A re-examination of Wolbachia-induced cytoplasmic incompatibility in California Drosophila simulans.

Lauren B Carrington,Ary A Hoffmann,Jeremy R Lipkowitz,Michael Turelli,Richard Cordaux

doi:10.1371/journal.pone.0022565

Lauren B Carrington, Ary A Hoffmann + Show 3 more

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https://doi.org/10.1371/journal.pone.0022565

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Journal: PloS one	Publication Date: Jul 25, 2011
Citations: 45	License type: CC BY 4.0

Affiliation: University of California, Davis, University of Melbourne

Abstract

BackgroundIn California Drosophila simulans, the maternally inherited Riverside strain Wolbachia infection (wRi) provides a paradigm for rapid spread of Wolbachia in nature and rapid evolutionary change. wRi induces cytoplasmic incompatibility (CI), where crosses between infected males and uninfected females produce reduced egg-hatch. The three parameters governing wRi infection-frequency dynamics quantify: the fidelity of maternal transmission, the level of cytoplasmic incompatibility, and the relative fecundity of infected females. We last estimated these parameters in nature in 1993. Here we provide new estimates, under both field and laboratory conditions. Five years ago, we found that wRi had apparently evolved over 15 years to enhance the fecundity of infected females; here we examine whether CI intensity has also evolved.Methodology/Principal FindingsNew estimates using wild-caught flies indicate that the three key parameters have remained relatively stable since the early 1990s. As predicted by our three-parameter model using field-estimated parameter values, population infection frequencies remain about 93%. Despite this relative stability, laboratory data based on reciprocal crosses and introgression suggest that wRi may have evolved to produce less intense CI (i.e., higher egg hatch from incompatible crosses). In contrast, we find no evidence that D. simulans has evolved to lower the susceptibility of uninfected females to CI.Conclusions/SignificanceEvolution of wRi that reduces CI is consistent with counterintuitive theoretical predictions that within-population selection on CI-causing Wolbachia does not act to increase CI. Within taxa, CI is likely to evolve mainly via pleiotropic effects associated with the primary targets of selection on Wolbachia, i.e., host fecundity and transmission fidelity. Despite continuous, strong selection, D. simulans has not evolved appreciably to suppress CI. Our data demonstrate a lack of standing genetic variation for CI resistance in the host.

Highlights

Wolbachia are maternally inherited intracellular bacteria found in many – and perhaps most – arthropods [1]
The four sets of crosses undertaken in both assays were identical: (1) 200 field males mated to W88 females on the first day, mated to R88 females on the second day; (2) 50 field males mated to W88 females on two successive days to test the effects of remating on cytoplasmic incompatibility (CI) [17,18]; (3) 20 W88 males mated to W88 females on the first day and Riv88 females on the second day to determine whether egg hatch from compatible crosses depended significantly on the origin of the uninfected male; and (4) a second group of 10 W88 males mated to W88 females on two successive days
When all crosses are compared by a Kruskal-Wallis test including those that produced sufficient offspring on either day 1 or day 2, there was no difference in CI between the three sets of compatible crosses involving field males (X2 = 0.37, df = 2, P = 0.831); these consisted of uninfected males mated to uninfected or infected females (73%, N = 9) and infected males mated to infected females (80%, N = 131)

Summary

Introduction

Wolbachia are maternally inherited intracellular bacteria found in many – and perhaps most – arthropods [1]. The reciprocal cross produced significantly more progeny, comparable to the number produced by infected pairs or uninfected pairs This cytoplasmically inherited incompatibility was associated with Wolbachia, first microscopically [3], via PCR [4]. In California Drosophila simulans, the maternally inherited Riverside strain Wolbachia infection (wRi) provides a paradigm for rapid spread of Wolbachia in nature and rapid evolutionary change. The three parameters governing wRi infection-frequency dynamics quantify: the fidelity of maternal transmission, the level of cytoplasmic incompatibility, and the relative fecundity of infected females. We last estimated these parameters in nature in 1993. We found that wRi had apparently evolved over 15 years to enhance the fecundity of infected females; here we examine whether CI intensity has evolved

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