest
Host’s immune
effectors (e.g. AMPs)
Pathogens
Colonization
resistance
Competition
Bacterial AMPs
Food digestion &
Toxins breakdown
Metabolites
Vitamins, SCFAs,
Amino acids
Signaling
pathways
Metabolism, growth
& development
Pheromones
Kairomones
Neuroactive substances
Behavior &
Social interactions
Cellulose,
carbohydratesTo xins
Gut lumen
PRR
Immune pathways
Intestine & immune
system maturation
Figure 1. Contributions of the gut microbiota to host phenotype. e gut microbiota (white rods) contributes to the normal development of
the intestine and the immune system (yellow). In addition, by interfering with host immune pathways, and by competing with other microbes,
gut symbionts enhance colonization resistance and thus protects the host against invading pathogens (red). Gut microbiota also has a crucial
role in food digestion (e.g. breaking down non-digestible substrates) and in the provisioning of important nutrients to the host. Moreover, it
helps in the degradation of either food-borne or environmental toxins (blue). e production of secondary metabolites by gut bacteria can
interfere with host signaling pathways (e.g. insulin pathway), resulting in various effects on host physiology and developmental processes (e.g.
growth, fat metabolism) (green). By producing neuro-active substances that directly act on host brain, or pheromones/kairomones that mediate
inter- or inter-species communication, gut microbiota further influences host behavior and social interactions (purple).
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sense; some of these organisms can be pathogenic to some
extent, while others might directly interfere with mutualistic
microbes (e.g. through toxins), and their status can change
with environmental conditions (Callens et al. 2016, King
et al. 2016; Fig. 2). Variations in the gut microbiota compo-
sition are thus not always adaptive for the host, as evidenced
by dysbioses-induced diseases. Overall, understanding the
gut microbiota, and its role in ecology and evolution, is
relatively more complicated than intracellular symbionts
because gut symbionts evolve in the ‘grey zone’ of symbiotic
interactions, i.e. are not strictly vertically, nor horizontally
transmitted, are facultative symbionts, and can be mutual-
istic or pathogenic depending on environmental conditions.
e molecular dialog between hosts and gut symbionts
starts to be deciphered, highlighting a crucial role of host
immune pathways in the acquisition and control of gut
microbiota (Vavre and Kremer 2014, Tasiemski et al. 2015).
Although the study of these mechanisms is still in its infancy,
it may provide an opportunity to better understand host–-
microbiota interactions, as well as their ecological and evo-
lutionary impacts. Shapira (2016) recently highlighted the
multilayered structure of the gut microbiota, composed of
both a core microbiota, under host genetic and immune
control, and a flexible pool of microbes modulated by the
environment, which likely differ in their contribution to
host fitness and in constraints on their maintenance (e.g.
the core microbiota is expected to contribute to more essen-
tial functions, and to be more reliable transmitted across
generations). Based on this framework, and after a review
of the diverse functions ensured by gut symbionts, we will
demonstrate how gut microbiota can mediate life history,
and drive the ecological and evolutionary dynamics of their
host, through effects on individual, population, community
and ecosystem levels (Fig. 3). We will finally delineate par-
ticular future perspectives for integrative studies to test these
hypotheses.
The pivotal role of gut microbiota in life history
mediated via effects on host physiology and behavior
Host nutrition and metabolism
e gut microbiota plays a prominent role in the host nutri-
tional ecology, either by aiding in digestion, or by providing
nutrients that are limited or lacking in the diet (Engel and
Moran 2013; Fig. 1). For instance, herbivorous insects and
mammals lack the appropriate enzymes to digest plant cell
wall material and resistant starches, and thus rely on their
gut symbionts to convert these indigestible compounds into
absorbable short-chain fatty acids (SCFAs) (Feldhaar 2011,
Douglas 2015, Amato 2016). In herbivorous animals, e.g.
termites, mutualistic gut symbionts also compensate for the
low amount of nitrogen provided by plants, either by recy-
cling nitrogenous waste products excreted by the host, or by
fixing nitrogen from the atmosphere (Hongoh et al. 2008,
ong-On et al. 2012).
e enzymatic degradation of food by bacteria, associated
with the signaling and epigenetic roles of bacterial metabo-
lites, have strong impacts on host metabolism, especially on
energy storage (Bäckhed et al. 2004, Tremaroli and Bäckhed
2012, Douglas 2015). In mice, the gut microbiota increases
both fat deposition and metabolic rate, through an increased
processing of polysaccharides and interactions with host
metabolic pathways (Bäckhed et al. 2004). Interestingly, the
gut microbiota differs between obese and non-obese mice
(Sommer and Bäckhed 2013), with more genes encoding for
carbohydrate metabolism enzymes and providing a greater
capacity to extract energy from the diet in the microbiome
of obese mice (Turnbaugh et al. 2006, 2009). Gut micro-
biota transplants towards germ-free animals further result in
the transfer of the donor phenotype (obese or lean), with
a higher fat deposition in mice receiving the gut microbes
from obese donors (Turnbaugh et al. 2006), highlighting the
pivotal role of gut microbiota in host metabolism. In Droso-
phila, germ-free animals have elevated levels of lipid and glu-
cose, together with reduced basal metabolic rates, indicative
of enhanced energy harvesting (Douglas 2014, Newell and
Douglas 2014, Ridley et al. 2012). ese effects have been
linked to altered insulin signaling in the host (Shin et al.
2011). From an ecological and evolutionary point of view,
microbial effects on host metabolism and fat deposition can
be important in areas with highly variable food resources or
extreme weather (Amato 2016), as host adipose tissues play
an important role in thermoregulation (Kozak et al. 2010).
In the same vein, cold exposure leads to a marked shift in
the gut microbiota composition of mice, and transplantation
of ‘cold’ microbiota to germ-free mice increases tolerance to
cold by promoting white fat browning, leading to increased
energy expenditure and fat loss. Transplant experiments fur-
ther showed that, during prolonged cold, the gut microbiota
is responsible for altered intestinal gene expression promot-
ing increased gut absorptive surface, thus increasing caloric
uptake (Chevalier et al. 2015).
In addition to contributing to food digestion, the gut
microbiota participates, through its enzymatic activities, in
the metabolism of xenobiotic bioactive molecules, such as
diet-derived toxins, human-crafted poison or therapeutic
drugs (Carmody and Turnbaugh 2014; Fig. 2), e.g. in her-
bivorous species which strongly depend on their gut symbi-
onts to escape toxins produced by the plant they consume.
In desert woodrats, for example, specialization of some pop-
ulations on the highly toxic creosote bush is mediated by
gut microbes: a disruption of the gut microbiota with anti-
biotics results in their inability to consume creosote toxins
(Kohl et al. 2014). In the same way, gut symbionts enable
Environment &
Diet Microbiota
Immunity
Nutrients, fiber, toxins
Fermentation Competition,
AMPs production
Figure 2. A complex network of interactions between the environ-
ment, the immune system and gut symbionts mediates the compo-
sition of the resident gut microbiota (adapted from Belkaid and
Hand 2014). Arrows indicate fluxes of nutrients, metabolites, vita-
mins, etc. and biotic processes within the host (e.g. fermentation or
competition).
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highly dependent on the presence of commensal intestinal
bacteria to achieve a normal development.
In both invertebrate and vertebrate species, gut bacteria
apparently promote host growth and development either
indirectly through their role in nutrient provisioning, or
directly through interference with host physiology, e.g. by
providing signals that stimulate developmental processes
(Engel and Moran 2013; Fig. 1). In mice and zebrafish, gut
microbes are required for a proper development of the gut
(reviewed by Gilbert et al. 2015). Indeed, germ-free animals
have smaller and less functional intestines, and these defects
can be reversed by the introduction of bacteria later during
animal development (Bates et al. 2006). e gut microbiota
the coffee berry borer to feed on coffee berries while avoid-
ing the otherwise toxic effects of caffeine (Ceja-Navarro et al.
2015). Such bacterially derived detoxification contributes to
local niche adaptation, and provides the host with food or
a habitat that would otherwise be inaccessible (Engel and
Moran 2013, Shapira 2016).
Host development and maturation of the immune system
ere is increasing evidence that bacterial symbionts influ-
ence host processes once thought to depend solely on the
genetic program of the host, including development, mor-
phogenesis and cell proliferation (Sommer and Bäckhed
2013, Gilbert et al. 2015). As such, host species are often
Selective recruitment
Available pool of microbes (potential colonizing symbionts)
Maternal microbiota Horizontal transfer Environmental bacteria
Resident gut
microbiota
Among-microbes
interactions
Host functions
Immunity
Physiology
Metabolism
Behavior
Ecology
Selection
Host evolution
Adaptation to the
environment
Host
population/species
Invasiveness
Divergence &
speciation
Communities &
ecosystems
Eco-evolutionary
dynamics
Landscapes
Host life history
and fitness Co-evolutionary
processes
Host genes
Vertically transmitted microbes
Horizontally transmitted microbes
Microbes acquired from the environment
Effects of microbiota on host fitness
Establishment of a core and a flexible
microbiota
Role of gut microbiota in eco-
evolutionary dynamics
Figure 3. e gut microbiota as a key factor of eco-evolutionary dynamics in natural systems. e gut microbiota has large impacts on host
physiology and behavior, and consequently on host life history and fitness (red arrows). Unlike intracellular symbionts, which are strictly
vertically transmitted to the embryo, gut associated microbes are mainly acquired during and after birth via maternal transmission and
horizontal transfer from either conspecifics or the surrounding environment. From this pool of microbes available to the host, only a certain
proportion is selectively recruited in the resident gut microbiota, depending on both host factors (genetic background, immunity) and a
complex interaction network between host, microbes and environmental factors (blue arrows). e gut microbiota is thus composed of
both a flexible pool of microbes, dependent on environmental diversity and external conditions, and a core microbiota linked to host genet-
ics. is duality makes the gut microbiota a source of both phenotypic plasticity, through fast variations in gut microbiota composition
within the life cycle of the host, and evolution, through selection on symbiont-mediated traits. Adaptation to local environmental condi-
tions can result in a rapid evolution of host genes (especially immune genes) involved in acquisition, control and tolerance of beneficial
symbionts, allowing for a co-inheritance of nuclear genes and microbes, which is a pre-requisite for evolution to occur. At the population
and species levels, such evolution can contribute to population divergence and speciation, or increase the invasiveness of the host species.
By mediating the interactions of the host with the rest of the community (e.g. parasites, host plant, predators), and by acting as an ecosys-
tem engineer that contributes to shaping the biotic and abiotic environment of the host, gut symbionts can further affect eco-evolutionary
dynamics and regulate community and ecosystem functioning (green arrows).
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host immunity, thus promoting their own containment and
limiting pathogen invasion (Hooper et al. 2012, Honda and
Littman 2016, aiss et al. 2016). In humans, imbalance in
the gut immune system homeostasis has a negative impact
on health, causing severe and/or chronic pathologies. Intes-
tinal dysbiosis during maturation of the immune system is
correlated with a failure of the immunological tolerance that
subsequently leads to exacerbated local auto-inflammatory
disorders such as inflammatory bowel diseases (IBD), but
also extra-intestinal inflammatory and autoimmune disorders
such as type 1 diabetes or rheumatoid arthritis (Kahrstrom
et al. 2016, Kataoka 2016). e system becomes even more
complex when taking into consideration the environmen-
tal/ecological context. In high-income countries, overuse of
antibiotics, changes in diet, and ‘over-hygienic conditions’,
can have selected for a gut microbiota that lacks the resil-
ience and diversity required to establish balanced immune
responses. is phenomenon referred to as the ‘hygiene
hypothesis’ (Box 1) might explain the dramatic rise in auto-
immune and inflammatory disorders, like IBDs such as
Crohn disease (Belkaid and Hand 2014). Understanding
the ecological, environmental influences on gut immunity
is another frontier for immunologists to cross by exploring
immuno-ecological concepts that would bridge the gap with
immunology concepts developed by ecologists.
Protection against parasites and pathogens
Increasing evidence demonstrates that the gut microbiota
plays a crucial role in host resistance against invading patho-
gens within the intestine, a process referred to as colonization
resistance (Kamada et al. 2013; Fig. 1). Consequently, loss or
also contributes to the homeostasis of the intestinal tissue,
by regulating the balance between cell renewal and death
(Broderick and Lemaitre 2012, Engel and Moran 2013,
Sommer and Bäckhed 2013). For example in Drosophila
melanogaster, the gut microbiota apparently promotes stem
cell proliferation and epithelium renewal, a process essen-
tial to the defense against bacterial infection. However, in
mutant flies unable to control the population of commen-
sal bacteria, an excessive proliferation of intestinal stem cells
can be observed, suggesting that the host response depends
on bacterial load and the composition of the microbiota
(Buchon et al. 2009).
Animal–bacteria interactions contribute at the organism
or tissue level to the development and maturation of the
immune system along the life of an individual (Fig. 1). Some
host species can be highly dependent on the presence of
intestinal bacteria, as exemplified by germ-free mice which
present an undeveloped mucosal immune system, a reduced
epithelial cell turn-over, resulting in a lower ability to regain
tissue homeostasis following injuries of the intestine as well
as structureless immune organs (lymph nodes and spleen;
Rakoff-Nahoum et al. 2004). Germ-free individuals suf-
fer from serious immune defects, and are more susceptible
to infections than colonized animals (Belkaid and Hand
2014).
e crosstalk between intestinal immunity and micro-
biota is particularly well described in mammals thanks to
the development of very powerful models such as germ-
free mice. A brief overview of this inter-relation is given
in Box 2 and Fig. 4. Gut symbionts have the remarkable
ability to promote and calibrate both innate and adaptive
Figure 4. Gut microbiota and host immunity. Schematic representation of immune system development and maturation before birth, after
birth and after weaning in mammals (adapted from Renz et al. 2012).
