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.

Reproductive Parasitism: Maternally Inherited Symbionts in a Biparental World

“…Spatial waves of advance of CI symbionts have been observed on multiple occasions (Turelli and Hoffmann 1991;Hoshizaki and Shimada 1995;Kriesner et al 2013), indicating that there are ongoing and repeated waves of symbiont spread in insects. The ability to drive rapidly to high prevalence is useful in that it potentiates Wolbachia-mediated control- of-vector competence following introduction (Walker et al 2011;Yeap et al 2011).…”

Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

“…An excellent example of this is presented by Kriesner et al (2013) on the Australian coastal populations of D. simulans. Historically, Australian D. simulans harbored the non-CI inducing Wolbachia strain wAu, at frequencies lower than 0.3.…”

Larval Competition Extends Developmental Time and Decreases Adult Size of wMelPop Wolbachia-Infected Aedes aegypti

“…4,5 The reproductive manipulation induced by Wolbachia enables the infection to proliferate rapidly, potentially leading to replacement of naturally uninfected populations. [6][7][8] Although many mosquito species are infected with Wolbachia, the container-breeding Aedes aegypti, the principal dengue vector, does not harbor a natural Wolbachia infection. 9 The wMelPop and wMel strains of Wolbachia, originally from Drosophila melanogaster, have been artificially transinfected into Ae.…”