Intragenomic conflict in populations infected by Parthenogenesis Inducing Wolbachia ends with irreversible loss of sexual reproduction

Abstract

Background: The maternally inherited, bacterial symbiont, parthenogenesis inducing (PI) Wolbachia, causes females in some haplodiploid insects to produce daughters from both fertilized and unfertilized eggs. The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased. Here we examine through models how an infection with PI-Wolbachia in a previously uninfected population leads to a genomic conflict between PI-Wolbachia and the nuclear genome. In most natural populations infected with PI-Wolbachia the infection has gone to fixation and sexual reproduction is impossible, specifically because the females have lost their ability to fertilize eggs, even when mated with functional males.

Results: The PI Wolbachia infection by itself does not interfere with the fertilization process in infected eggs, fertilized infected eggs develop into biparental infected females. Because of the increasingly female-biased sex ratio in the population during a spreading PI-Wolbachia infection, sex allocation alleles in the host that cause the production of more sons are rapidly selected. In haplodiploid species a reduced fertilization rate leads to the production of more sons. Selection for the reduced fertilization rate leads to a spread of these alleles through both the infected and uninfected population, eventually resulting in the population becoming fixed for both the PI-Wolbachia infection and the reduced fertilization rate. Fertilization rate alleles that completely interfere with fertilization ("virginity alleles") will be selected over alleles that still allow for some fertilization. This drives the final resolution of the conflict: the irreversible loss of sexual reproduction and the complete dependence of the host on its symbiont.

Conclusions: This study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.

Figure 1

Spread of PI-Wolbachia infection in a population and its effect on the population sex ratio. A. Solid curve: Increase of PI-Wolbachia infection in a population over time where initially 1% of the females are infected, the transmission efficiency of the Wolbachia (α) is set at 95%; there is no cost of being infected (ω = 1). All females are mated. Dashed curve: The fraction of uninfected females that are the offspring of infected mothers. B. The ratio of females to males in the population over the generations. Values were derived using equation 5 from the text.

Figure 2

Effect of PI-Wolbachia transmission efficiency and cost of infection on population sex ratio. The number of females per male in populations where the PI-Wolbachia infection is at equilibrium as a function of the relative fitness (offspring production) of the infected females (ω) and the Wolbachia transmission efficiency (α), when the egg fertilization rate is 0.5. Calculations were done using equation 7 from the text.

Figure 3

Spread and subsequent fixation of a low fertilization rate allele in a wild type population. At generation 1, a PI-Wolbachia infection enters the population in 1% of the females, while at the same time the mutant fertilization rate allele (with a fertilization rate of n = 0.3) is entered in 1% of the males. The PI-Wolbachia does not have any effect on the offspring production of the infected females (ω = 1) and has a transmission efficiency (α) of 95%. Genotypes: ++ = homozygote wildtype, nn = homozygote mutant and n+ = heterozygote. Male genotypes either + = wildtype or n = mutant. A. Frequency of Wolbachia infection in females; B. Frequency of genotypes among infected females (I), note only infected genotype frequencies are displayed.; C. Frequency of the mutant genotype among males, all plotted as a function of the number of generations.

Figure 4

Spread and subsequent fixation of a virginity mutant in a wild type population. Spread of the recessive mutant allele for fertilization rate of m = 0 ("virginity mutation") in a population with a wild type fertilization rate of x = 0.5. In generation 1 a PI-Wolbachia infection is entered in the population in 1% of the females, while at the same time the mutant fertilization rate allele is entered in 1% of the males. The PI-Wolbachia does not have any effect on the offspring production of the infected females (ω = 1) and has a transmission efficiency (α) of 95%. Calculations were done using the model described in additional file 1. A: Frequencies of the female genotypes for both infected (I) and uninfected (U) females, B: Frequencies of the male genotypes and C: Number of females in the population per male for all the female genotypes (nn, n+ and ++; solid line) and for those genotypes that are still fertilizing their eggs (n+ and ++; dotted line)

Figure 5

Speed of fixation for the virginity mutation when male mating capacity varies. The number of generations required for the recessive mutant allele for fertilization rate of n = 0 ("virginity mutation") to spread so that 99% of all females are infected and homozygous for the mutant (I_nn), when the number of females a male is capable of inseminating varies from 1 to 20 females. Calculations were done using the simulation model (additional file 1) with the following conditions: mutant sex ratio allele has a fertilization rate of n = 0 in a population with a wild type fertilization rate of x = 0.5. In generation 1 a PI-Wolbachia infection is entered in the population in 1% of the females, while at the same time the mutant sex ratio is entered in 1% of the males. The PI-Wolbachia does not have any effect on the offspring production of the infected females (ω = 1) and has a transmission efficiency (α) of 95%.

Figure 6

Mutant fertilization alleles can invade PI-Wolbachia infected populations even when they have a negative fitness effect in the homozygous state. When homozygosity for the recessive mutant allele n with a fertilization rate of m also carries a cost (s), the mutation can spread from rarity as long as the cost of homozygosity for the mutant and the fertilization frequency of the mutant within in the single hatched (simulation results) or in the double hatched area (simulation and analytical results). The mutant fertilization rate competes with a wildtype fertilization rate of x = 0.5. Other values: no cost of being infected (ω = 1), the Wolbachia transmission efficiency (α) equals 0.95.