Abstract
BackgroundThe 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.ResultsThe 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.ConclusionsThis 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.
Highlights
The maternally inherited, bacterial symbiont, parthenogenesis inducing (PI) Wolbachia, causes females in some haplodiploid insects to produce daughters from both fertilized and unfertilized eggs
Models We model the spread of a PI-Wolbachia infection in an initially uninfected population
The simulations were initiated with a wild type population into which we introduced a PIWolbachia infection at a 1% frequency among the females (frequency of infected (I) wildtype (++) females I++ = 0.01, frequency of uninfected (U) wildtype (++) females U++ = 0.99, with all other female genotypes at zero; see additional file 1) and a recessive fertilization mutant n at a frequency of 1% in the males (Mn = 0.01, M+ = 0.99)
Summary
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, the optimal sex ratio for the nuclear genome is more male-biased. Other cytoplasmically inherited genetic elements include endosymbiotic bacteria that are common in many arthropods In many cases such symbionts cause female-biased offspring sex ratio by several means: either transforming genetic males into females (feminization [6]), killing male offspring [7] or by inducing parthenogenesis [8]. Resistance to male-killing in this system has been shown [19] and a rapid invasion of populations infected with the male killer by these suppressor genes was recently observed [20]
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