Interacting host modifier systems control Wolbachia-induced cytoplasmic incompatibility in a haplodiploid mite

Many reproductive parasites such as Wolbachia spread within host populations by inducing cytoplasmic incompatibility (CI). CI occurs when parasite-modified sperm fertilizes uninfected eggs. In haplodiploid hosts, CI can lead to different phenotypes depending on whether the fertilized eggs die or develop into males. Genetic conflict theories predict the evolution of host modulation of CI, which in turn strongly influences the stability of reproductive parasitism. Yet, despite the ubiquity of CI-inducing parasites in nature, there is no conclusive evidence for strong intraspecific host modulation of CI strength and phenotype. Here, we tested for intraspecific host modulation of Wolbachia-induced CI in haplodiploid Tetranychus spider mites. Using a single CI-inducing Wolbachia variant and mitochondrion, a Tetranychus urticae nuclear panel was created that consisted of infected and cured near-isogenic lines. We performed a highly replicated age-synchronized full diallel cross comprised of incompatible and compatible control crosses. We uncovered host modifier systems that strongly suppress CI strength when carried by infected T. urticae males. Interspecific crosses showed that the male modifier systems suppress CI strength across species boundaries. We also observed a continuum of CI phenotypes in our crosses and identified strong intraspecific female modulation of CI phenotype when paired with a specific male genotype. Crosses established a recessive genetic basis for the maternal effect and were consistent with polygenic Mendelian inheritance. Our findings identify spermatogenesis as an important target of selection for host suppression of CI strength and underscore the importance of maternal genetic effects for the CI phenotype. Both mechanisms interacted with the genotype of the mating partner, revealing that intraspecific host modulation of CI strength and phenotype is underpinned by complex genetic architectures.