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.

Highlights

  • When microbes that live within animal cells are transmitted only maternally, their reproductive success is directly tied to that of the matrilines they inhabit

  • Our study reveals that bacteria and their hosts represent components of a dynamic interacting system that can evolve rapidly over time

  • Fecundity Effects in the Laboratory Apart from the viability effects associated with Cytoplasmic incompatibility (CI), female fecundity is the only fitness component known to be affected by the Drosophila simulans Wolbachia (wRi) infection in California D. simulans [9]

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Summary

Introduction

When microbes that live within animal cells are transmitted only maternally, their reproductive success is directly tied to that of the matrilines they inhabit Both intuition and mathematics suggest that such endosymbionts will be selected towards mutualism, if possible, increasing the fecundity of their female hosts [1]. Mutualisms generally have long evolutionary histories, but given the potentially explosive rate of bacterial evolution [3], rapid evolution of mutualisms in nature might be expected. We report such evolution by bacteria (Wolbachia) associated with a dipteran host (Drosophila simulans) in natural California populations. In less than 20 y, the Wolbachia in California D. simulans have changed so that infected females produce more eggs than uninfected females under laboratory conditions, whereas infected females previously suffered a significant fecundity deficit

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