Functional Ecology 2014, 28, 293–298
doi: 10.1111/1365-2435.12258
EDITORIAL
Defensive symbiosis: a microbial perspective
Keith Clay*
Department of Biology, Indiana University, Bloomington, IN, USA
The enemy of my enemy is my friend (Ancient Proverb)
Defensive symbioses are indirect interactions that
involve at least three species (host, symbiont and enemy)
where the net benefits of symbiosis are contingent on the
presence of enemies (Fig. 1, Clay, Holah & Rudgers 2005;
Lively et al. 2005). The performance of host and non-host
populations in the presence and the absence of natural enemies distinguishes the direct benefits of symbiosis (such as
nutrient provisioning) from indirect benefits arising from
protection from natural enemies. Defensive symbiosis
requires that the fitness of hosts is proportionally higher
than non-hosts in the presence of natural enemies relative
to enemy-free conditions. In the absence of enemies, the
defensive symbiont may decline in frequency or be lost
from the host population (Janzen 1973; Lively et al. 2005;
Palmer et al. 2008).
Protective or defensive mutualisms have long been recognized. Thomas Belt (1874), in The Naturalist in Nicaragua, first described the defence of acacia trees from
herbivores by ants (see also Boucher, James & Keeler
1982; Janzen 1985; Palmer et al. 2008). We now know that
extrafloral nectaries, Beltian bodies and other traits that
attract ants for defence against herbivores are widespread
in plants (Bentley 1977; Beattie 1985; Rudgers & Strauss
2004; Rico-Grey & Oliveira 2007). Outside of ant–plant
protective interactions, which are based on physical
aggression, defensive mutualisms involving microbial symbionts often involve the production of toxic secondary
metabolites. One well-understood example is grasses
infected by endophytic fungi (family Clavicipitaceae) that
grow systemically in above-ground plant tissues, are vertically transmitted through seeds and produce a variety of
alkaloid compounds deterrent to herbivores (Clay 1988;
Clay & Schardl 2002). The endophytes are under strong
selection for alkaloid diversification which may improve
their protective function (Schardl et al. 2013). Defensive
symbioses between insects and bacteria are also widespread. For example, Currie and colleagues (Currie, Mueller & Malloch 1999a; Currie et al. 1999b, 2006) reported
that leaf cutter ants (Atta spp.) harbour antibiotic-producing actinobacteria (Pseudocardinia spp.) that inhibit Escovopsis spp. pathogens of their fungal gardens and help
maintain the mutualism between ants and their fungal gardens. Many sap-sucking insects like aphids also harbour
defensive symbionts which provide protection against a
*Correspondence author. E-mail: [email protected]
range of natural enemies (Oliver et al. 2003, 2008; Scarborough, Ferrari & Godfray 2005; Oliver & Moran 2009;
Tsuchida et al. 2010; Lukasik et al. 2013).
Microbial interactions with plants and animals are typically invisible to the naked eye, but their impacts on hosts
and host communities can be very large. Higher organisms
host diverse microbial communities (Arnold et al. 2000;
Costello et al. 2009; Rodriguez et al. 2009; Hawlena et al.
2013), and microbial dependency on the host will favour
traits that help protect that resource and ensure their
transmission (Lukasik et al. 2013). Microbes have high
rates of evolutionary change, and horizontal transfer of
adaptive genes or genomes is common (McCutcheon,
McDonald & Moran 2009; Oliver et al. 2010; Werren
et al. 2010; Smillie et al. 2011; Zhu et al. 2013). New
approaches and technological advances are providing
novel insights into plant and animal microbiomes, and
more demonstrated and hypothesized examples of defensive symbiosis (Turnbaugh et al. 2009; White & Torres
2009; Zhu et al. 2011; Lundberg et al. 2012). Identifying
the key microbial players and the underlying mechanisms
of protection will improve our understanding of factors
affecting the dynamics of ecological communities and
provide applications for agriculture and human health
(Wicklow et al. 2005; Mazmanian, Round & Kasper 2008;
Mao-Jones et al. 2010).