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Direct interactions between commensals and patho-
gens, such as competition for shared nutrients and ecologi-
cal niches, have been shown to play an important role in
colonization resistance (Kamada et al. 2012, Khosravi and
Mazmanian 2013; Fig. 2). By consuming common limited
resources, such as organic acids, amino acids or other nutri-
ents, the indigenous gut microbiota contributes to limit the
growth and the survival of competing pathogenic bacteria.
For example, commensal strains of E. coli were shown to
suppress the growth of entero-hemorrhagic E. coli, through
competition for proline. is phenomenon of colonization
resistance was strongly attenuated by the addition of pro-
line in the medium (Momose et al. 2008). As a result of
competition, microbes have evolved mechanisms to out-
compete each other, such as the production of antimicrobial
substances that inhibit the growth and the survival of other
bacteria within the gut (Kamada et al. 2013). is chemi-
cal warfare further contributes to colonization resistance
against pathogens. For example, E. coli produces bacterio-
cins, a family of antimicrobial peptides (AMPs, Box 1), that
specifically targets similar bacterial strains, thus impairing
the growth of the related entero-hemorrhagic pathogen E.
coli. Similarly, in mosquitoes (Cirimotich et al. 2011) and
leeches (Tasiemski et al. 2015), production of antimicrobial
substances by gut symbionts provides protection against
invasive bacteria. Microbiota-derived metabolites, such as
perturbation of gut microbial communities are often associ-
ated with increased infectivity of pathogenic bacteria, with
evidence from diverse species including both invertebrates
and vertebrates (Engel and Moran 2013, Kamada et al. 2013,
Belkaid and Hand 2014). For example, in bumblebees, gut
microbes were recently shown to protect their host against
Crithidia bombi, a natural and highly virulent parasite (Koch
and Schmid-Hempel 2011). In the mosquito Anopheles gam-
biae, a clearance of gut microbes with antibiotics enhances
infections with Plasmodium falciparum, the causative agent
of malaria (Beier et al. 1994, Dong et al. 2009, Meister et al.
2009, reviewed by Engel and Moran 2013). Microbiota-
mediated resistance to pathogens has also been observed in
vertebrates, e.g. in mice, in which germ-free or antibiotic-
treated individuals are more susceptible to various enteric
pathogen infections (Kamada et al. 2013, Belkaid and Hand
2014). A diverse gut microbial community is expected to be
more difficult for an opportunistic microbe to invade as
more diverse ecological communities can be more resistant
to invaders (Romanuk and Kolasa 2005, Beisner et al. 2006,
Byun et al. 2013), so that individuals with high gut microbial
diversity should be more resistant to invading pathogens.
is hypothesis is supported, e.g. in the desert locust Schis-
tocerca gregaria, in which gut community diversity correlates
negatively with colonization success of the pathogen Serratia
marcescens (Dillon et al. 2005).
Box 1
AMPs (Anti Microbial Peptides). Key components of the innate immune system that rapidly eradicate or incapacitate
pathogenic agents such as viruses, bacteria, fungi, attempting to invade and proliferate in multicellular eukaryotes (Zasloff
2002, Bulet et al. 2004, Maroti et al. 2011). ey have also been evidenced to shape, control and confine the symbiotic
microflora into specific anatomic compartments (gut, bacteriomes, skin…), thus contributing to the symbiostasis of both
invertebrates and vertebrates (Salzman et al. 2010, Gallo and Nakatsuji 2011, Login et al. 2011, Franzenburg et al. 2013,
Tasiemski et al. 2015). In metazoans, the evolution of AMPs has been shown to be driven by recurrent duplications (i.e.
creation of paralogs) and balancing/positive selection to face and kill new and/or altered bacterial pathogens that can be
encountered in a novel habitat and/or that have rapidly evolved to escape the immune response (Tennessen 2005, Gosset
et al. 2014, Unckless et al. 2016).
PRR (Pattern Recognition Receptor). Receptors expressed by invertebrate and vertebrate cells. PRRs sense/recognize
conserved microbial molecules called microbe associated molecular patterns (MAMPs). MAMPs recognition by PRRs
induces, via an intracellular transducing pathway, an immune response (AMPs, cytokines production, cell migration….)
of the cell expressing the PRR. is response can be 1) deleterious by eliciting an inflammatory response; 2) beneficial by
eliminating pathogens or more surprisingly by contributing to various aspects of host development mediated by commen-
sal stimulation of host PRRs. Understanding how the same molecules can achieve such divergent and opposing responses
remains a challenging unanswered question.
SIgA (Secretory IgA): is the most abundant class of antibodies found in the intestinal lumen in most mammals. SIgA
produced by plasma cells, is secreted across the epithelium into the lumen. It serves as the first line of defense in protecting
the intestinal epithelium from enteric toxins and pathogenic microorganisms. SIgA promotes the clearance of antigens and
pathogenic microorganisms from the intestinal lumen by blocking their access to epithelial receptors, entrapping them in
mucus, and facilitating their removal. SIgA has also the capacity to directly quench bacterial virulence factors, and influence
composition of the intestinal microbiota (Mantis et al. 2011).
Tre g cells: comprise a large proportion of the T cells of the intestine in mice and humans. ey play an important role in
maintaining immune tolerance to dietary antigens (Stefka et al. 2014) and to the gut microbiota as well as suppressing
tissue damage caused by immune responses against some bacteria such as Clostridium rodentium (Josefowicz et al. 2012).
Hygiene hypothesis: is a term coined by Strachan (1989) based on reasonable clinical epidemiological evidence showing
that children from families of lower socio-economic status or brought up on farms have a decreased incidence of autoim-
mune or allergic diseases. Exposure to oro-faecal microorganisms and helminthes during childhood leads to deviation/
tradeoff of the immune responses that reduce the development of such atopies in adults.
EV-7
compounds emerging from these glands (Archie and Tung
2015). In Drosophila melanogaster, gut bacteria mediate
olfactory cues involved in social attraction, kin recognition
and mating preferences (Lizé et al. 2013). A striking exam-
ple is described in an experiment in which a population of
inbred flies was divided in two groups reared on two differ-
ent diets (Sharon et al. 2010). Within one generation, popu-
lations developed a mating preference for flies grown on the
same food, a preference that was abolished by an antibiotic
treatment. Infection experiments confirm the role of the gut
microbiota in this mating preference, and especially of the
bacteria Lactobacillus plantarum. Analytical data suggest that
these preferences rely on the modification of pheromone
profiles through the production of cuticular hydrocarbons
which serve as sex pheromones in Drosophila (Sharon et al.
2010). is could be an indirect effect of the symbiont or, as
in the grass grub beetle symbiont L. plantarum, could pro-
duce the pheromone itself (Shapira 2016).
The gut microbiota as crucial mediator of life-history
strategies
By affecting functions as important as nutrition, metabolism,
resistance to pathogens and behavior, the gut microbiota nec-
essarily affects life-history traits contributing to host fitness
(Fig. 3). Evidence mainly comes from studies comparing
germ-free to conventionally reared individuals, in particular
in arthropods, which reveal that gut bacteria have an over-
whelming influence on growth, development, reproduction
and survival. In the fruit fly Drosophila melanogaster (Storelli
et al. 2011) and in the water flea Daphnia magna (Sison-
Mangus et al. 2015, Callens et al. 2016), germ-free individu-
als develop more slowly and are smaller than conventional
animals, while in mosquitoes, axenic larvae fail to develop
beyond the first instar (Coon et al. 2014). In all these spe-
cies, inoculating axenic larvae with gut bacteria can restore
a normal developmental rate (Storelli et al. 2011, Coon
et al. 2014, Callens et al. 2016). Mono-association studies
in Drosophila (Shin et al. 2011, Storelli et al. 2011), mosqui-
toes (Coon et al. 2014) and Daphnia (Peerakietkhajorn et al.
2016) further identified single bacterial strains that are suffi-
cient to recapitulate the natural microbiota growth-promot-
ing effect. In Drosophila, these bacteria exert their beneficial
functions on the host by promoting insulin signaling (Shin
et al. 2011, Storelli et al. 2011). In some species including
Drosophila (Brummel et al. 2004, Ren et al. 2007, Petkau
et al. 2014), Daphnia (Sison-Mangus et al. 2015, Callens
et al. 2016), C. elegans (Houthoofd et al. 2002) and termites
(Rosengaus et al. 2011), germ-free animals have a reduced
lifespan and a lower fecundity.
e effects of gut microbes on host fitness are, however,
not always positive. Partnership with symbionts can entail
direct costs to the host, arising for example from a tradeoff
between allocating resources to symbiosis and reproduction
or growth. In addition, the effects of gut microbes on host
fitness can depend on environmental conditions. For exam-
ple, in Drosophila (Shin et al. 2011, Storelli et al. 2011) and
in Daphnia (Callens et al. 2016), the effects of gut microbes
on host fitness depend on the nutritional value of the diet.
In Drosophila, germ-free larvae exhibit reduced growth and
slower development than conventionally reared larvae, but
only when raised on poor medium. Conversely, in Daphnia,
SCFAs, also contribute to prevent pathogen infection by
altering the intestinal environment (e.g. pH) to inhibit the
growth of pathogens, or by down-regulating the expression
of virulence genes (Gantois et al. 2006).
In addition to these direct effects in invasive microbes, the
gut microbiota capacity to control infection is also associated
with its ability to mediate host immune responses (Kamada
et al. 2013). In mice, individuals treated with antibiot-
ics or raised under germ-free conditions have significantly
impaired immune responses, and are thus more susceptible
to pathogens (Belkaid and Hand 2014). As discussed previ-
ously, commensal bacteria produce signals that can enhance
expression of host defense genes, such as AMPs, which have
the dual effect of promoting their own containment and to
limit pathogen invasion (Belkaid and Hand 2014, Tasiemski
et al. 2015). In mice, the loss of microbiota-induced antimi-
crobial lectin leads to increased bacterial dissemination and
susceptibility to bacterial pathogens (Kamada et al. 2013,
Belkaid and Hand 2014). Another example is that of seg-
mented filamentous bacteria, which promote T-cell differen-
tiation in the mice intestine and are involved in the clearance
of pathogenic bacteria (Gaboriau-Routhiau et al. 2009).
Behavior and social interactions
Some parasites are known to manipulate the behavior of their
host to improve their own transmission. A famous example
occurs in crickets, in which hairworms induce suicidal behav-
ior and jumps into water, so that the parasite can complete
its life cycle (omas et al. 2002). Accumulating data now
indicate that symbiotic bacteria can also affect host behavior
(Archie and Tung 2015, Cryan and Dinan 2015, Shapira
2016; Fig. 1). In vertebrates, the gut microbiota commu-
nicates with the central nervous system through neural,
endocrine and immune pathways and thereby influences
brain function and behavior (Heijtz et al. 2011, Archie and
Tung 2015). Studies in germ-free animals and transplant
experiments have highlighted a role for the microbiota in
modulating stress responses and stress-related behaviors rel-
evant to psychiatric disorders, such as anxiety and depression
(Cryan and Dinan 2015). In germ-free mice, stress expo-
sure induces an exaggerated release of adrenocorticotropic
hormone and corticosterone compared with control mice
with a normal microbiota. e stress response in the germ-
free mice can be partially reversed by colonization with fecal
matter from control animals (Sudo et al. 2004). Reciprocal
microbiota transplant between mice strains differing in their
microbiota composition further reveals that the behavioral
profile of recipient mice is similar to that of the donor strain
(Bercik et al. 2011). ese data clearly demonstrate that the
microbial content of the digestive tract has a direct impact
on the host behavior.
In addition to effects on the nervous system, gut microbes
produce chemical signals used in social communication, thus
affecting social behavior (Archie and Tung 2015; Fig. 1).
As bacterial communities can be shaped by social contacts,
family relationship, genotype, environmental condition or
host health status, they have the potential to communicate
important information about their host (Lizé et al. 2013).
For instance, correlations have been observed between host
traits (e.g. dominance rank, social group membership), the
bacterial communities living in scent glands, and the volatile
EV-8
proposes that closely related species or populations experi-
encing different ecological conditions should consistently
differ in a suite of metabolic, hormonal and immunity traits
that have coevolved with life history (Ricklefs and Wikelski
2002, Wikelski et al. 2003, Martin II et al. 2006, Réale et al.
2010). Low rate of metabolism can be one potential compo-
nent of a slow life history that can lead to selection for other
slow traits, such as low fecundity and late reproduction.
Consistently with this, tropical birds are typically long-lived
and produce few offspring, develop slowly, mature relatively
late in life, and also have a low metabolic rate (Wikelski et al.
2003, Wiersma et al. 2007). Hence, relative to their temper-
ate zone counterparts, tropical birds have a slower pace of
life along both physiological and life-history axes of variation
(Réale et al. 2010). Réale et al. (2010) proposed to further
integrate behavior into this POLS theory. Indeed, there is
increasing evidence that personality phenotypes are linked to
specific life history and physiological patterns. For example,
in mammals, proactivity (i.e. high boldness and aggressive-
ness) is associated with an increased capacity to acquire and
monopolize resources, resulting in higher growth rate and
higher reproductive success, while decreasing longevity. At
the physiological level, proactive animals are characterized
by an elevated adrenaline production and heart rate under
stress, compared to non-proactive animals (Réale et al.
2010).
Given that gut microbiota has overwhelming effects on
host physiology and behavior (Fig. 1), it can be an impor-
tant missing piece in the POLS concept. In mammals, the
composition of the gut microbiota can affect host aggressive-
ness and anxiety levels, which drive variation in personality
traits, and thus in life history (Amato 2016). Furthermore,
by mediating the amount of energy extracted from food and
the metabolic rate, gut microbes can directly affect tradeoffs
between life-history traits. In this way, a microbiota promot-
ing a high metabolic rate would be expected to coevolve
with a fast pace of life. In Daphnia, the gut microbiota is
an important factor mediating the tradeoff between growth,
reproduction and survival (Callens et al. 2016). Indeed, while
an increase in food quantity significantly increases growth
rate and reproduction while decreasing survival in conven-
tionally reared individuals, this effect is less pronounced in
germ-free animals. Another argument supporting the idea
that gut microbiota mediates life-history strategies is that
gut microbiota composition changes across the life cycle of
an individual, in diverse species from insects (Chen et al.
