Date Published: September 12, 2013
Publisher: Public Library of Science
Author(s): Peter Kriesner, Ary A. Hoffmann, Siu F. Lee, Michael Turelli, Andrew R. Weeks, Sylvain Charlat.
The maternally inherited intracellular bacteria Wolbachia can manipulate host reproduction in various ways that foster frequency increases within and among host populations. Manipulations involving cytoplasmic incompatibility (CI), where matings between infected males and uninfected females produce non-viable embryos, are common in arthropods and produce a reproductive advantage for infected females. CI was associated with the spread of Wolbachia variant wRi in Californian populations of Drosophila simulans, which was interpreted as a bistable wave, in which local infection frequencies tend to increase only once the infection becomes sufficiently common to offset imperfect maternal transmission and infection costs. However, maternally inherited Wolbachia are expected to evolve towards mutualism, and they are known to increase host fitness by protecting against infectious microbes or increasing fecundity. We describe the sequential spread over approximately 20 years in natural populations of D. simulans on the east coast of Australia of two Wolbachia variants (wAu and wRi), only one of which causes significant CI, with wRi displacing wAu since 2004. Wolbachia and mtDNA frequency data and analyses suggest that these dynamics, as well as the earlier spread in California, are best understood as Fisherian waves of favourable variants, in which local spread tends to occur from arbitrarily low frequencies. We discuss implications for Wolbachia-host dynamics and coevolution and for applications of Wolbachia to disease control.
The vertically-transmitted intracellular bacterium Wolbachia may be the most widespread – and evolutionarily significant endosymbiont ,  of insects and other arthropods. Wolbachia induce many reproductive manipulations within hosts that increase their chance of spreading through females. Their ability to suppress other microbes in their hosts provides a novel method to control human vector-borne diseases such as dengue ,  and malaria , . Yet despite their ubiquity and potential importance in vector-borne disease control, there are few documented examples of Wolbachia infections spreading in natural host populations , .
Despite the ubiquity of Wolbachia in natural populations of arthropods, there are very few documented examples of Wolbachia spread , . This has limited our understanding of Wolbachia spatial dynamics, with bistable spread for CI-causing Wolbachia suggested by imperfect maternal Wolbachia transmission by wild-caught females ,  and demonstrated fecundity costs for infected females in the laboratory , , . However, bistable dynamics cannot explain the persistence of Wolbachia that cause little or no reproductive manipulation . Moreover, as emphasized by Fenton et al. , bistable dynamics are difficult to reconcile with molecular data indicating that the widespread occurrence of Wolbachia is attributable to rare horizontal transmission events involving one or very few infected founders , , , . These phenomena are more easily explained by Fisherian dynamics , in which the frequency dynamics of rare Wolbachia infections are dominated by positive fitness effects. Our temporal and spatial data, describing the sequential spread of two Wolbachia strains (wAu and wRi) through natural populations of D. simulans along the east coast of Australia over the last two decades, support the view that both strains may have spread under Fisherian dynamics.