From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila

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.

Figure 1. Fecundity Assays on Infected and Uninfected Isofemale Lines of D. simulans Collected from California in 2002 and 2004

(A) Mean number of eggs over 5 d laid by infected (black bars) and uninfected (white bars) lines collected at Riverside in 2002 and 1988. The 2002 lines were assayed four generations after collection. A significant overall increase in fecundity was associated with the infection (F _1,108 = 6.7, p = 0.011). (B) Mean number of eggs over 5 d laid by infected (black) and uninfected (white) lines collected at Riverside in 2002 and assayed 10 mo after collection. These flies were cultured on a yeast-restricted diet. Again, the infection produced a significant overall increase in fecundity (F _1,213 = 5.8, p = 0.017). (C) Mean number of eggs over 10 d laid by infected (black) and uninfected (white) lines collected at Irvine in 2004 and assayed five generations after collection. Infection status had a significant effect on fecundity (F _1,185 = 8.03, p = 0.005). Error bars are standard errors, and asterisks indicate significant differences at the 5% level.

Figure 2. Effects of Wolbachia Strain and Nuclear Background on 10-d Fecundity of D. simulans

The nuclear background (normal text) and Wolbachia strain (superscript text) are for flies collected in Riverside in 1988 (Riv88) or Irvine in 2004 (IR2). Error bars are standard errors. Different letters indicate significantly different means (at the 5% level).

Figure 3. Effects of Wolbachia Strain on 10-d Fecundity of D. simulans Collected at Irvine in 2004 and Backcrossed for Two Generations to Males from Riverside Collected in 1988

Error bars are standard errors.

Figure 4. Levels of CI Induced by Wolbachia-Infected D. simulans Males 5, 10, and 15 d Post-Eclosion When Mated to Uninfected Females

Isofemale lines originated from California in 1988 (hatched bars), 1999 (grey bars), and 2002 (white bars). Error bars are 95% confidence intervals.

Figure 5. Effects of Changes in Parameters for Various Values of F

(A) Assuming μ = 0.04, the solid line shows the value of H needed to produce p̂ = 0.90, and the dashed line shows the value of H needed to produce p̂ = 0.94. (B) Assuming H = 0.55, the solid line shows the value of μ needed to produce p̂ = 0.90, and the dashed line shows the value of μ needed to produce p̂ = 0.94. (C) Assuming H = 0.55 and μ = 0.045 (dashed line) or μ = 0.0225 (solid line), this shows how p̂ changes.

Figure 6. Selection Intensity Needed to Explain a Transient Polymorphism

Intensity of selection, s, needed to explain a current frequency of 0.8 (solid line), 0.4 (short-dashed line), or 0.1 (long-dashed line) as a function of the initial allele frequency measured in units of log₁₀, assuming equation 1.

Figure 7. Time Required for a Favoured Variant to Spread

Number of generations required for a favoured variant to go from an initial frequency of 0.001 to a final frequency of 0.1 (long-dashed line), 0.5 (short-dashed line), or 0.9 (solid line) as a function of the intensity of selection, s, assuming equation 1.