2016) to humans (Kostic et al. 2013). Especially, life-history
processes such as growth and reproduction, which require
additional energy, have been associated with important shifts
in the composition of the gut microbiota, suggesting that
gut microbiota acts as a buffer against variation in metabolic
demands across the life cycle (Kostic et al. 2013, Amato
2016). In humans and mice, for example, shifts in the
maternal microbiota have been associated with adaptation
to pregnancy, with an increase in gut bacteria promoting
fat deposition and energy harvest, which can help mothers
nourish their children (Moeller et al. 2016). Furthermore,
the transfer of this maternal gut microbiota to the newborn
during vaginal delivery can provide the neonate with imme-
diate access to microbiota that allow maximal energy harvest
during the incipient hours of life. Gut microbes may thus be
the positive effects of gut microbes on growth and survival
are only observed when food is sufficient or abundant, with
weaker effects under food limitation, demonstrating the
context-dependency of fitness effects on the host. e ben-
efits provided by symbionts may also depend on the presence
of other organisms in the environment. For example, in the
nematode C. elegans, the mildly pathogenic bacteria Entero-
coccus faecalis living in worms provides protection against
the more virulent pathogen Staphylococcus aureus, crossing
the parasitism–mutualism continuum. In an environment
in which S. aureus virulent infection is common, E. faecalis
would therefore represent a mutualist for the worm, while
being pathogenic in the absence of S. aureus (King et al.
2016).
Because gut symbionts interact with various aspects of
host physiology and metabolism, their effects on host life his-
tory traits can have diverse origins, such as a lower ability of
germ-free animals to extract energy from food. Recent stud-
ies, however, suggest that bacteria-derived metabolites and
RNAs can directly affect life-history traits such as senescence
in the host (Heintz and Mair 2014, Clark et al. 2015). For
example in C. elegans, the bacterial production of nitric oxide
(NO), a critical signaling molecule that C. elegans is unable
to produce, can modulate longevity, probably by regulating
host transcriptional responses (Gusarov et al. 2013, Heintz
and Mair 2014). In addition, Blaser and Webb (2014) suggest
that selection can differentially act on the composition of the
gut microbiota, depending on age. First, before and during
reproductive life, host genes favoring microbes that preserve
host function, e.g. through regulation of energy homeosta-
sis or promotion of fecundity, should be selected. However,
after reproductive life, selection for maintaining these bene-
ficial microbes should decrease, especially if the mechanisms
involved in the control of gut microbes are costly to the host.
Consistently with this, changes in gut microbiota composi-
tion in aging flies are responsible for changes in excretory
function and immune gene activation in the aging intestine,
resulting in a deterioration of the intestinal epithelium and
finally in death (Broderick and Lemaitre 2012, Broderick
et al. 2014, Clark et al. 2015). In humans, alterations of the
composition of the gut microbiota are correlated with aging
and measures of frailty, morbidity and inflammation (Chang
et al. 2008, Willing et al. 2010, Claesson et al. 2012). Such
observations suggest that alteration of microbiota dynamics
can contribute to health decline during aging in animals.
Microbiota and the pace of life syndrome
An important goal of life-history theory is to explain the
range of variation in life-history patterns exhibited in popu-
lations (Stearns 1992). Animal populations can be placed
along a fast–slow continuum, with species that mature early,
have large reproductive rates and short generation times
occupying the ‘fast’ end of the continuum, and those with
the opposite suite of traits occupying the ‘slowend of the
continuum (Read and Harvey 1989, Promislow and Harvey
1990, Réale et al. 2010). e optimal position on this con-
tinuum strongly depends on ecological conditions, which
thus affect the evolution of life-history strategies in natural
populations (Stearns 1992). Given the strong correlations
and mechanistic linkages between physiology and life his-
tory, the pace-of-life syndrome (POLS) hypothesis further
EV-9
between individuals from different species. For example, gut
microbes from humans or zebrafish can successfully establish
in the gut of mice (Seedorf et al. 2014). Social behaviors,
such as coprophagy and trophallaxis, can greatly facili-
tate the acquisition and exchange of beneficial microbes.
Recently, a distinct resident gut microbiota has been identi-
fied in bumblebees and honey bees that is not shared with
related solitary bee species, suggesting that a stable associa-
tion with the host can be facilitated by sociality (Martinson
et al. 2011). Koch and Schmid-Hempel (2011) have shown
that the successful establishment of this specific microbiota,
which protects bumblebees against natural parasites, requires
an exposure to the feces of nest mates after pupal eclosion.
Transmission of beneficial gut bacteria could therefore repre-
sent an important benefit of sociality. e social context also
shapes the establishment of mammalian gut microbiota, like
in Chimpanzees, in which individuals from the same com-
munity have more similar microbiota than with individuals
from different communities (Degnan et al. 2012).
Core versus flexible microbiome
Even when acquired independently at each generation, gut
communities are not random assemblages of bacteria from
the food or local environment (Engel and Moran 2013). e
composition of gut microbiota strongly differs from that of
the surrounding environment, even in filter-feeding species
like Daphnia, which are continuously in close contact with
the bacterioplankton (Freese and Schink 2011, Berg et al.
2016). From the available microbial pool, bacteria can be
selectively recruited in the gut, depending on host immu-
nity and genetic background, as well as on complex interac-
tions between microbes, host physiology and environmental
conditions (Spor et al. 2011, Engel and Moran 2013). In
a recent paper, Shapira (2016) highlights the multilayered
structure of the gut microbiota. On the one hand, a core
microbiota of host-specific microbes is assembled from
diverse environments and determined by host genetic fac-
tors. Although only part of these microbes may be strictly
beneficial to the host, they probably contribute to essential
functions or provide long-term adaptation to stable features
of the niche (e.g. herbivory). On the other hand, a flexible
pool of microbes depends on environmental diversity and on
external conditions. is flexible pool of microbes can vary
within the life cycle of an individual, and can thus exhibit
high inter-individual variation. is variation may be either
beneficial (e.g. diet-induced shift in the gut microbiota, that
may increase digestion efficiency), or detrimental to the host
(e.g. in the case of gut microbiota dysbioses responsible for
diseases in humans). e gut microbial community thus
comprises diverse microbes, some more adapted to their
host, others generalists, or transients, representing a broad
spectrum of potential contributions to host fitness.
e existence of a core microbiota, modulated by
host-dependent processes, has been identified in a num-
ber of species, from insects to mice and humans (Shapira
2016). For instance, in C. elegans, individuals raised in
diverse microbial environments reproducibly assemble
similar microbiota (Engel and Moran 2013, Berg et al.
2016). Similarly, in mice, transplant experiments reveal
that, despite highly dissimilar input communities, the out-
put gut microbial communities of recipient mice cluster
an important mediator of resource allocation strategies, both
within the life cycle of an individual (i.e. the gut microbiota
facilitates the adaptive adjustment of resource allocation pat-
tern), and on evolutionary time scales (i.e. the evolution of
different life-history strategies across species may be associ-
ated with the evolution of different gut microbiota composi-
tions).
The multilayered structure of the gut microbiota and
its consequences for host fitness
Vertical versus horizontal symbiont transmission
Unlike intracellular symbionts, which are strictly vertically
transmitted to the embryo, gut associated microbes are
mainly acquired during and after birth via horizontal transfer
from the surrounding environment (Broderick and Lemaitre
2012, Amato 2016). In many species, like the gypsy moth
or the cabbage white butterfly, gut bacterial communities are
highly dependent of food-related bacteria and are mainly
composed of widespread environmental taxa that opportu-
nistically colonize the gut (Engel and Moran 2013). “Gen-
eralist” bacteria from the soil were shown to successfully
colonize the gut of diverse species including the worm C.
elegans (Engel and Moran 2013), bean bugs (Kikuchi et al.
2012) and mice (Seedorf et al. 2014). ese environmen-
tal bacteria thus represent an important pool of genetic and
functional diversity for the gut microbiota.
Although gut symbionts are not directly transmitted from
the mother to the offspring during embryogenesis, females
sometimes display sophisticated mechanisms for inoculating
progeny with microbial symbionts via vertical transmission,
enabling long-term associations (Engel and Moran 2013).
For example, in some insects, like the Kudzu bug Megacopta
cribraria, juveniles acquire their gut symbionts from bacte-
rial capsules left by their mother (Hosokawa et al. 2008,
Ezenwa et al. 2012). In other insects, such as flies and but-
terflies, the eggshell is contaminated with bacteria derived
from adults. In the greater wax moth Galleria mellonella,
bacteria carrying a fluorescent label cross the gut epithelium
of mothers to reach the ovaries to be deposited on the egg
surface (Freitak et al. 2014). After hatching, larvae ingest the
chorion of embryos and thus acquire the bacteria coating
them (Broderick and Lemaitre 2012). In viviparous species,
including humans, symbionts can directly be transferred from
mother to offspring through direct contamination by vaginal
microbiota during parturition, or through the breast milk
(Amato 2016). Parent–offspring interactions and parental
care further facilitate inter-generational transmission of bac-
teria. us, an element of vertical transmission exists for the
mammalian gut microbiota. In rats, most taxa detected in
maternal feces can also be detected in their pups (Inoue and
Ushida 2003), while in mice, gut microbiota composition
is more similar between mother and offspring than between
unrelated individuals, regardless of diet or genetic similari-
ties shared by unrelated individuals (Ley et al. 2005).
e transmission of bacteria can also occur horizontally
between conspecifics (Engel and Moran 2013). For
instance in gregarious insects, such as cockroaches and
crickets, exchanges of bacteria occur between individu-
als defecating and feeding in a common area (Engel and
Moran 2013). Such transfer of bacteria can further occur
EV-10
a dramatic shift in the community, with an enrichment
of genes associated with carbohydrate utilization, charac-
teristic of the adult microbiome (Koenig et al. 2011). e
nutritional status of the host can further indirectly alter the
structure of the microbiota, by affecting the immune system,
through both metabolic requirements and direct sensing of
food-derived metabolites (Ostaff et al. 2013). In addition
to these diet-mediated effects, the persistence and establish-
ment of exogenous bacteria in the gut depends on among-
microbes interactions. ese interactions can be direct,
including e.g. competition for resources and production of
biologically active molecules like AMPs (Box 2), or indirect,
mediated by the host immune system (Kamada et al. 2013,
Douglas 2015). For instance, one microorganism can stimu-
late (or suppress) the production of immune effectors with
high activity against other microorganisms, so depressing (or
promoting) the abundance of the latter, as observed in the
tsetse fly (Douglas 2015).
The gut microbiota as a community of interacting
species: priority effects, cooperation and selfishness
Recent years have seen an astonishing paradigm convergence
between microbiologists, physiologists and evolutionary ecol-
ogists working on the gut microbiome regarding microbiome
dynamics at the scales of individual hosts and host popula-
tions. In mammals (mice and humans mostly), the process of
gut colonization has proved very similar to ecological succes-
sions (Koenig et al. 2011, Seedorf et al. 2014). e formation
of the gut microbial community can be viewed as a coloniza-
tion process, in which the initial adhesion of early coloniz-
ers to host-derived structure shapes the metabolic milieu in
a manner permissive for establishing a more diversified col-
lection of bacterial species (Hooper and Gordon 2001). For
example, the formation of biofilm modifies spatial structure
and chemical environment, thus influencing the establish-
ment of other species (McNally and Brown 2015). In addi-
tion, because of syntrophic interactions between community
members, what species of bacteria colonizes the gut will have
an important effect on the final mixture of fermentation
end-products, and will thus determine which syntrophs are
likely to flourish, which in turn will affect the growth and
activity of other bacterial fermenters (Fischbach and Sonnen-
burg 2012). Priority effects in community assembly theory
suggest that the successional pattern of a community can be
strongly influenced by the taxa that are first to establish (Law
and Morton 1993). As the gut microbiota develops from an
initial maternal inoculation at birth, there is likely a mater-
nal effect on its developmental trajectory (Amato 2016).
Supporting this hypothesis, infants delivered via C-section,
which are inoculated by skin microbes, exhibit patterns of
gut microbial succession different from those of infants born
vaginally (Dominguez-Bello et al. 2010). e community
assembly may further be affected by host genotype, which
determines how susceptible a host is to initial colonization by
particular microbes (Amato 2016).
As in other communities, interspecies interactions such
as cooperation or competition exist within the gut micro-
biota, and may have an impact on the structure of the whole
microbial community (Porter and Martens 2016). For exam-
ple, Rakoff-Nahoum et al. (2016) revealed that the promi-
nent human gut symbiont Bacteroides ovatus releases large
together, systematically excluding clades that prosper
poorly in the mouse gut (Seedorf et al. 2014). An increas-
ing number of studies are stressing the importance of host
genetic background in structuring this core gut microbiota.
In mice, for example, the gut microbial composition dif-
fers between genetic lines (Buhnik-Rosenblau et al. 2011),
and between mice that are genetically predisposed or not
to obesity (Ley et al. 2006, Turnbaugh et al. 2006). In
humans, monozygotic twins living separately exhibit more
similar gut microbiota than domestic partners (Zoetendal
et al. 2001), and monozygotic twins share more of the same
types of microbes than dizygotic twins (Goodrich et al.
