From Parasite to Mutualist: Rapid Evolution of Wolbachia in Natural Populations of Drosophila

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Abstract
Wolbachia are maternally inherited bacteria that commonly spread through host populations by causing cytoplasmic incompatibility, often expressed as reduced egg hatch when uninfected females mate with infected males. Infected females are frequently less fecund as a consequence of Wolbachia infection. However, theory predicts that because of maternal transmission, these “parasites” will tend to evolve towards a more mutualistic association with their hosts. Drosophila simulans in California provided the classic case of a Wolbachia infection spreading in nature. Cytoplasmic incompatibility allowed the infection to spread through individual populations within a few years and from southern to northern California (more than 700 km) within a decade, despite reducing the fecundity of infected females by 15%–20% under laboratory conditions. Here we show that the Wolbachia in California D. simulans have changed over the last 20 y so that infected females now exhibit an average 10% fecundity advantage over uninfected females in the laboratory. Our data suggest smaller but qualitatively similar changes in relative fecundity in nature and demonstrate that fecundity-increasing Wolbachia variants are currently polymorphic in natural populations. Wolbachia are endosymbiotic bacteria that live inside the cells of their invertebrate hosts. They are transmitted directly from mother to offspring, and spread through populations by manipulating the reproduction of their hosts. The most common reproductive manipulation responsible for the spread of these bacteria, called “cytoplasmic incompatibility,” arises when infected males mate with uninfected females, resulting in fewer offspring than normal. There are fitness costs for the hosts associated with Wolbachia infections, most commonly involving a reduction in egg production. Theory predicts that this detrimental effect of Wolbachia on its host should result in selection for the bacteria to evolve a more benign lifestyle, changing the bacterium from being parasitic to more mutualistic. We document such a shift in a Wolbachia infection of fruit flies (Drosophila simulans) from California. The shift occurred extremely rapidly, over 20 years. Consequently, Wolbachia-infected hosts now have higher rates of egg production than their uninfected counterparts. Changes in the genome of Wolbachia seem to be responsible for this, rather than changes in the host genome. Our study reveals that bacteria and their hosts represent components of a dynamic interacting system that can evolve rapidly over time.