Key research directions
While a few systems have been well studied, our knowledge of the diversity, distribution, mechanisms and ecological consequences of defensive symbioses is limited. This is
despite increasing scientific interest and technological innovations enabling rapid discovery and novel research directions in symbiotic systems. Most macro-organisms support
diverse microbial communities, but we have limited understanding of how microbes interact with each other within
hosts and with enemies of the host. It is perhaps not surprising that the best understood defensive symbioses occur
in hosts with just one (e.g. grasses) or a few (e.g. aphids)
dominant microbial symbionts, which are easier to evaluate. A major challenge is to identify potential defensive
contributions of particular microbes in hosts with diverse
microbiomes or determine whether protection arises
through interactions within microbial consortia. To help
begin to address these and other gaps, several research
directions are recommended.
© 2014 The Author. Functional Ecology © 2014 British Ecological Society
294 Editorial
within hosts (Klyachko et al. 2007), and q-PCR can be
used to assess symbiont density in relation to host age,
gender, habitat, etc. More generally, a combination of
molecular and microscopic approaches can serve to identify and localize microbial symbionts and identify potential
genes with defensive functions.
MECHANISMS OF DEFENCE
Fig. 1. Defensive symbiosis arising from an indirect interaction of
S (symbiont) with H (host). S imposes a direct cost on H for its
metabolic demands, but this cost is more than offset by the negative effect of S on E (natural enemy). E has a stronger negative
effect on H than S, resulting in a net positive benefit of S on H.
IDENTIFYING DEFENSIVE SYMBIOSES
Are defensive symbioses common and widespread, or do
they occur only in a few specific systems with particular
organisms and habitats? Based on the rate at which new
examples of defensive symbiosis are being described, we
may be seeing only the tip of the iceberg. However, in complex communities of macro- and micro-organisms, it is nontrivial challenge to obtain direct evidence of defensive symbiosis. Comparing performance of host and non-host populations with and without natural enemies is the most direct
way to identify defensive symbioses. Cases where resistance
to enemies can be “cured” by antibiotic or fungicide applications, or where resistance is strictly maternally inherited,
also represent strong candidates for defensive symbiosis.
More typically, evidence for defensive symbiosis is indirect. Microbial production of secondary metabolites with
known toxic functions is often taken as prima facie evidence of defensive symbiosis. For example, Nakabachi
et al. (2013) recently described a bacterial symbiont (Candidatus Profftella armature) of the Asian citrus psyllid,
Diaphorina citri, where 15% of its highly reduced genome
is devoted to two biosynthetic gene clusters that encode a
polyketide toxin similar in structure to pederin. In Paederus rove beetles, pederin is synthesized by a Pseudomonas
symbiont and accumulates in the body fluid of the beetle,
where it serves to deter predators (Kellner & Dettner
1996). Likewise, antibiotic production by insect-associated
bacteria also suggests that these symbionts play a protective role (Scott et al. 2008; Um et al. 2013).
The increasing availability of molecular and genomic
technologies offers new opportunities to identify and characterize defensive symbioses. 16S rRNA tag sequencing
using a high-throughput pyrosequencing can efficiently
search for and identify particular groups of bacterial
symbionts (Hawlena et al. 2013), and metagenomic,
whole-genome shot-gun sequencing can be used to identify
alkaloid or antibiotic production genes diagnostic for
defensive symbiosis. Fluorescent in-situ hybridization can
be used to visualize and localize microbial symbionts
The mechanism of defence is not known in many systems,
even where defensive symbiosis has been experimentally
documented (e.g. Scarborough, Ferrari & Godfray 2005;
Jaenike et al. 2010; Xie, Vilchez & Mateos 2010; Busby
et al. 2013). Identification of those mechanisms will enhance
our understanding of defensive symbiosis and point to
potential applications for pest control and improved plant
and animal health. Where the mechanism of defence is
clear, most defensive symbioses appear to exhibit one of
two basic patterns but others may exist. First, the production (or detoxification) of bioactive secondary compounds
by microbial symbionts is common to many defensive symbioses. Related chemistry can often be found in free-living
relatives, suggesting that pre-existing microbial pathways
have been co-opted for host defence. For example, toxinproducing bacterial and fungal endosymbionts infect poisonous plants such as locoweeds (Fabaceae, Braun et al.
2003; Panaccione, Beaulieu & Cook 2014) and some species
of grasses (Clay & Schardl 2002), morning glories (Convoluvulaceae, Beaulieu et al. 2013; Cook et al. 2013) and Rubiaceae (Verstraete et al. 2011), as well as marine organisms
(Lopanik, Lindquist & Targett 2004; Simmons et al. 2008).