2014). Interestingly, the study of Goodrich et al. (2014)
revealed that the most heritable bacterial taxa within the
human gut microbiota are those associated with important
metabolic functions, such as fat deposition and weight
gain. ere is increasing evidence that host genetic con-
trol over the gut microbiota relies on the intercession of
the immune system (Ostaff et al. 2013). Shotgun meta-
genomics data from the Human Microbiome Project has
e.g. revealed associations between microbiota composition
and host genetic variation, especially in genes involved in
immunity pathways (Blekhman et al. 2015). In many spe-
cies, the balanced relationship with microbes depends on
a complex and multileveled intestinal barrier that involves
an intricate immune strategy network (Box 2). e intesti-
nal epithelium, as the outermost cell layer, constitutes the
first line of defense, ensuring the elimination of pathogens
while maintaining a coexistence with mutualistic partners
(Belkaid and Hand 2014, Gilbert et al. 2015). AMPs (Box
1), natural antibiotics produced in the gut of most animals,
are of particular importance in shaping the gut microbiota,
in both vertebrate and invertebrate species (Franzenburg
et al. 2013, Ostaff et al. 2013, Tasiemski et al. 2015).
When their expression is reduced, either experimentally
or in the context of immune deficiencies, it results in a
dramatic alteration of gut microbial communities (Ostaff
et al. 2013). Although their mode of action does not rely
on the recognition of specific molecules at the cell surface
of microorganisms, AMPs control symbiosis by selectively
killing specific bacterial taxa, while being inoffensive for
other ones (Tasiemski et al. 2015). e interplay between
the suite of AMPs expressed by the host and profile of AMP
susceptibility of different community members thus likely
play an important role in shaping the composition of the
gut microbiota (Broderick and Lemaitre 2012).
e flexible microbial pool is largely influenced by the
diet, which can induce important changes in the microbial
composition over short periods of time (Spor et al. 2011).
For example, in humans, historical shifts from plant-based
diet to meat-based diet have been followed by strong shifts
in the gut microbial community, with an increase in ani-
mal protein metabolizing bacteria and a decrease in bacte-
ria that metabolize dietary plant saccharides (David et al.
2014). Furthermore, the infant gut community assembly
undergoes discrete steps of bacterial succession punctuated
by life events. e earliest microbiome is enriched in genes
facilitating lactate utilization and genes involved in plant
polysaccharide metabolism are present before the introduc-
tion of solid food, priming the infant gut for an adult diet.
e introduction of solid food in the diet, however, causes
EV-11
to the dysbioses reported in ulcerative colitis and Crohn’s
disease patients.
Interaction network between bacterial, viral, archaeal and
fungal members of the community
Although most information on gut microbiota in the lit-
erature concerns bacteria, they are not the only inhabitants
of the guts. Other members of the community, such as
archaea, fungi and viruses, likely play a crucial role in the
structure and functioning of the gut microbiota (Fischbach
and Sonnenburg 2012, Ogilvie and Jones 2015). e differ-
ent members of the community are for example engaged in
syntrophic interactions, whereby each microorganism lives
off the metabolic or waste products of its predecessor. In
such association, the producer is dependent on the activi-
ties of the consumer, and vice versa (Dolfing 2014). Even
in cases where two communities harbor the same bacte-
rial strains (i.e. the same set of bacterial genes), the func-
tions carried out by bacteria may differ greatly, depending
on the presence or absence of other community members,
such as archaea (Fischbach and Sonnenburg 2012). As an
example, fermentation of dietary fiber involves syntrophic
interactions between microbes linked in a metabolic food
web: primary bacterial fermenters (i.e. Bacteroidetes and
amounts of inulin (a dietary fiber) digestion products via
a pair of dedicated cross-feeding secreted enzymes that are
unnecessary for its own use of inulin. ese enzymes allow
for cooperation with cross-fed species (e.g. Bacteroides vulga-
tus), which provide benefits in return. Other inulin-degrad-
ing bacteria like Bacteroides fragilis, however, exhibited a
more selfish behavior, generating far fewer inulin degrada-
tion products, and did not promote the growth of non-
inulin degrading bacteria. Such selfish behavior may
thus lead to dysbioses in the gut microbiota, with poten-
tial negative impacts on the hosts fitness, as exemplified
by the microbiota disruption associated with inflamma-
tory bowel disease (IBD) in humans (Tailford et al. 2015).
Some bacteria in the gut are able to degrade mucin, a pro-
tein that is abundant in the outer layer of mucus covering
the gastrointestinal tract epithelial cells. e degradation of
mucins results in the liberation of sialic acid, that becomes
available as a nutrient source for other bacteria of the com-
munity (Tailford et al. 2015). It was shown that Ruminococ-
cus gnavus, a mucin-degrading bacteria that is present in
the gastro-intestinal tract of 90% of humans, but is over-
represented in IBD, does not release sialic acid, but another
compound that cannot be used by other bacteria. is ‘self-
ish’ behavior of mucosal glycan utilization could contribute
Box 2
Gut microbiota and host immunity (see also Fig. 4 adapted from Renz et al. 2012)
After birth, developmental (such as formation of intestinal crypt and crypt based Paneth cells) combined with microbial
signals issued from the bacterial colonization of the intestine, drive significant changes of the intestinal epithelial cells
which start to rapidly proliferate and to produce a complex mucus layer protecting the gastrointestinal tract from potential
invasion (Renz et al. 2012). e gut microbiota shapes the innate and adaptive immune system which in turn controls
the microbiota from over-proliferation and invasion of the intestinal tissue. Immunity is the guardian of the host gut
environment, it coordinates cellular and biochemical responses through the epithelial cells, creating a robust equilibrium
between the healthy host and its normal microbiota (i.e. intestinal homeostasis). Many of these mechanisms are controlled
by PRR signaling (Box 1) induced by the recognition of the MAMPs produced by commensal microbes. e intestinal
reactivity to microbial sensing takes place after birth after a period of tolerance of the microbiota. In the small intestine,
Paneth cells derived AMPs (Box 1) such as defensins are induced upon PRR stimulation by commensal microbes. AMPs
are important in controlling and selecting microbiota as evidenced in defensin-deficient mice (Salzman et al. 2010). Local
concentrations of microbiota-derived metabolites also build the myeloid landscape not only in intestinal tissues, but also
systemically (Zhang et al. 2015). Microbiota driven modification in the myeloid cell pool increases the host susceptibility
to infection, sepsis, allergy and asthma (Hill et al. 2012, Fonseca et al. 2015, aiss et al. 2016). Conversely, immune
signals stemming from commensal microorganisms also influence the proper tissue-dependent functioning of innate
lymphoid cells (ILC) (Honda and Littman 2016). Tissue resident ILCs integrate signals from microbiota to link and
refine the innate and adaptive response at the tissue level. ILC3 1) produces Tumor Necrosis Factor b (TNFb) which
is crucial for microbiota homeostasis and production of IgA, 2) contributes to the differentiation of T cells and B cells
and 3) promotes the expansion of T
reg cells (Box 1) in the intestinal mucosa. e production of IgA by the gut plasma
cells is the result of the mucosal adaptive immunity (Honda and Littman 2016). Plasma cells producing IgA (Box 1) are
only generated after birth to provide SIgA to the lumen, maternal SIgA is provided by breast milk during the postnatal
period. e gut microbiota modifies the accumulation of IgA-expressing cells as well as the level and diversity of IgA in
the lumen (omas 2016). Interestingly, some members of the microbiota, such as Sutterella species, reduce the level of
IgA by degrading them (Moon et al. 2015) while others such as segmented filamentous bacteria (SFB), which colonize the
surface of the epithelium, activate their production through the T-cell independent pathway (Ivanov and Littman 2010).
e type of bacteria targeted by IgA differs according to the diet of the host (Kau et al. 2015) supporting the trialogue
that exists between the host, the microbiota and environmental factors. is trialogue is also sustained by the ‘hygiene
hypothesis’ (Box 1).
EV-12
factor contributing to the stability and the resilience of the
gut microbiota.
The role of the microbiome in host ecology and
evolution
Effects of variation in gut microbiota at the individual level
Unlike the host genome, the flexible microbiome can change
rapidly as a result of modifications in either the composi-
tion of the microbial community or individual microbial
genomes, resulting in modified transcriptomic, proteomic
and metabolic profiles (Sommer and Bäckhed 2013). Gut
microbiota thus represents an important source of metabolic
flexibility that can allow its host to rapidly acquire a pheno-
type that is adapted to current environmental conditions. As
such, the gut microbiota might be a key, yet understudied,
factor driving fast acclimatization to new environments and
resistance to habitat disturbance. is can be particularly
important in the current context of global climate change
and of intense anthropogenic activities, which impose fast
and drastic environmental changes to which organisms do
not necessarily have the time to adapt (Gilbert et al. 2015).
Contrary to vertically transmitted symbionts, which pro-
mote coevolution and optimization of host–symbiont inter-
actions, but can also prevent interactions of symbionts with
the environment and reduce their adaptive potential, the gut
microbiota has the unique property to be highly flexible and
interactive. rough horizontal transfer and recruitment of
bacteria from the environment, the gut microbiota repre-
sents a huge genetic and functional diversity, with a high
potential for adaptation, and provide the host with an almost
unlimited set of metabolic functions (Shapira 2016; Fig. 2).
e advantage of exchanging symbionts with the environ-
ment is illustrated by the bean bug Riptortus pedestris, which
has developed insecticide resistance through the acquisition
of insecticide-degrading bacteria from the soil (Kikuchi et al.
2012). In addition to this ability to recruit environmental
bacteria, the gut microbial community can rapidly respond
to changes in host diet or environmental conditions through
variation in the relative abundance of resident bacteria, a
process which is facilitated by the high genetic diversity and
the short generation time of gut microbes (Bordenstein and
eis 2015). For example, in the herbivorous desert wood-
rat, animals fed toxic plants show a shift in the composition
of their gut microbial community, with an increase in the
abundance of bacterial genes that metabolize toxic com-
pounds, compared to animals fed non-toxic plants (Kohl and
Dearing 2012). e responsiveness of the gut microbiota is
further increased by the fast evolution of bacteria, through
either horizontal gene transfer or mutations that increases
both genetic and functional diversity of the microbial com-
munity (Dillon and Dillon 2004). For example, in Japanese
populations that regularly consume red algae in sushi and
other foods, the gut bacterium Bacteroides plebeius acquired
the capability, through lateral gene transfer from environ-
mental marine bacteria, to degrade the polysaccharides of
marine red algae (Hehemann et al. 2010). Mutations in
members of the gut microbiota can also change interactions
with parasites. For example, experimental evolution of the
tripartite interaction between C. elegans and two of its patho-
gens revealed that the low pathogenic bacteria Enterococcus
Firmicutes) generate SCFAs, other organic acids (e.g. for-
mate) and gases such as hydrogen (H2) and carbon diox-
ide (CO2). Accumulation of H2 inhibits bacterial NADH
dehydrogenases, thereby reducing the yield of ATP. is H2
is removed by means of archaeal methanogenesis, resulting
in improved fermentation efficiency (Samuel and Gordon
2006). Furthermore, colonization of germ-free mice with
Bacteroides thetaiotaomicron (bacterial fermenter), with or
without the archaea Methanobrevibacter smithii, revealed
that the presence of M. smithii decreases the carbohydrate
fermentation activity of B. thetaiotaomicron, while increas-
ing the fermentation of fructans (fructose polymers), the
by-products of which are used by M. smithii for methano-
genesis (Samuel and Gordon 2006). Bacteriodes thetaiotao-
micronM. smithii co-colonization also produced an increase
in host adiposity compared with mono-associated animals.
ese findings demonstrate a link between this archaeon,
prioritized bacterial utilization of polysaccharides, and host
energy balance.
Another component of the gut microbiome that is often
neglected is the gut virome, which can be defined as the
community of viruses associated with the gut microbial
community. Although information on the gut virome is
limited compared to that on gut bacteria, current evidence
suggests that it may play an important role in modulating
gut microbiota structure and function (Ogilvie and Jones
2015). Given the predominance of bacteria in the gut micro-
biota, the gut virome is usually dominated by prokaryotic
viruses, i.e. bacteriophages, which mostly have a temperate
lifestyle (i.e. they integrate into bacterial host chromosomes
as prophages and propagate through lysogenic cycles, or
exist as quiescent episomal elements without lytic replica-
tion) (Breitbart et al. 2003, Ogilvie and Jones 2015, Murall
et al. 2017). ese temperate phages are important for the
exchange of genetic material between bacterial hosts (trans-
duction), and themselves encode a rich functional repertoire
that confers a range of attributes to their bacterial hosts,
including toxin synthesis, production of virulence factors
and metabolic flexibility (Minot et al. 2011, Reyes et al.
2012, Modi et al. 2013, Ogilvie and Jones 2015). Meta-
genomic surveys of gut viruses have revealed an important
number of genes involved in energy harvest (e.g. carbohy-
drate and amino acid metabolism; Reyes et al. 2010, Minot
et al. 2011), suggesting that phages may confer important
metabolic capabilities to their bacterial host, which may in
turn indirectly affect animal host metabolism. e genes
encoded by the viral genome may thus expand the niche
of gut bacteria, and strongly affect the dynamics of the gut
microbial community. Furthermore, phages may consti-
tute a genetic reservoir for bacterial adaptation, safeguard-
ing important functions and facilitating the recovery of the
community in case of disruption (Ogilvie and Jones 2015).
Consistent with this hypothesis, a study performed in mice
revealed that antibiotic treatment leads to the enrichment
of phage-encoded genes that confer antibiotic resistance,
as well as genes involved in gut colonization and growth,
indicating that the phageome becomes enriched for func-
tionally beneficial genes under stress-related conditions
(Modi et al. 2013; but see Enault et al. 2016 on the possible
overestimation of phage-related antibiotic resistance in viral
metagenome studies). Phages may thus be an important
EV-13
borer (Ceja-Navarro et al. 2015) and the desert woodrat
(Kohl et al. 2014). Although these studies suggest that gut
symbionts constitute a crucial factor mediating host plant
specialization in herbivorous species, they do not document
the evolutionary processes leading to such adaptation. One
of the few studies documenting the role of gut symbionts
in the process of adaptation is that of Kohl et al. (2016),
which shows that experimental evolution on bank voles
Myodes glareolus for increased herbivorous capabilities results
in the concomitant evolution of gut microbial communities.
