Abstract
Symbionts can have mutualistic effects that increase their host’s fitness and/or parasitic effects that reduce it. Which of these strategies evolves depends in part on the balance of their costs and benefits to the symbiont. We have examined these questions in Wolbachia, a vertically transmitted endosymbiont of insects that can provide protection against viral infection and/or parasitically manipulate its hosts’ reproduction. Across multiple symbiont strains we find that the parasitic phenotype of cytoplasmic incompatibility and antiviral protection are uncorrelated. Strong antiviral protection is associated with substantial reductions in other fitness-related traits, whereas no such trade-off was detected for cytoplasmic incompatibility. The reason for this difference is likely that antiviral protection requires high symbiont densities but cytoplasmic incompatibility does not. These results are important for the use of Wolbachia to block dengue virus transmission by mosquitoes, as natural selection to reduce these costs may lead to reduced symbiont density and the loss of antiviral protection.
Highlights
Heritable symbionts are frequent in insects and their evolutionary success relies on various strategies
Arthropods are commonly infected with heritable bacteria, and some of these symbionts can protect their hosts against infection and/or be reproductive parasites
Using a panel of strains of the symbiont Wolbachia in the fruit fly Drosophila simulans, we found that the beneficial effect of antiviral protection and the parasitic phenotype of cytoplasmic incompatibility occur independently across the strains
Summary
Heritable symbionts are frequent in insects and their evolutionary success relies on various strategies. By sharing a common route of transmission with their host’s genes, they benefit from increasing host fitness. Because most of these heritable bacteria are maternally-transmitted, the evolutionary interests of host and symbiont are not perfectly aligned since only females transmit the symbiont. This has led to many symbionts evolving selfish strategies that consist of parasitic manipulation of their host’s reproduction by inducing female-biased sex-ratios or cytoplasmic incompatibility (CI) [10]. The balance between the benefits and costs of these extended phenotypes to the symbiont’s fitness, as well as the genetic correlations between them, will determine which of these strategies is favoured by natural selection
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