Animals are increasingly understood to be complex cellular conglomerates. While some parts are derived from the genome of the host organism, the rest comprises microbial symbionts. In the best of cases, these pieces of the puzzle form tight partnerships that provide mutual benefits. However, because symbionts can also be a burden, it is sometimes useful for hosts to go it alone. But what if evicting symbionts makes things worse? In these cases, can hosts become addicted to their microbial passengers? In a fascinating new report in the Proceedings of the Royal Society, Series B, Julien Martinez and colleagues from the University of Cambridge, UK, describe just such an outcome.
Wolbachia bacteria are ubiquitous in insects and infect more than half of all species. While best known as manipulators of insect reproduction, these bacteria can also play defensive roles for their insect hosts. In Drosophila, they provide protection against the highly lethal fly virus Drosophila C virus (DCV). However, flies can also become resistant to DCV without Wolbachia via mutations in their genomes at a single gene called pastrel. If you can have one mode of resistance, why keep both? This is particularly true for Wolbachia, whose carriage can be highly costly to flies. And if you do carry Wolbachia, how does this affect the evolution of pastrel?
To address these questions the team established two groups of flies that were identical except for the presence or absence of Wolbachia symbionts. They then infected flies from these treatments with DCV. As expected, fewer flies with the bacterial symbiont died than those without it. Some flies without Wolbachia, however, survived, and this minority overwhelmingly carried mutations at the pastrel locus. By contrast, pastrel mutations in the Wolbachia flies remained at very low levels. This result indicated that, at least in the short term, bacterial symbionts suppressed the evolution of host resistance. But what about in the longer term?
Martinez and his colleagues next reared both groups of DCV-infected flies through nine generations. Although viral resistance increased in both fly groups, the effects on pastrel mutations were dramatically different. While pastrel mutations rapidly increased in frequency in the flies lacking Wolbachia, becoming fixed in these populations, the ascent of mutations in the gene was markedly slower in flies harbouring the symbiont. More strikingly, the group estimated that while DCV imposed very strong natural selection to increase the frequency of pastrel mutations in the no-symbiont group, this was almost entirely absent in flies carrying Wolbachia. In short, Wolbachia carriage arrested the evolution of genomic mutations for DCV resistance.
So why is Wolbachia an addiction? Simply, because flies carrying costly bacterial symbionts suspend fighting DCV on their own. Thus, when DCV is common, Wolbachia-mediated protection might become the only form of protection available, despite the fact that pastrel mutations could do just as well at much lower cost. At present, the authors are not sure if this result extends to other defensive symbionts. It is also unclear whether this type of addiction occurs with symbionts playing non-defensive roles in other animals or plants. More generally, is this the selfish route by which transient symbionts become permanent? If so, it would suggest that the alliance between animals and microbes is not always a simple one and that even highly mutualistic interactions between microbial symbionts and hosts may have coercive origins.