Another example is that of the western corn rootworm, in
which the gut microbiota was shown to mediate adaptation
to human-driven landscape changes. is major crop pest,
that has been controlled via annual rotation between corn
and non-host soybean, has evolved to a “rotation-resistant”
variant with a shifted gut microbiota composition that
increases tolerance to anti-herbivory defenses of the new
host plant (Chu et al. 2013).
Selection on symbiont-mediated traits promoting adap-
tation to local environmental conditions can result in a rapid
evolution of host genes (especially immune genes) involved
in acquisition, control and tolerance of beneficial symbionts,
allowing for an indirect co-inheritance of nuclear genes and
microbes (Vavre and Kremer 2014, Bordenstein and eis
2015). While genes involved in immune defense are among
the fastest evolving in the genome of many species, as a result
of a coevolutionary arms race between hosts and pathogens
(Decaestecker et al. 2007), genes encoding AMPs have been
shown to evolve more slowly than average and to exhibit
high rates of non-synonymous polymorphisms (Unckless
and Lazzaro 2016). Studies performed in both invertebrates
(Unckless et al. 2016) and vertebrates further revealed that
these non-synonymous mutations strongly affect the anti-
bacterial activity of AMPs and thus resistance to bacterial
infection (Tennessen et al. 2009). In diverse species includ-
ing Drosophila, marine mussels, frogs, birds and humans,
AMP polymorphism has been suggested to be maintained
through balancing selection, driven by fluctuation in natu-
ral selective pressure over time and/or geographical space
(Tennessen and Blouin 2008, Unckless and Lazzaro 2016).
is may be mediated by shifting diversity of pathogens, as
well as by correlated life-history costs of overactive immune
systems (Unckless and Lazzaro 2016). For example in frogs,
differences in the expression and activity of antimicrobial
skin peptide across geographically distinct populations was
suggested to reflect current and past encounters of these
populations with different skin pathogens (Tennessen and
Blouin 2008). As AMPs have a role in the control of gut
microbiota, it might also be that balancing selection on
AMPs results from fluctuating environmental conditions
that exert different selective pressures on the gut microbi-
ota composition. Variation in AMPs could thus contribute
importantly to the ability of animal hosts to adapt to chang-
ing environments through adaptive changes of their symbi-
otic communities. In addition to act on immunity, selection
can further act on genetically heritable traits or behaviors,
such as egg-smearing or coprophagy, which encourages the
acquisition and/or vertical transmission of specific beneficial
symbionts. Although not acting on the gut microbiota itself,
such selective processes would result in heritable microbial
traits (Amato 2016).
faecalis rapidly evolved the ability to suppress its competitor,
the highly pathogenic Staphylococcus aureus, through muta-
tions associated with an increased production of antimicro-
bial superoxide (King et al. 2016).
e microbial facilitation of host dietary flexibility and
resistance to pathogens may support host expansion into
new habitats. Even in humans, dispersal and the ability to
colonize the most extreme regions on Earth might have been
mediated by gut symbionts. In this sense, the gut microbiota
can contribute to determining the geographical range in
which a species will be able to establish. In primates, such
as howler monkeys, microbiota of species with distinct rang-
ing patterns suggest that more diverse gut microbial com-
munities are associated with wider geographical distribution,
supporting the idea that more flexible microbiota increase
colonization abilities (Amato 2016). In addition, when dif-
ferent species, or different populations of an invasive species,
come into contact, the opportunity for horizontal transmis-
sion of gut symbionts arises, which can result in ad hoc acqui-
sition of new traits, which in turn can enhance the invasive
potential of host species (Feldhaar 2011). Such hypotheses,
however, remain to be investigated.
Not all variation in gut microbiota composition is how-
ever beneficial to the host. Given that the fitness of hosts
and gut microbes are not always aligned, a conflict might
exist and result in a negative outcome for the parties involved
(Wasielewski et al. 2016). e western diet, characterized by
a paucity of fermentable carbohydrates, has for example been
shown to select for a community of microbes that eat host-
derived carbohydrates found in the intestinal mucus layer,
resulting in mucus layer thinning. By increasing microbial
colonization and translocation into host tissues, such mucus
thinning can interfere with the normal absorptive func-
tion of epithelial microvilli, and induce inflammation and
colitis (Sonnenburg and Sonnenburg 2014, Wasielewski
et al. 2016). ere is increasing evidence that dysbioses in
the gut microbiota are involved in human diseases, such as
inflammatory bowel disease and obesity (Belkaid and Hand
2014).
The core gut microbiota as an extended phenotype that
promotes adaptation
Although strong empirical evidence is still lacking, the gut
microbiota is increasingly hypothesized to contribute to
host evolution and adaptation to the environment (Gilbert
et al. 2015). e strongest evidence of symbiont-mediated
adaptation comes from intracellular, vertically transmitted,
endosymbionts in herbivorous species, which have been
shown to mediate host-plant specialization. For example,
the pea aphid Acyrthosiphon pisum encompasses ecologically
and genetically distinct host races that are locally adapted to
their respective host plants (red clover or alfalfa), while being
unable to reproduce on the other host plant. is instance
of host-plant specialization has long been attributed to chro-
mosomal loci of the aphid, but recent studies revealed that
it is in fact mainly mediated by bacterial endosymbionts
(Tsuchida et al. 2004). Information concerning the role of
gut microbes in host adaptation is more limited, and would
deserve further investigation in future studies. e gut
microbiota was shown to mediate the ability of herbivorous
species to feed on toxic plants, as exemplified by the coffee
EV-14
and that a coevolution occurred. By definition, coevolution
requires that each lineage undergoes evolutionary change
due to selective forces imposed by the other lineages. e
reciprocal impacts on fitness and speciation are, however,
usually not known, hence nothing really proves that cospe-
ciation occurred. At the extreme opposite, organisms that
do not interact at all could diversify in parallel if subjected
to the same series of geographic isolation events. Another
hypothesis is that codiversification reflects unidirectional
selection. For example, as host lineages evolve, they may shift
in their selectivity to pick-up bacteria from the environment,
reflecting an evolution of mechanisms underlying microbial
community assembly in the host, e.g. the evolution of host
immune genes resulting in the recruitment of different sym-
bionts from the environment. ese hypotheses, however,
remain theoretical, and would need to be tested experimen-
tally. For example, germ-free animals from different host lin-
eages could be exposed to a same microbial inoculum, to see
if the community assembly differs among lineages. Recipro-
cal transplant experiments between related hosts could also
be performed, to measure the impacts on both host and
microbial fitness.
Generally, due to the fact that host–microbes interactions
are labile and dependent on environmental conditions, the
room for host–microbiota coevolution is thought to be more
limited than for endosymbionts (Moran and Sloan 2015).
Especially, co-evolution can only occur if the host-associated
phase is predominant in the symbiont’s life-cycle. e strength
of selection on microbes to benefit their host, and on hosts
to maintain a favorable niche for their symbionts, is expected
to depend on the tightness of the mutualistic relation and
on how the interests of the host and of the symbionts are
aligned. From the symbiont perspective, microbe-mediated
protection of the host can be directly favored when micro-
bial fitness strongly depends on host fitness, such as when
microbes are vertically transmitted, or when the host selec-
tively recruit beneficial symbionts, e.g. through immunity.
From the host perspective, behavioral or physiological traits
involved in the recruitment and the maintenance of symbi-
onts will be favored if the benefits provided by the symbionts
outweigh any cost (Ford and King 2016).
When hosts and symbionts are tightly linked, both hosts
and symbionts may become dependent on their mutualistic
partner to ensure some functions, which may lead to gene
and function loss, especially if the function is costly to per-
form. is function must provide an indispensable public
good, necessitating its retention by at least a subset of the
individuals in the community - one cannot play Hearts
without a queen of spades (Black Queen hypothesis, BQH,
Morris 2015). Any function that is both costly to perform
and leaky (e.g. nutrient acquisition, biofilm matrix deposi-
tion, nitrogen fixation) is a potential target for function loss
in the framework of the BQH (Morris et al. 2012). Many
host-associated bacteria have e.g. lost the capacity to syn-
thesize essential metabolites, such as amino acids, provided
by their host or by other microbes of the community. Hosts
have also evolved dependency on their gut microbes, some-
times resulting in the evolution of specialized anatomical
structures aiming at housing the microbes and facilitat-
ing their activity (Engel and Moran 2013, Shapira 2016).
Mammalian herbivores and sap-feeding insects have become
Gut microbiota can promote divergence of host lineages
and speciation
Selection for symbiont-mediated traits adapted to the local
environment can lead to dramatic changes in gut microbial
communities over short periods of time, within both indi-
viduals and populations. Consequently, selective pressure
on the host to control and tolerate beneficial symbionts can
change, fostering a rapid evolution of host immune or devel-
opmental genes. Hybrids of populations exhibiting different
gut microbial communities may thus suffer from a decreased
fitness, favoring the emergence of post-zygotic barriers and
differentiation between populations (Vavre and Kremer 2014,
Shapira 2016). Consistent with this hypothesis, hybrids
of two closely related Nasonia species with distinct micro-
biota are non-viable, and show altered microbiota. When
reared under germ-free conditions, however, hybrid viability
is restored (Brucker and Bordenstein 2012). Similarly, in
Drosophila (Miller et al. 2010) and Nasonia (Chafee et al.
2011), hybrid sterility has been associated with the over-
proliferation of symbionts in male testes, which may reflect
perturbation of the interaction between symbionts and genes
involved in the control of symbiotic populations (Vavre and
Kremer 2014). In addition, symbiont-mediated changes in
host behavior, such as mate preference, may reduce gene
flow between individuals or populations harboring differ-
ent microbiota, fostering reproductive isolation (Vavre and
Kremer 2014). us, divergence of host lineages living in
different environments and species diversification may be
facilitated by the microbiota.
Coevolutionary dynamics between hosts and their
symbionts
Similarities in gut microbiomes are often observed between
related species, suggesting a high specificity between hosts
and their symbionts (Bordenstein and eis 2015). A
recent study in hominids suggests that multiple lineages of
the predominant gut bacteria arose via cospeciation with
humans, chimpanzees, bonobos and gorillas over the past
15 million years (Moeller et al. 2016). Especially, the clades
Bacteroidaceae and Bifidobacteriaceae have been maintained
exclusively within host lineages, and their divergence times
are congruent with those of hominids, suggesting that nuclear
and gut microbial genomes diversified in concert during
hominid evolution. In contrast, for Lachnospiraceae, several
between-host-species transfer events occurred since the com-
mon ancestor of the Hominidae. Interestingly, the Lachno-
spiraceae, unlike Bacteroidaceae and Bifidobacteriaceae, are
spore-forming and can survive outside the gut, which may
enhance their ability to disperse and transfer among host
species. ese results suggest that gut microbiomes are com-
posites of cospeciating species, which are highly specific to
their host, and independently diversifying bacterial lineages,
which are less strongly linked to a particular host and can
be shared among different host species. Similarly, in Nasonia
wasps, the pattern of phylogenetic branching of gut symbi-
onts were shown to mirror that of their host, a phenomenon
that is sometimes referred to as “phylosymbiosis” (Brucker
and Bordenstein 2012). However, as explained by Moran
and Sloan (2015), phylosymbiosis should be interpreted
with caution. It is indeed tempting to conclude that hosts
and their gut symbionts have a shared evolutionary history,
EV-15
Over evolutionary time, a host may thus become dependent
on microbe-mediated protection, a hypothesis that has been
invoked to explain the loss of immune genes in pea aphids
and honeybees (Gerardo et al. 2010, Kaltenpoth and Engl
2014). Finally, gut symbionts can shape the evolution of par-
asite virulence, through mechanisms similar to interactions
occurring between co-infecting parasites, such as resource
competition, interference competition or immune media-
tion. is principle may be extended to interactions other
than host–parasite coevolution, such as plant–insect coevo-
lution, and may be valuable for a more realistic understand-
ing of coevolutionary processes.
rough the horizontal transfer of bacteria, species or
populations of the same species can affect the fitness, and thus
potentially the evolution, of each other (Feldhaar 2011). Gut
symbionts can also act as ecosystem engineers and contrib-
ute to modifying the biotic and abiotic environment of their
host, potentially affecting other species of the community.
For example, by contributing to food digestion, gut symbi-
onts play a major role in the food web and can contribute to
the stability of the whole community. If we push this reason-
ing to its extreme, one could even argue that gut microbes
might play a non-negligible role in shaping landscapes. For
instance, the African savanna ecosystem, characterized by
grasses and small dispersed trees, is controlled by the climate,
but also by the dynamics of herbivorous animal populations,
which are themselves controlled by predators. Without the
appropriate set of gut symbionts, herbivorous species would
be unable to consume plants, which would result in very
different vegetation types, and savanna might thus not exist,
replaced by more arborous vegetation. In the same way, by
allowing soil animals to decompose dead organic matter,
gut microbes are major players of nutrient recycling. More
precisely, the microbiome can change host phenotype and,
via an eco-evolutionary loop (Fig. 3), it can also affect the
environment via niche diversification and construction. In
particular, developmental symbiosis and plasticity – the
ability of larval or embryonic organisms to react to environ-
mental input with a change in form, physiology or behavior
has been described as leading to ecosystem engineering,
given that such plasticity can provide the phenotypic ranges
within which animals can accommodate to environmental
challenges such as climate change (Gilbert et al. 2015).
As recently highlighted in a review by Amsellem et al.
