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.

Figure 1. Location of Drosophila simulans collection sites in eastern Australia and the frequency of infection by wAu and wRi in (A) 1994 (data adapted from Hoffmann et al. [33]), (B) 2004, (C) 2008 and (D) 2011/12.

Blue shaded parts of the pie are wAu-infected D. simulans, red shaded are wRi-infected and unshaded are uninfected individuals. Pie size represents sample size (n).

Figure 2. Fecundity assays on Australian wRi-infected, wAu-infected, and uninfected laboratory lines of D. simulans.

Mean number of eggs laid over 5 d by wRi-infected (red bar), uninfected (green bar) and wAu-infected (blue bar) females. Error bars are standard errors.

Figure 3. Predicted local wAu dynamics (where the infection increases host fitness (F _A) and offsets occasional loss of infection through maternal leakage) showing the observed increase in infection frequency between 1993/4 and 1999 assuming ∼20 host generations per annum at subtropical latitudes.

If the stable equilibrium frequency for wAu is ≈0.6, parameter combinations (a) and (b) are sufficient to explain the observed rate of increase, whereas combination (c) is not.

Figure 4. Predicted local dynamics for wAu displacement by wRi to account for the speed of change observed for both infections along coastal New South Wales between 2008 and 2011 (assuming ∼15 host generations per annum for temperate latitudes).

F _R (the fitness of wRi-infected hosts relative to uninfecteds) is predicted to be on the order of 1.08 or higher in a simple model (employing previously estimated parameter values of F _A = 1.061 and μ _A = 0.023 for wAu, and μ _R = 0.045 and H = 0.55 for wRi).