Defensive symbiosis: a microbial perspective

Department of Biology, Indiana University, Bloomington, IN, USAThe enemy of my enemy is my friend (Ancient Proverb)Defensive symbioses are indirect interactions thatinvolve at least three species (host, symbiont and enemy)where the net beneﬁts of symbiosis are contingent on thepresence of enemies (Fig. 1, Clay, Holah & Rudgers 2005;Lively et al. 2005). The performance of host and non-hostpopulations in the presence and the absence of natural ene-mies distinguishes the direct beneﬁts of symbiosis (such asnutrient provisioning) from indirect beneﬁts arising fromprotection from natural enemies. Defensive symbiosisrequires that the ﬁtness of hosts is proportionally higherthan non-hosts in the presence of natural enemies relativeto enemy-free conditions. In the absence of enemies, thedefensive symbiont may decline in frequency or be lostfrom the host population (Janzen 1973; Lively et al. 2005;Palmer et al. 2008).Protective or defensive mutualisms have long been rec-ognized. Thomas Belt (1874), in The Naturalist in Nicara-gua, ﬁrst described the defence of acacia trees fromherbivores by ants (see also Boucher, James & Keeler1982; Janzen 1985; Palmer et al. 2008). We now know thatextraﬂoral nectaries, Beltian bodies and other traits thatattract ants for defence against herbivores are widespreadin plants (Bentley 1977; Beattie 1985; Rudgers & Strauss2004; Rico-Grey & Oliveira 2007). Outside of ant–plantprotective interactions, which are based on physicalaggression, defensive mutualisms involving microbial sym-bionts often involve the production of toxic secondarymetabolites. One well-understood example is grassesinfected by endophytic fungi (family Clavicipitaceae) thatgrow systemically in above-ground plant tissues, are verti-cally transmitted through seeds and produce a variety ofalkaloid compounds deterrent to herbivores (Clay 1988;Clay & Schardl 2002). The endophytes are under strongselection for alkaloid diversiﬁcation which may improvetheir protective function (Schardl et al. 2013). Defensivesymbioses between insects and bacteria are also wide-spread. For example, Currie and colleagues (Currie, Muel-ler & Malloch 1999a; Currie et al. 1999b, 2006) reportedthat leaf cutter ants (Atta spp.) harbour antibiotic-produc-ing actinobacteria (Pseudocardinia spp.) that inhibit Escov-opsis spp. pathogens of their fungal gardens and helpmaintain the mutualism between ants and their fungal gar-dens. Many sap-sucking insects like aphids also harbourdefensive symbionts which provide protection against arange of natural enemies (Oliver et al. 2003, 2008; Scarbor-ough, Ferrari & Godfray 2005; Oliver & Moran 2009;Tsuchida et al. 2010; Lukasik et al. 2013).Microbial interactions with plants and animals are typi-cally invisible to the naked eye, but their impacts on hostsand host communities can be very large. Higher organismshost 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 favourtraits that help protect that resource and ensure theirtransmission (Lukasik et al. 2013). Microbes have highrates of evolutionary change, and horizontal transfer ofadaptive genes or genomes is common (McCutcheon,McDonald & Moran 2009; Oliver et al. 2010; Werrenet al. 2010; Smillie et al. 2011; Zhu et al. 2013). Newapproaches and technological advances are providingnovel insights into plant and animal microbiomes, andmore demonstrated and hypothesized examples of defen-sive symbiosis (Turnbaugh et al. 2009; White & Torres2009; Zhu et al. 2011; Lundberg et al. 2012). Identifyingthe key microbial players and the underlying mechanismsof protection will improve our understanding of factorsaﬀecting the dynamics of ecological communities andprovide applications for agriculture and human health(Wicklow et al. 2005; Mazmanian, Round & Kasper 2008;Mao-Jones et al. 2010).