(2017), the gut microbiota likely plays a role in the pro-
cess of biological invasions, i.e. when non-indigenous spe-
cies expand their range in their newly introduced habitat,
inducing perturbations in the structure and population
dynamics of the recipient community. e microorganisms
hosted by alien species can for example facilitate invasion,
if they provide a selective advantage for the invasive hosts
over native ones (Lymbery et al. 2014, Strauss et al. 2012,
Amsellem et al. 2017). is may occur, for instance, when
alien species harbor mutualist symbionts that are more effi-
cient than those of native populations, or when they harbor
pathogens that are tolerated by the invasive carrier but can
affect or kill native competitors in newly colonized habitats
(i.e. “spill-over” phenomenon, resulting from the fact that
parasites are more virulent in new hosts because of a lack of
evolved immunological resistance; Power and Mitchell 2004,
Amsellem et al. 2017). Parasite spillover has for example
dependent on plant-degrading microbes, for which they have
evolved specialized gut structures, such as the rumen that
serves as a fermentation chamber in cows. Such adaptations
arose independently during evolution, resulting in distinct
anatomical structures, but resemble each other in microbial
composition, suggesting that microbes are adapted to some
shared functional characteristics of their niche.
Impacts of gut microbes on the eco-evolutionary dynamics
of the host community
Recently, there has been considerable interest in the interac-
tion of ecological and evolutionary dynamics in an attempt
to understand them as coupled ‘eco-evo’ processes. Such eco-
evolutionary feedbacks can occur at multiple levels, such as
in demographic parameters, community composition, food
webs, nutrient cycling and productivity (Hairston et al.
2005, Urban et al. 2008, Pelletier et al. 2009, Hiltunen
and Becks 2014, Govaert et al. 2016, Hendry 2016). At the
population level, natural selection and population dynam-
ics are closely linked because both are affected by the birth
and death of individuals. us, if natural selection acts on
a trait through survival or reproductive success, it will leave
a population dynamical signature. At a larger scale, changes
in the genetic composition of a species can affect its fit-
ness dependencies with other species (e.g. through trophic
interactions or competition) and hence alter the ecologi-
cal dynamics of an ecosystem, and vice versa. Given that
the gut microbiota is a crucial mediator of host physiology
and behavior, and thus of life-history, we here propose that
it may be an important piece missing in eco-evolutionary
dynamics theory.
rough its effects on reproduction, survival and disper-
sal, the gut microbiota can affect population dynamics and
genetic diversity, and thus play a role in eco-evolutionary
feedbacks. Moreover, by mediating interactions between
hosts and other organisms, such as parasites, predators or
plants in herbivores, gut symbionts can play a direct role in
the process of coevolution between these species. So far, most
models and laboratory experiments investigating coevo-
lution processes, such as the Red Queen hypothesis, have
been based on pairwise-species interactions (Decaestecker
et al. 2007, 2013, Salathé et al. 2008, Lively et al. 2014).
However, in natural environments a lot of factors, such as
complex species interaction networks may constrain coevo-
lution, and should thus be more systematically considered
in future research (Koskella and Brockhurst 2014). By com-
bining knowledge of defensive microbe–parasite interactions
at the mechanistic level with evolutionary theory, Ford and
King (2016) predict how defensive microbes might alter the
evolution of host and parasite traits, such as resistance and
virulence, which in turn might greatly affect host popula-
tion dynamics. First, a direct coevolution between defensive
microbes and parasites would provide ‘real time’ control of
the infection, whereby evolutionary changes in parasites are
met by rapid reciprocal evolution in defensive microbes.
Second, given that defensive microbes protect hosts from
parasite-induced fitness costs, they could reduce selection for
costly immune or behavioural defense mechanisms in the
host. Consistent with this, Trachymyrmex ant populations
harbouring protective antibiotic-producing bacteria exhibit
reduced cleaning behaviour (Fernández-Marín et al. 2009).
EV-16
Other species, like the freshwater crustacean Daphnia, may
offer an interesting alternative to the mouse and Drosophila
models. Indeed, their high experimental tractability, short
life cycle, clonal reproduction and high responsiveness to
environmental stressors, combined with the possibility to
easily manipulate their gut microbiota and an absence of
ethic restrictions, provide a unique opportunity to study the
interactions between genotype, innate immune system, envi-
ronment and microbiota, with a high degree of experimental
control (Callens et al. 2016).
To connect microbiota studies with the coevolution of
hosts and their symbionts, we think it is also necessary to
sharpen our observations of microbiota dynamics. Even
though the processes by which microbiota can be horizon-
tally or vertically transmitted from one host to the next are the
same for all its constituting microbes, the ability of microbes
to infect new hosts may vary (Seedorf et al. 2014). More-
over, different microbes’ fitness may benefit differently from
the within-host and environmental parts of their life cycles.
Caution should be warranted when interpreting the results
of host-microbiota coevolution experiments as different
means of microbiota transfer and different pace of host life
cycle might positively select different microbial taxa. Despite
the powerful genomic tools available, our knowledge regard-
ing the functional capacities of gut microorganisms and how
their genetic variation influences their ability to colonize
the gut remains limited. Recently, Yaung et al. (2015) used
an approach termed Temporal FUnctional Metagenomics
sequencing” (TFUMseq) to identify genetic regions that
increase microbial fitness in the mammalian intestine, and
thus contribute to colonization success. To determine if con-
stitutively expressed genetic loci from Bacteroides thetaiotao-
micron modulate the ability of Escherichia coli to colonize
the mammalian intestine, they inoculated germfree animals
with E. coli harboring plasmids from a library covering the
whole genome of B. thetaiotaomicron and tracked the abun-
dance of B. thetaiotaomicron genes over time by sequencing
DNA samples from fecal pellets at different time points.
Applied to different recipient mouse strains, or to already
colonized animals, this method may allow disentangling the
influence of host organism genome, or of other microbes, on
the competitive profile of the targeted bacterial genes.
Estimate the fitness returns from the symbiotic
relationship for both hosts and symbionts
To predict the evolutionary consequences of host–microbi-
ota interactions, it is important to determine how far both
hosts and symbionts draw a benefit from this relationship.
Microbial fitness is still poorly assessed in the literature,
which impedes any exploration of the correlations between
host and symbiont fitness. Methods do exist to measure
and compare microbial fitness between hosts, in space or in
time, e.g. by measuring infectivity in time-shift experiments
(Koskella 2014). Collecting and freezing microbiota at dif-
ferent points during a host–symbiont coevolutionary experi-
ment, together with reciprocal microbiota inoculations,
could help assess local adaptation of symbionts to their host
following the general methodology of Red Queen studies
(Gandon et al. 2008).
From the host point of view, there is generally a lack of
connections between evolutionary and functional questions
been shown to occur between commercially produced bum-
blebees and honeybees and wild bumblebee populations,
contributing to the decline of the latter (Fürst et al. 2014,
Graystock et al. 2014). Conversely, the lack of appropriate
mutualistic symbionts can be a major constraint to the estab-
lishment of alien species. e success of exotic invaders may
also depend on the microorganisms hosted by native popula-
tions (Amsellem et al. 2017). While the horizontal transfer
of beneficial mutualistic symbionts from native species can
facilitate adaptation of alien species to their new habitat,
the acquisition of native parasites may hamper the invasion
process. e loss of microorganisms sometimes observed
in introduced populations, resulting from either sampling
effect (introduced hosts are by chance not infected) or an
absence of conditions required for microorganisms growth
in the introduction area, can further affect their invasive-
ness (Amsellem et al. 2017). e loss of pathogens has for
example been shown to facilitate invasion in mosquito (Alia-
badi and Juliano 2002). In contrast, the loss of mutualists is
expected to negatively affect the invasive potential of alien
species (Amsellem et al. 2017).
Perspectives for future research on the role of the
gut microbiota in ecology and evolution
Shifting from a proximate to an integrative view of
host–microbiota interactions
Although studies on gut microbiota are currently boom-
ing, many essential details about the reciprocal interactions
between host physiology, gut microbiota and environmental
factors remain to be discovered. e gut microbiota is often
considered as a single entity, even sometimes referred to as
a novel “organ” (Guinane and Cotter 2013), a representa-
tion that is erroneous and may lead to a certain confusion.
e gut microbiota is indeed far more complex, and should
rather be considered as an ecological community involv-
ing an interacting network of species. e diverse players of
this network include microorganisms (e.g. bacteria, yeast,
fungi), viruses and bacteriophages, but also host cells (as the
physical environment and as resources) and immune factors
(Murall et al. 2017). is community is strongly dependent
on external (e.g. diet) and host (e.g. genetic background) fac-
tors, thus leading to high inter-individual variability (Murall
et al. 2017). Given this complexity, studies are often limited
to only a subset of players involved in gut microbiota func-
tioning, hence the mechanistic scheme underlying the estab-
lishment and the transmission of gut symbionts, as well as
their impacts on host physiology, remains incomplete. Deci-
phering these mechanisms is nevertheless very important to
understand the evolutionary dynamics of host–microbiota
interactions. ere is thus a need for more integrative stud-
ies that take all these factors into account, using a biological
model amenable to carefully controlled experiments. Excel-
lent resources are available to study such questions in vivo,
especially in mice and Drosophila, in which germ-free ani-
mals can easily be obtained, while the existence of a large
number of inbred isogenic lines allows controlling for the
host genetic background. In addition, their genome and their
immune system are well characterized, making these species
favorite models in the study of interactions between host
immunity, genotype and microbiota (Hooper et al. 2012).
EV-17
in the study of adaptation. is may for example be done
by removing gut symbionts with antibiotics, and determine
whether local adaptation patterns observed in the field per-
sist. It may also be done by performing experimental evo-
lution, under either germ-free or conventional conditions,
to determine whether the evolutionary trajectory will be
affected.
Despite its potential key role in driving adaptation to
changing environments, the evolutionary history of host–
microbiota associations has been poorly investigated so far.
One very constraining aspect is the difficulty to find well-
preserved fossil records of microbiota, and to study the
mechanisms underlying host–microbiota associations (e.g.
immune factors) in ancient organisms. Hence, evidence of
microbiota evolution is mainly indirect, coming e.g. from
the comparison between contemporary populations submit-
ted to different environments. For example, the putative tra-
jectory of human gut microbiota evolution from Paleolithic
hunter–gatherer to modern Western societies has recently
been traced by comparing the gut microbiota structure
of modern populations with different lifestyles (e.g. rural
African populations, western communities, etc.; Quercia
et al. 2014). However, the analysis of such snapshot spatial
patterns in gut microbiota structure does not provide infor-
mation about the evolutionary processes that have led to the
pattern observed in present-day populations. For instance, it
is unclear whether geographic variation in human gut micro-
biota structure results from host genetic evolution, or rather
reflects the flexibility of host–microbiota associations. A
powerful way of documenting the course of host–microbiota
evolution would be to study organisms, like Daphnia, that
produce temporally stratified dormant propagule banks. By
resuscitating past populations in the laboratory and compet-
ing isolates against their modern descendants, the function
and fitness effects of genes evolving in step with the changing
environment can be experimentally inferred (Decaestecker
et al. 2007, Orsini et al. 2013). Such resurrection studies can
be useful to investigate, e.g. the evolution of the immune sys-
tem and the consequences for the gut microbiota structure.
Another aspect which is linked to the study of microbiota
adaptation is the topology of the microbial interaction net-
work within the gut. Using an analogy with gene network
topology, the latter is thought to affect the speed of adapta-
tion to changing environments and maximal fitness in stable
ones, with simpler topologies allowing quicker adaptations
at the cost of poorer maximal performances (Malcom 2011a,
b). In the same vein, the topology of microbial interaction
networks should be investigated as a potential driver of adap-
tation to changing environments. e use of lab-tractable
host organisms with short generation times and well-studied
innate immune systems would facilitate experimentation to
test such ideas and allow determining whether particular
immune system components have been lost or are expressed
less over evolutionary time.
A gut microbiota perspective on life-history evolution and
eco-evolutionary dynamics
Classically, life-history traits, such as age at maturity, the
mode of reproduction or dispersal ability, have been con-
sidered ‘disconnected from the gut’, i.e. their evolution has
been mostly investigated in the light of population genetics,
on host–microbiota interactions. Although genomic tools
provide important information on the proximate mecha-
nisms through which microbiota may affect host fitness,
they mostly do not quantify the consequences on fitness
itself. Hence, in addition to studying how microbiota func-
tional profile changes in response to the environment and
how it affects host physiology, it is necessary to study how
such changes affect host life-history traits such as survival
or reproduction. Information we have regarding fitness
consequences for the host mainly comes from the compari-
son between germ-free and conventionalized animals, and
remains limited and sometimes inconsistent. For example
in Drosophila, the microbiota can increase lifespan in some
studies (Brummel et al. 2004) while other studies demon-
strate either negative effects (Petkau et al. 2014, Clark et al.
2015) or no effect (Ren et al. 2007) on lifespan. One pos-
sible explanation to such conflicting conclusions is that the
composition of the gut microbiome varied between studies,
likely due to differences in rearing conditions (Heintz and
Mair 2014). Such variation in experimental conditions can
have a great influence on the results obtained, thus ham-
pering the determination of fitness consequences of gut
microbiota. ere is thus a need of standardized microbiota
for reproducible experiments, otherwise we may face confu-
sion from variable results attributable to differences between
experimental microbiota (Hooper et al. 2012). Moreover,
cross-taxon studies investigating the functional consequences
of gut microbiota across host phylogeny can provide inter-
esting information on the link between microbiota, host
ecology and life history. So far, such studies have focused
on vertebrates (Ley et al. 2008, Sullam et al. 2012). ere
would be much to learn from generalizing these studies to
other groups, especially in order to assess the relative impor-
tance of diet and habitat on microbiota, and reciprocally of
microbiota on host diet and habitat. In the same vein, the
link between microbiota and the time since last shift in diet
in the focal host species has not been much investigated.
is could lead to interesting observations regarding the
hypotheses that recent changes in diet could be associated
with microbes that are still harmful to the host and/or that
such recent changes in diet actually occur because of a shift
in microbiota – through host manipulation or changes in
ontogeny for instance. Adapting models of trait evolution on
phylogenies (Garland et al. 1993, Paradis and Claude 2002,
Ives and Godfray 2006, Ives and Garland 2010) to models of
gut microbiota associations on host phylogenies, or extend-
ing the framework of co-phylogenetic studies (Banks and
Paterson 2005, Charleston and Perkins 2006, Conow et al.