Similarly, antibiotics are produced by free-living soil bacteria but are also produced by bacterial symbionts of insects,
where they provide resistance to pathogenic micro-organisms (Currie, Mueller & Malloch 1999a; Scott et al. 2008;
Um et al. 2013). In the case of pea aphids and their Hamiltonella endosymbiont, host protection against parasitoids
imparted by Hamiltonella depends on symbiont being
infected with a toxin-producing bacteriophage (Moran et al.
2005; Weldon, Strand & Oliver 2013).
Parasites and herbivores can also turn the table and use
microbial symbionts to detoxify or resist their target
organism’s defensive chemistry. For example, conifers
respond to beetle attack by producing toxic terpenes, but
bacterial symbionts associated with mountain pine beetles
(Dendroctonus ponderosae) can reduce terpene concentrations in artificial media (Boone et al. 2013), suggesting that
beetle–bacteria symbiosis reduces the efficacy of host plant
defence responses. Similarly, secretion of symbiotic bacteria by the Colorado potato beetle during feeding elicits
salicylic acid-regulated defences, which inhibits plant activation of jasmonate-mediated resistance (Chung et al.
2013), and gut microbiota of woodrats that detoxify secondary metabolites produced by their creosote bush food
plant (Kohl & Dearing 2012).
A second general mechanism of microbially mediated
defence is priming of the host’s immune system with infec-
© 2014 The Author. Functional Ecology © 2014 British Ecological Society, Functional Ecology, 28, 293–298
FE Spotlight
tion by the symbiont, increasing resistance to subsequent
parasites or pathogens (Little & Kraaijeveld 2004). This
mechanism is not limited to higher animals but occurs also
in invertebrates and plants (Moreira et al. 2009; Jung et al.
2012; Hussa & Goodrich-Blair 2013). For example, colonization of plant roots by mycorrhizal fungi can induce resistance to plant pathogens by the priming of jasmonic
acid-dependent defences (Cameron et al. 2013), and leaf endophytes of trees reduce infection by plant pathogens
(Arnold et al. 2003; Busby et al. 2013). Microbial symbionts
can therefore serve as a vaccine to enhance immunological
defence. The role of microbial symbionts in immunological
priming also raises the more general question of how hosts
permit infection by beneficial symbionts while simultaneously discriminating against damaging pathogens.
Other potential mechanisms of defensive symbiosis may
exist. Formation of biofilms or epiphytic layers can provide
a physical or chemical barrier between host and pathogen.
For example, seaweeds are often colonized by epiphytic
bacteria with antifouling properties that protect chemically
undefended seaweeds from secondary colonization by detrimental epiphytic growth (Egan et al. 2013). Similarly, skin
bacteria of amphibians can reduce susceptibility to chytridiomycosis (Daskin & Alford 2012). Microbial symbionts
may also directly interfere with the growth or replication of
the pathogenic agent. For example, some Wolbachia strains
protect Drosophila hosts against RNA virus infection, suggesting that Wolbachia may interfere with viral replication
(Hedges et al. 2008; Teixeira, Ferreira & Ashburner 2008;
Osborne et al. 2009). Other potential mechanisms of
defence may include competitive exclusion of pathogens by
symbionts (Koch & Schmid-Hempel 2011) and use of protective viruses by parasitoid wasps that inject symbiotic
polydnaviruses during oviposition to suppress the host’s
immune response (Strand & Burke 2012).
COSTS AND BENEFITS OF MICROBIAL SYMBIOSIS VS.
INNATE DEFENSIVE MECHANISMS
Macro-organisms possess a variety of physical, chemical
and immune defence mechanisms. Under what circumstances are symbiont-based defence favoured over inherent
defence? Presumably, microbial symbionts provide services
that the host is not capable of, or they provide services
more cheaply than can the host themselves. For example,
the fungal endophyte-derived alkaloids found in many
grasses occur in a plant family that does not typically produce the diverse secondary compounds found in many
other plant families (Clay & Schardl 2002). Likewise, the
capacity for antibiotic production is limited to bacteria
and fungi but has been exploited by various insect groups
via symbiosis with antibiotic-producing partners (Currie,
Mueller & Malloch 1999a; Currie et al. 1999b; Kaltenpoth
et al. 2005). The relative costs and benefits of microbial
symbiosis vs. innate defensive mechanisms may vary
within a host species or among groups of closely related
species as evidenced by trade-offs between defensive strate-
295
gies. For example, fungus-growing Trachymyrmex ants
exhibit a trade-off where species with bacterial symbionts
do not exhibit behaviours to reduce Escovopsis infection
and species with strong behavioural responses do not
possess antibiotic-producing symbionts (Fern
andez-Marın
et al. 2013). Detailed analysis of the spatial and temporal
patterns of defensive symbiosis and inherent host defences
will shed light on the costs and benefits of each strategy.
