As reflected elsewhere in this volume, insects and other arthropods possess a formidable immune system, comprising both cellular and humoral responses, that responds to a wide array of pathogens and parasites. This response, which can cope with an array of opportunistic infections, is combined with specific resistance to particular pathogens, that may be encoded within this system or in other nuclear genes that interact with the particular parasite or pathogen.
Recently, it has been observed that variation in resistance to pathogens is sometimes not associated with genetic variation in nuclear genes. Rather,
Table 8.1 The taxonomy of bacteria known to show reproductive parasitism, with notes on phenotypes observed, and the host range within which these are observed. For sources, see main text.
Spiroplasma Many arthropods Cardinium
Bacteroidetes Coleoptera (unnamed)
Isopoda, Lepidoptera, Hemiptera
Many haplodiploid arthropods
Acari, Hymenoptera Acari, Hymenoptera
One strains shows antiviral resistance.
Some strains show horizontal transmission through plant/animal.
Many strains show horizontal transmission through plant/animal.
Some strains are likely not to be reproductive parasites.
Also has horizontal transmission; relatives in the genus Arsenophonusare likely to be secondary symbionts.
variation in resistance was maternally inherited, and associated with the presence/absence of secondary symbionts. Detailed study of the effects of secondary symbionts has been largely confined to the resistance of pea aphids, Acrythosiphum pisum, to a variety of pathogens. This has been studied both experimentally through comparison of the susceptibility to parasitism of an aphid clone differing in infection status, and through testing whether parasitism is necessary and sufficient to maintain infection in population cages. Five different secondary symbionts are known to occur in this species, alongside the primary symbiont Buchnera, but two of these—a Rickettsia and a member of the S. ixodetis clade—have not been subject to functional study with respect to resistance to natural enemies (Table 8.2).
Secondary symbionts were first established as a major component of aphid resistance to parasit-oid wasps (Oliver et al., 2003, 2005; Ferrari et al., 2004). Hamiltonella defensa and Serratia symbiotica infection reduced the success of Aphidius ervi parasitism. The defence was not a deterrant to A. ervi oviposition, but defence against the wasp within a challenged aphid. In both cases, laboratory populations of aphids maintained these symbionts in the presence of the host's natural enemy, but the symbiont reduced in frequency in their absence. Following this work, a third secondary symbiont, Regiella insecticola, was observed to be associated with resistance to infection by the fungus Pandora neoaphidis (Scarborough et al., 2005). The ability to resist fungi has also been observed in actinomy-cete symbionts of insects, albeit in this case outside of the insect in the environment the insect occupies (Currie et al, 1999, 2003; Kaltenpoth et al, 2005; Scott et al, 2008).
The intense level of research on Wolbachia has also provided evidence that this bacterium can impact on resistance to pathogens. A strong positive effect of Wolbachia on resistance to RNA virus infection has been revealed recently. Presence of Wolbachia in Drosophila melanogaster protected against three RNA viruses—C virus, Nora virus, and Flock House virus—but not a DNA virus, insect iridescent virus 6 (Hedges et al, 2008; Teixeira et al, 2009). This result has several ramifications. First, it indicates that symbiont-mediated protection extends to viruses. Second, the protecting symbiont can be an existing reproductive parasite. In this case, the bacterium is the wMel strain of Wolbachia, which can also induce weak cytoplasmic incompatibility. Third, resistance can be delivered to a variety of pathogens with similar biology.
Table 8.2 The symbiotic microflora of the pea aphid, Acrythosiphum pisum. All bacteria show maternal transmission. Synonyms given are those used in papers before taxonomic description. References to the data may be found in the corresponding text section. Note, whereas Buchnera is present in all populations and all individuals, secondary symbionts vary in frequency both geographically and temporally.
Symbiosis Bacterium: type division
Gamma proteobacteria Gamma proteobacteria Gamma proteobacteria Gamma proteobacteria Alpha proteobacteria Mollicutes
Candidatus Hamiltonella defensa Candidatus Serratia symbiotica Candidatus Regiella insecticola Rickettsia sp.
Provision of essential amino acids; essential for normal reproduction Increased parasitoid resistance
Increased parasitoid resistance
Increased fungal resistance
Elevated temperature tolerance
Common but variable; sex and oral/faecal Common but variable; sex and oral/faecal Common but variable; sex and oral/faecal Yes, rarely, mechanism unknown Yes, rarely, mechanism unknown
PABS, T type PASS, R type PAUS, U type PAR, S type
Perhaps most surprising is that defence against natural enemies goes beyond immunity. An inherited Pseudomonas symbiont encodes protection of the rove beetle Pederea against predation by spiders. The bacterium is responsible for the synthesis of the small molecule pederin, which is a potent toxin of spiders (though apparently does not harm Pederea) (Kellner and Dettner, 1996; Kellner, 2001, 2002; Piel et al, 2004).
Although records of increased resistance to natural enemies dominate, secondary symbionts may also sometimes negatively affect the chance of para-sitization. Sodalis, a secondary symbiont residing in the gut epithelia, increases vector competence of its tsetse fly host, probably by altering the ability of trypanosome to establish in the midgut (Baker et al., 1990; Geiger et al, 2007). In Drosophila simulans, Wolbachia presence was associated with increased susceptibility to parasitoid infection (Fytrou et al., 2006). Infection with Wolbachia strain wVulC in the woodlouse Armadillidium vulgare is associated with lowered haemocyte density, and also increased titre of culturable bacteria (i.e. not Wolbachia) in the haemolymph, implying that infection was associated with immunosuppression (Braquart-Varnier et al., 2008). Reduced longevity associated with wVulC infection was also observed.
Notwithstanding these data, positive effects on resistance to natural enemies are probably of greatest importance. It is unlikely that secondary-symbiont-encoded resistance is limited to fungi, viruses, parasitoids, and predators. The resistance of secondary-symbiont-infected individuals to other natural enemies will be of interest. Resistance to entomopathogenic nematodes seems likely, given the ability of Photorhabdus to infect both nematodes and insects (and in effect be a secondary symbiont of nematodes), and interactions with other common natural enemies (such as microsporidia, and nucleopolyhedrosis viral infection) should also be investigated.
Perhaps the most fertile ground will be interaction with other bacterial infections. This is most likely to occur as a defence against infectiously transmitted pathogens rather than vertically transmitted symbionts, as in general vertically transmitted symbionts share a common 'desiderata' of mutual transmission. There are two reasons to believe it is likely that secondary symbionts will provide resistance to other bacteria. First, bacteria are well known for their ability to secrete a number of small antimicrobial molecules, such as colicins, to which they themselves are resistant (Cascales et al., 2007), and phage may also be more active in other bacterial hosts. The only requirement for these systems to play a role in secondary symbiosis is that these are induced in response to bacterial challenge of the host. Second, Photorhabdus
(which can be considered a secondary symbiont of nematodes) possesses an array of genes encoding defence against other bacteria, in this case to defend the corpse of its insect host against incursion from other microbes after it has killed it (Sharma et al., 2002; Duchaud et al., 2003).
Symbiont-mediated protection is a relatively recent discovery in host-parasite interactions. There are three clear lines of research for the future. First, how commonly is resistance to natural enemies mediated by symbionts? Second, how are the effects produced mechanistically, and are these exploitable? Third, what is the population and evolutionary ecology of these interactions?
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