2010, Drinkwater and Charleston 2014) to include whole
gut microbiota would help understand the link between
host–microbe evolutionary contact duration and the effect
of the microbe on the host.
Consider more systematically the gut microbiota in the
study of host fitness and adaptation
e capacity of animal populations to adapt to new environ-
ments has long been considered to rely on nuclear genes.
However, evidence is accumulating that some traits that
affect the fitness of an organism are not directly encoded in
the nuclear genome, but rather in the microbiome. e gut
microbiota should thus be considered more systematically
EV-18
Gut microbiota and its link to host specialization and
speciation
To understand the selective pressures and processes involved
in the evolution of symbiotic relationships, e.g. in the gut,
and their potential roles in the diversification of their hosts,
there is a need for studies of symbiosis diversification at a
short time-scale (Vavre and Kremer 2014). To understand
the processes driving host–microbiota coevolution, variation
in gut microbiota composition, as well as the mechanisms
underlying host–microbes interactions (e.g. immunity)
within species and between host races or closely related spe-
cies, should be investigated. Metatranscriptomics and meta-
genomics provide very useful and powerful tools to study
these questions, allowing to investigate the structural and
functional profile of gut microbial communities, and facili-
tating the detection of host and microbial genes involved in
local adaptation. It is not yet clear whether the genes revealed
by transcriptomics studies in the host are associated with the
regulation of the symbiotic compartment. Moreover, the
ultimate effect of these genes on host fitness is still to be
determined. A possibility would be that such genes select for
certain microbiota together with having effects on the life
cycle of the host, or could select microbiota which in turn have
an effect on its life cycle. Divergence in life cycles between
closely related hosts could lead to speciation by inducing
reproductive isolation through a mismatch in reproductive
timing or through outbreeding depression linked to another
part of the life cycles. e role of the microbiota in host
race formation (Feldhaar 2011) and speciation (Brucker and
Bordenstein 2012) is a process that needs further enquiry.
Reciprocal gut microbiota transplant between different host
races or closely related species might be a very useful tool
to assess the role of gut symbionts in species divergence. It
may also be interesting to investigate more deeply the role of
gut microbiota in hybrid lethality (or more generally hybrid
depression) in species such as Nasonia, e.g. by determining
if this effect results from a co-adaptation between hosts and
symbionts, or from an intrinsic hybrid dysfunction (e.g.
immune defects) that leads to the incapacity of dealing with
many free-living bacteria (Chandler and Turelli 2014). Evi-
dencing co-adaptation between hosts and symbionts leading
to hybrid depression would be an important step because
this mechanism parallels the Bateson–Dobzhansky–Muller
model of genetic incompatibility at the origin of speciation
(Gavrilets 2003), but based on the hologenome rather than
the host genome only.
Methodological perspectives on eco-evolutionary studies
of gut microbiota
ere are at least two main axes for caveats and method
development for studies on gut microbiota. e first one is
to observe, as is the case in epigenetics studies (Birney et al.
2016), that host–microbiota observational studies relate phe-
notype with phenotype, and are thus prone to inversion of
causality interpretations. In other words, because microbiota
can cause trait change in the host or be selected in the host
because of some pleiotropic effect linked to the focal trait of
the host, it is impossible to conclude on mechanisms linking
microbiota to host traits without effective manipulation of
the microbiota. Such manipulative designs include gnotobi-
otic hosts (e.g. obtained through fecal transplants) and hosts
or more recently in the light of epigenetics. However, given
the mostly horizontal mode of transmission of gut micro-
biota between individual hosts, host–microbiota coevolu-
tion could have unsuspected effects on the evolution of
host life-history traits. For instance, the fluctuating epista-
sis theory of selection for sexual reproduction (Gandon
and Otto 2007) could also apply when considering
microbial symbionts instead of genes, if offspring micro-
biota could be regarded as some ‘recombined’ version of
those of its parents. Indeed, different microbial taxa could
confer variable fitness to their hosts depending on host
adaptation to the microbiota (following the Red Queen
explanation of fluctuating epistasis) or depending on the
interaction between microbiota and the environment of
its host (e.g. diet or climate conditions, thus following
the more environmentally based version of fluctuating
epistasis). In both cases, this process of host–microbiota
coevolution leading to fluctuating effects on host fitness
would lead to the same selective pressure acting on the
maintenance of sexual reproduction, provided offspring
microbiota are related to those of its parents. Transmis-
sion of symbionts between parents and offspring, however,
does not need to be directly linked to reproduction for this
effect to hold. Other life-history traits which are somehow
more difficult to explain based on purely vertical trans-
mission of biological information (genes), such as senes-
cence or parity, could also benefit from a gut microbiota
perspective.
From a more demographic perspective, host microbiota
composition can affect population dynamics and genetic
diversity of hosts through effects on reproduction, mor-
tality and dispersal. It is well known that endosymbionts
such as Wolbachia have important effect on host reproduc-
tion, genetic diversity and population dynamics through
male-killing, parthenogenesis induction, cytoplasmic
incompatibilities, or feminization of genetic males (Werren
et al. 2008), which all induce a distortion of the sex ratio
and, hence, a decrease in genetic diversity and birth rate.
Mildly pathogenic taxa within the gut microbiota could
display similar effects, e.g. when they affect behavior and
social interactions of the host. Conversely, gut microbiota
could also play a positive role on reproduction which could
be evinced through experiments on axenic or gnotobiotic
hosts. For instance, it has been reported that rifampin-
treated termite founders tend to have lower oviposition
rates (Rosengaus et al. 2011).
e effects of gut microbiota on life history can have
an important impact in eco-evolutionary dynamics, at
varying levels, ranging from populations to ecosystems.
Future studies investigating eco-evolutionary feedbacks
should thus take account of this factor. A great challenge
for ecology in the coming decades is to understand the role
humans play in eco-evolutionary dynamics. Humans are
major selective agents with potential for unprecedented
evolutionary consequences for Earth’s ecosystems, espe-
cially as cities expand rapidly (Alberti 2015). Among
the human-induced selective pressures that can affect
this dynamics, the massive use of antibiotics and over-
hygienic lifestyles (e.g. over-use of sanitizers) may be of
particular importance, through their effects on microbial
communities.
EV-19
will most likely be less pronounced than the effects that have
been detected for endosymbionts, given the more labile
association between the host and the microbiota in compari-
son with endosymbionts. Nevertheless, given that the core
microbiota is partly heritable (either due to vertical trans-
mission, or to interactions with host genotype, e.g. through
immune genes), it can affect quantitative genetic variation
over multiple generations.
Depending on their transmission routes, gut symbionts
may affect heritability in different ways. Vertical transmis-
sion of gut symbionts from mothers to offspring (e.g. via
symbionts capsules in insects) may lead to an over-estimation
of heritability for traits that are affected by these symbionts.
Horizontal exchanges of symbionts may also affect herita-
bility, e.g. by increasing resemblance between interacting
individuals. Interactions of the gut microbiota with host
genotype (e.g. through immunity) likely further reinforce
heritability. In the future, when studying variations in a par-
ticular phenotypic trait, the structure of the gut microbiota
should be ezamined, to determine whether variation in this
trait could be explained by variations in the structure of the
microbiota (i.e. individuals with similar phenotype have
similar gut microbial communities). To determine whether
the gut microbiota influences the heritability of this trait,
different methods might be envisaged. First, the heritability
could be compared between conventional and germ-free ani-
mals. Any difference would mean that gut symbionts affect
the measurement of heritability. To investigate more deeply
the underlying mechanisms, e.g. to determine whether the
effect of gut microbiota on heritability is due vertical trans-
mission of symbionts, germ-free juveniles could be colo-
nized with either the microbiota from their mother, or with
a different gut microbial inoculum. If heritability is stronger
when juveniles are inoculated with the microbiota from their
mother, it may indicate that microbiota-mediated effects on
heritability occur via the vertical transmission of symbionts.
In future studies, it will be important to disentangle
what proportion of the microbiota is really heritable and
what proportion is a transient maternally or environmen-
tally induced effect, and to assess whether the core taxa show
heritability as if they were vertically transmitted between
mother and progeny (which could be mediated through the
host immune system) or more like horizontal transmission
from the population or the environment (e.g. if a certain
bacterial species in the core gut microbiota is genetically
more closely related to the same species in the mother than
this same species in other nonrelated individuals). ere is
an urgent need for transgenerational studies investigating
microbiome x host genotype interactions (adaptive versus
non-adaptive microbiome host genotype combinations)
with respect to host life history and fitness effects, more in
particular disentangling the role of the host and the symbi-
ont immune system.
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  • ... Figure 1 remains an over-simplification, as the community that is depicted only represents one subset of interacting species. In reality, local systems will be characterized by food webs involving predators ( Gravel et al. 2011;Poisot et al. 2015), parasites ( Lafferty et al. 2006;Thompson 2005) and mutualists ( Koskella et al. 2017;Macke et al. 2017) (Figure 2). A body of knowledge exists for predator-prey, host-parasite and host-mutualist co-evolution and how this evolution impacts interaction strengths and population dynamics ( Penczykowski et al. 2016). ...
    ... The table excludes studies that address interaction modules such as predator-prey interactions (e.g. Becks et al. 2012;Hiltunen & Becks 2014;Yoshida et al. 2003), host-parasite interactions ( Brunner et al. 2017;Decaestecker et al. 2013;Frickel et al. 2016;Masri et al. 2015) and host-mutualist interactions ( Ford et al. 2016;Macke et al. 2017), unless they involved whole communities of predators, prey, hosts, parasites or mutualists. ...
    ... Most eco-evolutionary studies of predator-prey and host-parasite interactions involve one species of each type of interactors (predator and prey, host and parasite) and thus while taking a two-species approach they do not allow estimating the degree to which evolution of competing predator or prey influence dynamics. We also excluded studies from the table that show that genetic variation in a host species can influence gut microbiome composition ( Macke et al. 2017). Because the gut microbiome develops internally in a particular host individual, incorporating a multi-species context with respect to the host might be less pressing, although the presence of other species might influence patterns by modulating environmental source bacteria in case the microbiome is horizontally acquired. ...
    Article
    1.The field of eco‐evolutionary dynamics is developing rapidly, with a growing number of well‐designed experiments quantifying the impact of evolution on ecological processes and patterns, ranging from population demography to community composition and ecosystem functioning. The key challenge remains to transfer the insights of these proof‐of‐principle experiments to natural settings, where multiple species interact and the dynamics are far more complex than those studied in most experiments. 2.Here we discuss potential pitfalls of building a framework on eco‐evolutionary dynamics that is based on data on single species studied in isolation from interspecific interactions, which can lead to both under‐ and overestimation of the impact of evolution on ecological processes. Underestimation of evolution‐driven ecological changes could occur in a single‐species approach when the focal species is involved in co‐evolutionary dynamics, whereas overestimation might occur due to increased rates of evolution following ecological release of the focal species. 3.In order to develop a multi‐species perspective on eco‐evolutionary dynamics, we discuss the need for a general definition of ‘eco‐evolutionary feedbacks’ that include any reciprocal interaction between ecological and evolutionary processes, next to a stricter definition of a ‘feedback loop’ that refers to interactions that directly feed back on the interactor that evolves. 4.We discuss the challenges and opportunities of using more natural settings in eco‐evolutionary studies by gradually adding complexity: (i) multiple interacting species within a guild, (ii) food web interactions, and (iii) evolving metacommunities in multiple habitat patches in a landscape. A literature survey indicated that only a few studies on microbial systems so far developed a truly multi‐species approach in their analysis of eco‐evolutionary dynamics, and mostly so in artificially constructed communities. 5.Finally, we provide a roadmap of methods to study eco‐evolutionary dynamics in more natural settings. Eco‐evolutionary studies involving multiple species are necessarily demanding and might require intensive collaboration among research teams, but are highly needed. This article is protected by copyright. All rights reserved.
  • ... Animal bodies are sophisticated centers of symbiotic interactions ( Ley et al., 2008; Huttenhower and The human microbiome project consortium, 2012; Macke et al., 2017) that have allowed for adaptations enabling hosts to exploit new niches ( Russell et al., 2009;Godoy-Vitorino et al., 2012;Dietrich et al., 2014;Macke et al., 2017). Of the many microbial communities associated with hosts, the digestive tract microbiota (DTM) is likely the most diverse, fulfilling essential functions in nutrition absorption, breakdown of macromolecules, vitamin synthesis, detoxification, and defense (Kohl, 2012;Poulsen et al., 2014;Ceja-Navarro et al., 2015). ...
    ... Animal bodies are sophisticated centers of symbiotic interactions ( Ley et al., 2008; Huttenhower and The human microbiome project consortium, 2012; Macke et al., 2017) that have allowed for adaptations enabling hosts to exploit new niches ( Russell et al., 2009;Godoy-Vitorino et al., 2012;Dietrich et al., 2014;Macke et al., 2017). Of the many microbial communities associated with hosts, the digestive tract microbiota (DTM) is likely the most diverse, fulfilling essential functions in nutrition absorption, breakdown of macromolecules, vitamin synthesis, detoxification, and defense (Kohl, 2012;Poulsen et al., 2014;Ceja-Navarro et al., 2015). ...
    ... The DTM is not only of importance in the digestive tract, but also impacts the growth, development, and behavior of hosts (Round and Mazmanian, 2009;Sommer and B?ckhed, 2013). Although extensive work on DTMs has been carried out on a number of hosts, a thorough understanding of the composition and role of the DTM is limited to relatively few taxa, including mammals ( Ley et al., 2008; Huttenhower and The human microbiome project consortium, 2012; Kohl et al., 2018), insects (Macke et al., 2017), and some captive and livestock animals ( Waite and Taylor, 2015;Hird, 2017). ...