DYNAMICS OF DEFENSIVE SYMBIOSIS
A key question is whether defensive symbionts are fixed in
host populations or whether they are dynamic in space and
time, contingent on variable pest pressure? There are welldocumented cases of rapid changes in symbiont distribution
and prevalence (Oliver et al. 2008; Jaenike et al. 2010), but
the underlying causes may vary. In cases where symbionts
cause reproductive incompatibility or induced parthenogenesis, symbionts can sweep rapidly through host populations
(Perlman, Kelly & Hunter 2008; Himler et al. 2011). Relatively few experiments have directly manipulated defensive
symbionts and natural enemies and measured host population responses, but they demonstrate that symbiosis is
favoured in the presence of natural enemies and that symbiont prevalence increases over time. For example, endophyte-infected tall fescue grass (Lolium arundinaceum)
exhibits increased resistance to herbivores due to the production of alkaloids by the symbiont (Bush, Wilkinson &
Schardl 1997; Rudgers & Clay 2008). In a factorial experiment where insect and mammalian herbivory were manipulated independently, infection frequency increased
significantly faster in populations with the greatest level of
herbivory (Clay, Holah & Rudgers 2005). The endophyte
spreads only through vertical transmission, so increasing
infection frequency reflects the greater relative fitness of
infected individuals under herbivore pressure (see also Koh
& Hik 2007). Similarly, in population cage experiments with
the pea aphid (Acythrosiphon pisum), the frequency of the
protective endosymbiont Hamiltonella defensa increased
dramatically after exposure to parasitoid wasps but
decreased in the absence of parasitoids (Oliver et al. 2008).
Evaluation of symbiont dynamics over time can also provide insights into factors leading to intermediate or fluctuating infection frequencies and frequency-dependent selection.
MECHANISMS OF SYMBIONT TRANSMISSION
Understanding the mechanisms of symbiont transmission
will provide additional insights into their dynamics over
space and time. Most cases of defensive symbiosis involve
vertically transmitted symbionts (through eggs, seeds,
maternal environment, etc.), ensuring continuity of symbiosis
across generations. A general threat to mutualism is the
exploitation of host resources by symbionts that do not
provide any benefits (i.e. cheaters; Bronstein 2001; Sachs
et al. 2004; Orona-Tamayo & Heil 2013). Hereditary symbioses provide strong sanctions against cheaters because
© 2014 The Author. Functional Ecology © 2014 British Ecological Society, Functional Ecology, 28, 293–298
296 Editorial
vertically transmitted pathogens and their hosts will go
extinct (Ewald 1987; Lipsitch, Siller & Nowak 1996; Haine
2008). Given the strong correlation between mutualism
and vertical transmission, vertically transmitted microbes
should be highly represented in defensive symbioses. Nevertheless, non-hereditary symbionts such as mycorrhizal
fungi or leaf endophytes can confer protection against
pathogens (Arnold et al. 2003; Busby et al. 2013), possibly
by priming the plant immune system, and socially transmitted gut microbiota can protect bumblebees against intestinal parasites (Koch & Schmid-Hempel 2011). Defensive
toxins, and the genetic machinery to synthesize them, may
represent highly specific constitutive traits that are best
maintained by vertical transmission. By contrast, immune
system-priming mechanisms may be better accomplished
by symbionts that are not permanent residents of the host.
