Abstract
Cytoplasmic incompatibility is a selfish reproductive manipulation induced by the endosymbiont Wolbachia in arthropods. In males Wolbachia modifies sperm, leading to embryonic mortality in crosses with Wolbachia-free females. In females, Wolbachia rescues the cross and allows development to proceed normally. This provides a reproductive advantage to infected females, allowing the maternally transmitted symbiont to spread rapidly through host populations. We identified homologs of the genes underlying this phenotype, cifA and cifB, in 52 of 71 new and published Wolbachia genome sequences. They are strongly associated with cytoplasmic incompatibility. There are up to seven copies of the genes in each genome, and phylogenetic analysis shows that Wolbachia frequently acquires new copies due to pervasive horizontal transfer between strains. In many cases, the genes have subsequently acquired loss-of-function mutations to become pseudogenes. As predicted by theory, this tends to occur first in cifB, whose sole function is to modify sperm, and then in cifA, which is required to rescue the cross in females. Although cif genes recombine, recombination is largely restricted to closely related homologs. This is predicted under a model of coevolution between sperm modification and embryonic rescue, where recombination between distantly related pairs of genes would create a self-incompatible strain. Together, these patterns of gene gain, loss, and recombination support evolutionary models of cytoplasmic incompatibility.
Highlights
Maternally-transmitted bacteria in the genus Wolbachia commonly manipulate the reproduction of their arthropod hosts by inducing cytoplasmic incompatibility (CI)
CI is the most commonly observed reproductive manipulation induced by Wolbachia, and its evolution has been investigated for over sixty years through phenotypic experiments (Laven 1957; Sinkins et al 1995; Charlat et al 2003; Zabalou et al 2008) and evolutionary models
We analysed 71 Wolbachia genome sequences to investigate the importance of recombination, pseudogenization and horizontal gene transfer in the evolution of CI
Summary
Maternally-transmitted bacteria in the genus Wolbachia commonly manipulate the reproduction of their arthropod hosts by inducing cytoplasmic incompatibility (CI). A certain threshold in Wolbachia frequency, CI allows the infection to rapidly spread in the host population, even if it induces moderate fitness costs (Turelli et al 1992) This is thought to have contributed to the remarkable evolutionary success of Wolbachia, which is estimated to infect around half of terrestrial arthropod species (Weinert et al 2015). When the male and female parents are infected with different Wolbachia strains, it is common to find that the cross is incompatible (bidirectional CI) (O’Neill and Karr 1990; Bordenstein et al 2001; Atyame et al 2014) This suggests the modification and rescue factors must match each other for development to proceed normally (Poinsot et al 2003)
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