Cytological analysis of cytoplasmic incompatibility induced by<i>Cardinium</i>suggests convergent evolution with its distant cousin<i>Wolbachia</i>

Abstract

Cytoplasmic incompatibility (CI) is a conditional sterility in numerous arthropods that is caused by inherited, intracellular bacteria such as <i>Wolbachia</i> Matings between males carrying CI-inducing <i>Wolbachia</i> and uninfected females, or between males and females infected with different <i>Wolbachia</i> strains, result in progeny that die during very early embryogenesis. Multiple studies in diploid (<i>Drosophila</i>) and haplodiploid (<i>Nasonia</i>) insects have shown that CI-<i>Wolbachia</i> cause a failure of the paternally derived chromatin from resolving into distinct chromosomes. This leads to the formation of chromatin bridges and other mitotic defects as early as the first mitotic division, and to early mitotic arrest. It is currently unknown if CI-inducing symbionts other than <i>Wolbachia</i> affect similar cellular processes. Here, we investigated CI caused by an unrelated bacterium, <i>Cardinium</i>, which naturally infects a parasitic wasp, <i>Encarsia suzannae</i> CI crosses in this host-symbiont system resulted in early mitotic defects including asynchrony of paternal and maternal chromosome sets as they enter mitosis, chromatin bridges and improper chromosome segregation that spanned across multiple mitotic divisions, triggering embryonic death through accumulated aneuploidy. We highlight small differences with CI-<i>Wolbachia</i>, which could be due to the underlying CI mechanism or host-specific effects. Our results suggest a convergence of CI-related cellular phenotypes between these two unrelated symbionts.