COMMUNITY AND ECOSYSTEM CONSEQUENCES OF
DEFENSIVE SYMBIOSIS
One overarching question is how do defensive symbioses
affect the structure and dynamics of communities and ecosystems? With defensive symbiosis, we should predict that
the prevalence of the host and symbiont will increase while
the prevalence of enemies will decrease. But we have limited
understanding of how the density of natural enemies is
affected by defensive symbiosis, and how those changes cascade through higher and lower trophic levels. In one example, manipulation of endophyte infection of tall fescue grass
in field plots demonstrated that the structure of the plant
community in plots with the symbiont became increasingly
dominated by the host grass over time, while the abundance
and diversity of insect herbivores in the same communities
decreased (Clay, Holah & Rudgers 2005; Rudgers & Clay
2008). However, there were no changes in plant productivity
(Clay & Holah 1999), and as a result, endophyte infection
altered the relationship between diversity and ecosystem
processes (Rudgers, Koslow & Clay 2004). There is a need
for additional manipulative field studies as well as theoretical models exploring community dynamics of defensive symbioses analogous to models of nutritional or pollination
symbioses (Schwartz & Hoeksema 1998; Bronstein 2001;
Sachs et al. 2004; Holland & DeAngelis 2010). For example,
if the density of enemies decreases with defensive symbiosis,
then the advantage of symbiosis would also decrease, potentially leading to time-lagged, oscillatory dynamics in the
numbers of symbiotic hosts and their enemies. This type of
response may be less likely where interactions are non-specific or where there is little cost to symbiont infection. More
research is required to evaluate the impacts of defensive
symbioses on larger ecological processes.
Introduction to the Special Feature
The goal of this Special Feature is to explore the diversity, mechanisms and consequences of defensive symbiosis mediated by micro-organisms to help organize and
interpret the growing body of work and place it within a
broader ecological and evolutionary context of mutualism
and symbiosis. In the accompanying papers, leading
researchers in the field synthesize their own and related
research on defensive symbiosis and provide independent
perspectives on the current state of the field and future
directions. Kaltenpoth & Engl (2014) consider defensive
symbiosis in the Hymenoptera. In addition to the wellknown association of leaf cutter ants and wasps with
antibiotic-producing symbiotic bacteria, there exist several other mechanisms of defence in this diverse and
important insect group, including the use of symbiotic
viruses to disable defensive responses of victims attacked
by parasitoids. Lopanik (2014) explores the great diversity bioactive secondary chemistry in marine organisms
and their role in defensive symbiosis. Many important
marine groups such as corals and sponges represent complex symbiotic amalgamations (Gil-Turnes, Hay & Fenical 1989; Kwan et al. 2012) and marine bioprospecting
promises to reveal more potential cases of defensive symbiosis. May & Nelson (2014) examine the important issue
of interactions of symbionts within the same host. Most
plants host a great diversity of fungal endosymbionts
that can exhibit broad variety of effects on their hosts
ranging from mutualistic to parasitic. The specific effects
of these symbionts on the ecology and evolution of their
hosts may be conditional on their interactions with each
other such that quantifying the effects of single symbionts on hosts may be inaccurate or misleading. Oliver,
Smith & Russell (2014) focus on heritable bacterial symbionts of insects and explore their population dynamics
and fluctuating infection frequencies in natural host populations. Intermediate and fluctuating infection frequencies of defensive symbionts suggest that their relative
costs and benefits vary in time and space. The rapid generation times and large populations of insects make them
ideal systems to explore dynamics of defensive symbiosis.
Finally, Panaccione, Beaulieu & Cook (2014) explore the
expanding realm of heritable fungal endosymbionts of
plants that produce bioactive alkaloid compounds. While
the role of systemic fungal endophytes in protection of
cool-season grass hosts from herbivores has been understood for several decades, recent research is revealing
that the toxins produced by many poisonous plants are
microbial in origin, and the microbes are systemic and
vertically transmitted through seeds, suggesting convergent evolution of a common defence strategy.
Several common themes emerge from this series of papers
including contingency of outcomes based on the larger community context, convergent evolution of similar defensive
strategies by independent groups of organisms and the
exploitation of defensive symbionts by hosts, by symbionts
and by enemies for a range of ecological interactions. The
contributor’s focus on defensive symbiosis represents a
fruitful area given that the phylogenetic and metabolic
diversity of microbes provides a wealth of biochemical and
immunological mechanisms by which host defence can be
achieved and given that research has been greatly advanced
© 2014 The Author. Functional Ecology © 2014 British Ecological Society, Functional Ecology, 28, 293–298
FE Spotlight
by the application of powerful microbiological and molecular techniques. The results of research on defensive symbiosis have many implications for ecological communities and
ecosystems, agriculture and human health.
Acknowledgements
I would like to thank Charles Fox, Jennifer Meyer and other members of
the Functional Ecology editorial office for their support and help in organizing this special feature. I especially thank the authors for their contributions and the reviewers for their helpful advice and suggestions.
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Received 28 Jan 2014; accepted 30 January 2014
Handling Editor: Charles Fox
© 2014 The Author. Functional Ecology © 2014 British Ecological Society, Functional Ecology, 28, 293–298