Most symbionts are actually beneficial, but not essential, and many have multiple impacts on their host
In our paper in 2008, we started from the premise that the bacteria we were studying were parasites of arthropod reproductive systems that spread using sex ratio distortion or cytoplasmic incompatibility as drive mechanisms. However, we noted that, in most cases, the nature of the interactions between these inherited bacteria (including Wolbachia) and their hosts was not known, and thus remained to be determined.
It is now clear that the heritable microorganisms we studied are not simply reproductive parasites. Wolbachia in arthropods has emerged as a conditional mutualist conferring advantages under certain environmental conditions. For instance,
Wolbachia increases fecundity of Drosophila melanogaster reared on iron-restricted or -overloaded diets, and can thus confer a direct fitness benefit during periods of nutritional stress [2]. The most dramatic findings are that Wolbachia can protect their hosts against attack by natural enemies. Wolbachia infection interferes with the replication and transmission of a wide range of pathogens and parasites (including RNA viruses, bacteria, protozoa and nematodes), and protects its host from parasite-induced mortality [3]. These properties have led to Wolbachia being developed as an agent to limit transmission of human pathogens by arthropod vectors [4].
Wolbachia is not alone in being a defensive symbiont. Diverse symbionts in aphids provide protection against parasitic wasp and fungal attack, and include members of the Rickettsia and Spiroplasma genera [5, 6]. Drosophila, an organism intensively studied with respect to determinants of resistance to parasites, was recently revealed to have defensive Spiroplasma [7]. Paederus rove beetles carry heritable Pseudomonas that produces a toxin that deters predators [8]. Apart from protective effects, symbionts mediate variation in heat tolerance, plant use and body color [5, 9]. For instance, the symbiont Rickettsiella changes the body color of the aphid host from red to green, and is thus likely to influence relative susceptibility to predators [9].
It is also now clear that individual symbionts have multiple properties. For instance, the Wolbachia strain in D. melanogaster was characterized initially as one producing only weak reproductive manipulation but is now also known to confer nutritional and protective benefits. Similarly, Himler et al. [10] found that Rickettsia infection in whiteflies both increased host survival and reproductive success, and biased the sex ratio towards production of daughters, a classical feature of reproductive parasites. The further observation that some symbiont effects are revealed only in novel hosts suggests multiple potencies may be common [11]. Multiple effects on the host are also very important in the application of heritable microbes in disease control. The reproductive parasitism of Wolbachia allows it to invade and be maintained at high frequency in a population, such that the effect it has on the competence of individuals to act as disease-carrying vectors is then observed at a population scale [4].