    Article
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    The digestive tract microbiota (DTM) plays a plethora of functions that enable hosts to exploit novel niches. However, our understanding of the DTM of birds, particularly passerines, and the turnover of microbial communities along the digestive tract are limited. To better understand how passerine DTMs are assembled, and how the composition changes along the digestive tract, we investigated the DTM of seven different compartments along the digestive tract of nine New Guinean passerine bird species using Illumina MiSeq sequencing of the V4 region of the 16S rRNA. Overall, passerine DTMs were dominated by the phyla Firmicutes and Proteobacteria. We found bird species-specific DTM assemblages and the DTM of different compartments from the same species tended to cluster together. We also found a notable relationship between gut community similarity and feeding guilds (insectivores vs. omnivores). The dominant bacterial genera tended to differ between insectivores and omnivores, with insectivores mainly having lactic acid bacteria that may contribute to the breakdown of carbohydrates. Omnivorous DTMs were more diverse than insectivores and dominated by the bacterial phyla Proteobacteria and Tenericutes. These bacteria may contribute to nitrogen metabolism, and the diverse omnivorous DTMs may allow for more flexibility with varying food availability as these species have wider feeding niches. In well-sampled omnivorous species, the dominant bacterial genera changed along the digestive tracts, which was less prominent for insectivores. In conclusion, the DTMs of New Guinean passerines seem to be species specific and, at least in part, be shaped by bird diet. The sampling of DTM along the digestive tract improved capturing of a more complete set of members, with implications for our understanding of the interactions between symbiont and gut compartment functions.
  • ... At one extreme, gut symbionts can be directly transferred from mother to off- spring, but most of the time they are randomly picked up from the environment [1]. In general, the gut microbiota is a multilayered structure, composed of both a core microbiota under host genetic and immune control and a flexible pool of microbes modulated by the environment [2,3]. Although hosts can be colonized by opportunistic food-related or widespread environmental taxa, they are often directly or indirectly colonized by microbiota re- leased in the environment by conspecifics [4]. ...
    ... Many factors can, however, influence the community composition of the microbiota that becomes established on the host [3]. Processes governing the microbiota as- sembly seem to be strictly regulated in some species, strongly reducing inter-individual variation [16]. ...
    ... Only OTUs which occurred in at least two samples within a group are included way to antibiotic gradients [31]. Furthermore, antibiotic ex- posure can impact the microbiota indirectly through its ef- fect on host physiology (e.g., via host immunity, [3,32,33]), which can also be dose-dependent [34]. In this study, an increase in resistance of Hydrogenophaga sp. was ob- served after 23 days of exposure to 100 μg OTC L −1 , which allowed this OTU to outcompete Acinetobacter sp. and dominate the microbiota community. ...
    Article
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    Background: Host-associated microbiota is often acquired by horizontal transmission of microbes present in the environment. It is hypothesized that differences in the environmental pool of colonizers can influence microbiota community assembly on the host and as such affect holobiont composition and host fitness. To investigate this hypothesis, the host associated microbiota of the invertebrate eco(toxico)logical model Daphnia was experimentally disturbed using different concentrations of the antibiotic oxytetracycline. The community assembly and host-microbiota interactions when Daphnia were colonized by the disturbed microbiota were investigated by inoculating germ-free individuals with the microbiota. Results: Antibiotic-induced disturbance of the microbiota had a strong effect on the subsequent colonization of Daphnia by affecting ecological interactions between members of the microbiota. This resulted in differences in community assembly which, in turn, affected Daphnia growth. Conclusions: These results show that the composition of the pool of colonizing microbiota can be an important structuring factor of the microbiota assembly on Daphnia, affecting holobiont composition and host growth. These findings contribute to a better understanding of how the microbial environment can shape the holobiont composition and affect host-microbiota interactions.
  • ... Het microbioom wordt zelfs een functioneel deel van het gastheer-organisme. De positieve effecten van het microbioom voor de gastheer krijgen recent meer aandacht en gaan van de beschikbaarheid van extra voedingsstoffen tot verhoogde immuniteit en algemene conditie ( Macke et al. 2017a, Flandroy et al. 2018). In het SPEEDY-project bestudeerden we een aantal soorten en hun tegenwerkende of samenwerkende relaties binnen en buiten de stad. ...
    ... De samenstelling van het microbioom wordt bepaald door welke micro-organismen in de omgeving aanwezig zijn en hoe deze organismen interageren met de genen en immuniteit van de gastheer ( Macke et al. 2017a). Wanneer verstedelijking de gemeenschap van aanwezige micro-organismen verandert, zal dit dus ook een verstoring veroorzaken in het microbioom van de ...
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    Research within the SPEEDY-network has shown that urbanisation has an effect on the parasite and symbiont community. In a few cases urbanisation was associated with a reduction in the number of micro-organisms associated with the host. Nevertheless there are species specific responses: particular species increase and others decrease in the city. The possibility of the host to invest in immune responses is an important explaining factor in this pattern. It is important to note that initiatives to increase biodiversity in cities are recommended, this to avoid that opportunistic and harmful infections thrive. The SPEEDY-research further showed that the microbiome is a crucial element in the flexibility for the host to adapt to fast and changing environments, inclusive the presence of toxic substances and infectious diseases.
  • ... The whitefish intestinal microbiota was not reflective of the whitefish environment within each lake tested. Therefore, host physiology, immunity, and genetic back- ground may play a role in determining the internal in- testinal microbiota [34,45,47,81]. The taxonomy between the fish intestinal microbiota and the bacterial water community was highly distinct among lakes. ...
    ... The difference in genera diversity may result from both host genetic and immunity effects. Although the intes- tinal tract of animals contains the largest number of bac- teria, which explains the difference between the intestinal mucosa and the kidney microbiomes at the OTU level, bacterial selection by the host may stabilize the number of intestinal genera [14,16,17,81]. Such host-driven selection was highlighted in a zebrafish (Danio rerio) intestinal microbiota study, where the number of OTUs decreased during zebrafish develop- ment until reaching an equilibrium at fish maturity [89]. ...
    Article
    Full-text available
    Background: It is well established that symbionts have considerable impact on their host, yet the investigation of the possible role of the holobiont in the host's speciation process is still in its infancy. In this study, we compared the intestinal microbiota among five sympatric pairs of dwarf (limnetic) and normal (benthic) lake whitefish Coregonus clupeaformis representing a continuum in the early stage of ecological speciation. We sequenced the 16s rRNA gene V3-V4 regions of the intestinal microbiota present in a total of 108 wild sympatric dwarf and normal whitefish as well as the water bacterial community from five lakes to (i) test for differences between the whitefish intestinal microbiota and the water bacterial community and (ii) test for parallelism in the intestinal microbiota of dwarf and normal whitefish. Results: The water bacterial community was distinct from the intestinal microbiota, indicating that intestinal microbiota did not reflect the environment, but rather the intrinsic properties of the host microbiota. Our results revealed a strong influence of the host (dwarf or normal) on the intestinal microbiota with pronounced conservation of the core intestinal microbiota (mean ~ 44% of shared genera). However, no clear evidence for parallelism was observed, whereby non-parallel differences between dwarf and normal whitefish were observed in three of the lakes while similar taxonomic composition was observed for the two other species pairs. Conclusions: This absence of parallelism across dwarf vs. normal whitefish microbiota highlighted the complexity of the holobiont and suggests that the direction of selection could be different between the host and its microbiota.
  • ... This molecular dialog between host immunity and gut symbionts plays a crucial role and is starting to be deciphered. These interactions are currently placed in an eco-evolu- tionary context reflecting the role of the microbiome in host acclimatization and adaptation in fast changing environments (Macke et al., 2017). ...
    Article
    Full-text available
    Plants, animals and humans, are colonized by microorganisms (microbiota) and transiently exposed to countless others. The microbiota affects the development and function of essentially all organ systems, and contributes to adaptation and evolution, while protecting against pathogenic microorganisms and toxins. Genetics and lifestyle factors, including diet, antibiotics and other drugs, and exposure to the natural environment, affect the composition of the microbiota, which influences host health through modulation of interrelated physiological systems. These include immune system development and regulation, metabolic and endocrine pathways, brain function and epigenetic modification of the genome. Importantly, parental microbiotas have transgenerational impacts on the health of progeny. Humans, animals and plants share similar relationships with microbes. Research paradigms from humans and other mammals, amphibians, insects, planktonic crustaceans and plants demonstrate the influence of environmental microbial ecosystems on the microbiota and health of organisms, and indicate links between environmental and internal microbial diversity and good health. Therefore, overlapping compositions, and interconnected roles of microbes in human, animal and plant health should be considered within the broader context of terrestrial and aquatic microbial ecosystems that are challenged by the human lifestyle and by agricultural and industrial activities. Here, we propose research priorities and organizational, educational and administrative measures that will help to identify safe microbe-associated health-promoting modalities and practices. In the spirit of an expanding version of “One health” that includes environmental health and its relation to human cultures and habits (EcoHealth), we urge that the lifestyle-microbiota-human health nexus be taken into account in societal decision making.
  • ... 18-20 However, symbiotic microbes can also degrade toxins present in their host's food, provide defense against parasites and pathogens, or confer resistance to abiotic environmental factors and actively manipulate their host's biotic environment. [19][20][21][22][23] Furthermore, microbial symbionts can impact the development and evolution of the animal immune system, 23,24 as well as the nervous system, including the photo-and chemosensory apparatus. 25 On the other hand, reproductive manipulators like many strains of Wolbachia, Rickettsia, Cardinium, Spiroplasma, Arsen- ophonus and some Bacteroidetes bacteria actively interfere with their host's reproduction in one of four different ways that promote their own spread within a host population: partheno- genesis, male killing, feminization and cytoplasmic incompat- ibility (CI). ...
    Article
    Covering: up to 2018 Pheromones serve as chemical signals between individuals of the same species and play important roles for mate localization and mate choice as well as other social interactions in insects. A growing body of literature indicates that microbial symbionts can modulate their hosts' chemical profiles, mate choice decisions and social behavior. This modulation can occur by the direct biosynthesis of pheromone components or the provisioning of precursors, or through general changes in the metabolite pool of the host and its resource allocation into pheromone production. Here we review and discuss the contexts in which microbial modulation of intraspecific communication in insects occurs and emphasize cases in which microbes are known to affect the involved chemistry. The described examples for a symbiotic influence on mate attraction and mate choice, aggregation, nestmate and kin recognition highlight the context-dependent costs and benefits of these symbiotic interactions and the potential for conflict and manipulation among the interacting partners. However, despite the increasing number of studies reporting on symbiont-mediated effects on insect chemical communication, experimentally validated connections between the presence of specific symbionts, changes in the host's chemistry, and behavioral effects thereof, remain limited to very few systems, highlighting the need for increased collaborative efforts between symbiosis researchers and chemical ecologists to gain more comprehensive insights into the influence of microbial symbionts on insect pheromones.
  • Preprint
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    Understanding of what ecological factors shape intraspecific variation of insect microbiota is still relatively poor. In Lepidopteran caterpillars, microbiota is assumed to be mainly composed of transient bacterial symbionts acquired from the host plant. We sampled Glanville fritillary (Melitaea cinxia) caterpillars from natural populations to describe the microbiome and to identify potential factors that determine the structure of the microbial community, including the sex of the host, the impact of parasitoid infection, and the possible link between host plant and caterpillar microbiota. Our results demonstrate high variability of microbiota composition even among caterpillars that shared the same host plant individual. The observed variation in microbiota composition is partially attributed to the measured properties of the host or its plant microbial and chemical composition, and is aligned with microbial phylogenetic structure, with related taxa exhibiting similar patterns. However, the prevailing part of the observed variation was not associated with any of the assessed characteristics, although it followed a pronounced segregation structure: in some caterpillars the microbial communities were dominated by several related Enterobacteriaceae taxa, while in others these taxa were absent. Our results challenge previous findings that the host plant properties are the major drivers of microbiota communities of insect herbivores.
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    Background The relatively fast selection of symbiotic bacteria within hosts and the potential transmission of these bacteria across generations of hosts raise the question of whether interactions between host and bacteria support emergent adaptive capabilities beyond those of germ-free hosts. Results To investigate possibilities for emergent adaptations that may distinguish composite host-microbiome systems from germ-free hosts, we introduce a population genetics model of a host-microbiome system with vertical transmission of bacteria. The host and its bacteria are jointly exposed to a toxic agent, creating a toxic stress that can be alleviated by selection of resistant individuals and by secretion of a detoxification agent (“detox”). We show that toxic exposure in one generation of hosts leads to selection of resistant bacteria, which in turn, increases the toxic tolerance of the host’s offspring. Prolonged exposure to toxin over many host generations promotes anadditional form of emergent adaptation due to selection of hosts based on detox produced by their bacterial community as a whole (as opposed to properties of individual bacteria). Conclusions These findings show that interactions between pure Darwinian selections of host and its bacteria can give rise to emergent adaptive capabilities, including Lamarckian-like adaptation of the host-microbiome system. Reviewers This article was reviewed by Eugene Koonin, Yuri Wolf and Philippe Huneman.
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    Microorganisms comprise the majority of earth's biodiversity and are integral to biosphere processes. Biological invasions are no exception to this trend. The success of introduced macroorganisms can be deeply influenced by diverse microorganisms ( bacteria, virus, fungus and protozoa) occupying the whole range of species interaction outcomes, from parasitism to obligate mutualism. This large range of interactions, often coupled with complex historical and introduction events, can result in a wide variety of ecological dynamics. In this chapter, we review different situations in which microorganisms affect biological invasions. First, we consider outcomes of microorganism loss during the introduction of alien species. Second, we discuss positive effects of microorganisms on the invasiveness of their exotic hosts. Third, we examine the influence of microorganisms hosted by native species on the success of introduced species. Finally, in an applied perspective, we envisage how microorganisms can be used (i) to better decipher invasion processes and (ii) as biological control agents.
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