Rapid Sequential Spread of Two Wolbachia Variants in Drosophila simulans

Abstract

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. Wolbachia are bacteria that live within the cells of arthropod hosts and are widespread in many groups of insects. These bacteria can rapidly spread through a population through a process of cytoplasmic incompatibility whereby females uninfected by Wolbachia show embryo death when they mate with males carrying the bacteria. Because the infected females pass on Wolbachia to their offspring, this places them at a reproductive advantage, ensuring that the infection spreads through insect populations once it reaches a high enough frequency to overcome any negative fitness effects on its host. Yet while such a rapid spread has been predicted, it has rarely been observed in nature. Here we show that a Wolbachia infection of Drosophila simulans flies has spread very rapidly in eastern Australia, replacing another Wolbachia infection that has also spread in recent years. These invasions appear to have taken place from a very low frequency, implying that both infections are likely to have had a benefit to their hosts rather than a cost. These results have implications for the spread of Wolbachia infections currently being introduced into populations of mosquitoes and other insects for disease suppression.